生物学（英文版）：3

419 Catching evolution in action A hundred years ago Charles Darwin’s theory of evolution by natural selection was taught as the foundation of biology in public schools throughout the United States. Then something happened. In the 1920s, conservative religious groups began to argue against the teaching of evolution in our nation's schools. Darwinism, they said, contradicted the revealed word of God in the Bible and thus was a direct attack on their religious beliefs. Many of you will have read about the 1925 Scopes "monkey trial" or seen the move about it, Inherit the Wind. In the backwash of this contro- versy, evolution for the first time in this century disap- peared from the schools. Textbook publishers and local school boards, in a wish to avoid the dispute, simply chose not to teach evolution. By 1959, 100 years after Darwin's book, a famous American geneticist cried in anguish, "A hundred years without Darwin is enough!" What he meant was that the theory of evolution by natural selection has be- come the central operating concept of the science of biol- ogy, organic evolution being one of the most solidly vali- dated facts of science. How could we continue to hide this truth from our children, crippling their understanding of science? In the 1970s, Darwin reappeared in our nation's schools, part of the wave of concern about science that followed Sputnik. Not for long, however. Cries from creationists for equal time in the classroom soon had evolution out of our classrooms again. Only in recent years, amid considerable uproar, have states like California succeeded in reforming their school curriculums, focusing on evolution as the cen- tral principle of biology. In other states, teaching Darwin remains controversial. While Darwin’s proposal that evolution occurs as the result of natural selection remains controversial in many local school boards, it is accepted by practically every biol- ogist who has examined it seriously. In this section, we will review the evidence supporting Darwin’s theory. Evolu- tionary biology is unlike most other fields of biology in which hypotheses are tested directly with experimental methods. To study evolution, we need to investigate what happened in the past, sometimes many millions of years ago. In this way, evolutionary biology is similar to astron- omy and history, relying on observation and deduction rather than experiment and induction to examine ideas about past events. Nonetheless, evolutionary biology is not entirely an ob- servational science. Darwin was right about many things, but one area in which he was mistaken concerns the pace at which evolution occurs. Darwin thought that evolution occurred at a very slow, almost imperceptible, pace. How- ever, in recent years many case studies of natural popula- tions have demonstrated that in some circumstances evolu- tionary change can occur rapidly. In these instances, it is possible to establish experimental studies to directly test evolutionary hypotheses. Although laboratory studies on fruit flies and other organisms have been common for more than 50 years, it has only been in recent years that scientists have started conducting experimental studies of evolution in nature. To conduct experimental tests of evolution, it is first nec- essary to identify a population in nature upon which strong selection might be operating (see above). Then, by manipu- lating the strength of the selection, an investigator can pre- dict what outcome selection might produce, then look and see the actual effect on the population. Part VI Evolution The evolution of protective coloration in guppies. In pools below waterfalls where predation is high, guppies are drab colored. In the absence of the highly predatory pike cichlid, guppies in pools above waterfalls are much more colorful and attractive to females. The evolution of these differences can be experimentally tested. 420 Part VI Evolution The Experiment Guppies offer an excellent experimental opportunity. The guppy, Poecilia reticulata, is found in small streams in north- eastern South America and the nearby island of Trinidad. In Trinidad, guppies are found in many mountain streams. One interesting feature of several streams is that they have waterfalls. Amazingly, guppies are capable of colonizing portions of the stream above the waterfall. During flood seasons, rivers sometimes overflow their banks, creating secondary channels that move through the forest. During these occasions, guppies may be able to move upstream and invade pools above waterfalls. By contrast, not all species are capable of such dispersal and thus are only found in these streams below the first waterfall. One species whose distribution is restricted by waterfalls is the pike cichlid, Crenicichla alta, a voracious predator that feeds on other fish, including guppies. Because of these barriers to dispersal, guppies can be found in two very different environments. In pools just below the waterfalls, predation is a substantial risk and rates of survival are relatively low. By contrast, in similar pools just above the waterfall, few predators prey on guppies. As a result, guppy populations above and below waterfalls have evolved many differences. In the high-predation pools, guppies exhibit drab coloration. Moreover, they tend to re- produce at a younger age. The differences suggest the action of natural selection. Perhaps as a result of shunting energy to reproduction rather than growth, the fish in high-predation pools attain relatively smaller adult sizes. By contrast, male fish above the waterfall display gaudy colors that they use to court fe- males. Adults there mature later and grow to larger sizes. Although the differences between guppies living above and below the waterfalls are consistent with the hypothesis that they represent evolutionary responses to differences in the strength of predation, alternative explanations are pos- sible. Perhaps, for example, only very large fish are capable of moving past the waterfall to colonize pools. If this were the case, then a founder effect would occur in which the new population was established solely by individuals with genes for large size. The only way to rule out such alternative possibilities is to conduct a controlled experiment. The first experiments were conducted in large pools in laboratory greenhouses. At the start of the experiment, a group of 2000 guppies were divided equally among 10 large pools. Six months later, pike cichlids were added to four of the pools and killi- fish (which rarely prey on guppies) to another four, with the remaining pools left as “no predator” controls. The Results Fourteen months later (which corresponds to 10 guppy generations), the scientists compared the populations. The guppies in the killifish and control pools were indistin- guishable, brightly colored and large. In contrast, the gup- pies in the pike cichlid pools were smaller and drab in col- oration. These results established that predation can lead to rapid evolutionary change, but does this laboratory experi- ments reflect what occurs in nature? To find out, scientists located two streams that had gup- pies in pools below a waterfall, but not above it. As in other Trinidadian streams, the pike cichlid was present in the lower pools, but only the killifish was found above the wa- terfalls. The scientists then transplanted guppies to the upper pools and returned at several-year intervals to moni- tor the populations. Despite originating from populations in which predation levels were high, the transplanted popu- lations rapidly evolved the traits characteristic of low-pre- dation guppies: they matured late, attained greater size and brighter colors. Control populations in the lower pools, by contrast, continued to mature early and at smaller size. These results demonstrate that substantial evolutionary change can occur in less than 12 years. To explore this concept further go to our interactive lab at www.mhhe.com/raven6e Evolutionary change in spot number. Populations transported to the low-predation environment quickly increased in number of spots, whereas selection in more dangerous environments, like the predator-filled pool above right, led to less conspicuous fish. 421 20 Genes within Populations Concept Outline 20.1 Genes vary in natural populations. Gene Variation Is the Raw Material of Evolution. Selection acts on the genetic variation present in populations, favoring variants that increase the likelihood of survival and reproduction. Gene Variation in Nature. Natural populations contain considerable amounts of variation, present at the DNA level and expressed in proteins. 20.2 Why do allele frequencies change in populations? The Hardy–Weinberg Principle. The proportion of homozygotes and heterozygotes in a population is not altered by meiosis or sexual reproduction. Five Agents of Evolutionary Change. The frequency of alleles in a population can be changed by evolutionary forces like gene flow and selection. Identifying the Evolutionary Forces Maintaining Polymorphism. A number of processes can influence allele frequencies in natural populations, but it is difficult to ascertain their relative importance. Heterozygote Advantage.—In some cases, heterozygotes are superior to either type of homozygote. The gene for sickle cell anemia is one particularly well-understood example. 20.3 Selection can act on traits affected by many genes. Forms of Selection. Selection can act on traits like height or weight to stabilize or change the level at which the trait is expressed. Limits to What Selection Can Accomplish. Selection cannot act on traits with little or no genetic variation. N o other human being is exactly like you (unless you have an identical twin). Often the particular charac- teristics of an individual have an important bearing on its survival, on its chances to reproduce, and on the success of its offspring. Evolution is driven by such consequences. Genetic variation that influences these characteristics pro- vides the raw material for natural selection, and natural populations contain a wealth of such variation. In plants (figure 20.1), insects, and vertebrates, practically every gene exhibits some level of variation. In this chapter, we will ex- plore genetic variation in natural populations and consider the evolutionary forces that cause allele frequencies in nat- ural populations to change. These deceptively simple mat- ters lie at the core of evolutionary biology. FIGURE 20.1 Genetic variation. The range of genetic material in a population is expressed in a variety of ways—including color. in the genetic makeup of populations. Allele frequencies can also change as the result of repeated mutations from one allele to another and from migrants bringing alleles into a population. In addition, when populations are small, the frequencies of alleles can change randomly as the result of chance events. Evolutionary biologists debate the rela- tive strengths of these processes. Although no one denies that natural selection is a powerful force leading to adaptive change, the importance of other processes is less certain. Darwin proposed that natural selection on variants within populations leads to the evolution of different species. 422 Part VI Evolution Gene Variation Is the Raw Material of Evolution Evolution Is Descent with Modification The word “evolution” is widely used in the natural and so- cial sciences. It refers to how an entity—be it a social sys- tem, a gas, or a planet—changes through time. Although development of the modern concept of evolution in biology can be traced to Darwin’s On the Origin of Species, the first five editions of this book never actually used the term! Rather, Darwin used the phrase “descent with modifica- tion.” Although many more complicated definitions have been proposed, Darwin’s phrase probably best captures the essence of biological evolution: all species arise from other, pre-existing species. However, through time, they accumu- late differences such that ancestral and descendant species are not identical. Natural Selection Is an Important Mechanism of Evolutionary Change Darwin was not the first to propose a theory of evolution. Rather, he followed a long line of earlier philosophers and naturalists who deduced that the many kinds of organisms around us were produced by a process of evolution. Un- like his predecessors, however, Darwin proposed natural selection as the mechanism of evolution. Natural selec- tion produces evolutionary change when in a population some individuals, which possess certain inherited charac- teristics, produce more surviving offspring than individu- als lacking these characteristics. As a result, the popula- tion will gradually come to include more and more individuals with the advantageous characteristics. In this way, the population evolves and becomes better adapted to its local circumstances. Natural selection was by no means the only evolution- ary mechanism proposed. A rival theory, championed by the prominent biologist Jean-Baptiste Lamarck, was that evolution occurred by the inheritance of acquired characteristics. According to Lamarck, individuals passed on to offspring body and behavior changes ac- quired during their lives. Thus, Lamarck proposed that ancestral giraffes with short necks tended to stretch their necks to feed on tree leaves, and this extension of the neck was passed on to subsequent generations, leading to the long-necked giraffe (figure 20.2a). In Darwin’s the- ory, by contrast, the variation is not created by experi- ence, but is the result of preexisting genetic differences among individuals (figure 20.2b). Although the efficacy of natural selection is now widely accepted, it is not the only process that can lead to changes 20.1 Genes vary in natural populations. Proposed ancestor of giraffes has characteristics of modern-day okapi. The giraffe ancestor lengthened its neck by stretching to reach tree leaves, then passed the change to offspring. (a) Lamarck's theory: variation is acquired. stretching stretching reproduction reproduction reproduction reproduction Individuals are born who happen to have longer necks. Over many generations, longer-necked individuals are more successful and pass the long-neck trait on to their offspring. growth to adult growth to adult (b) Darwin's theory: variation is inherited. FIGURE 20.2 How did giraffes evolve a long neck? Gene Variation in Nature Evolution within a species may result from any process that causes a change in the genetic composition of a population. In considering this theory of population genetics, it is best to start by looking at the genetic variation present among individuals within a species. This is the raw material avail- able for the selective process. Measuring Levels of Genetic Variation As we saw in chapter 13, a natural population can contain a great deal of genetic variation. This is true not only of hu- mans, but of all organisms. How much variation usually oc- curs? Biologists have looked at many different genes in an effort to answer this question: 1. Blood groups. Chemical analysis has revealed the ex- istence of more than 30 blood group genes in humans, in addition to the ABO locus. At least a third of these genes are routinely found in several alternative allelic forms in human populations. In addition to these, there are more than 45 variable genes encoding other pro- teins in human blood cells and plasma which are not considered blood groups. Thus, there are more than 75 genetically variable genes in this one system alone. 2. Enzymes. Alternative alleles of genes specifying particular enzymes are easy to distinguish by measur- ing how fast the alternative proteins migrate in an electric field (a process called electrophoresis). A great deal of variation exists at enzyme-specifying loci. About 5% of the enzyme loci of a typical human are heterozygous: if you picked an individual at random, and in turn selected one of the enzyme- encoding genes of that individual at random, the chances are 1 in 20 (5%) that the gene you selected would be heterozygous in that individual. Considering the entire human genome, it is fair to say that almost all people are different from one another. This is also true of other organisms, except for those that repro- duce asexually. In nature, genetic variation is the rule. Enzyme Polymorphism Many loci in a given population have more than one allele at frequencies significantly greater than would occur from mutation alone. Researchers refer to a locus with more variation than can be explained by mutation as polymor- phic (poly, “many,” morphic, “forms”) (figure 20.3). The ex- tent of such variation within natural populations was not even suspected a few decades ago, until modern techniques such as gel electrophoresis made it possible to examine en- zymes and other proteins directly. We now know that most populations of insects and plants are polymorphic (that is, have more than one allele occurring at a frequency greater than 5%) at more than half of their enzyme-encoding loci, although vertebrates are somewhat less polymorphic. Het- erozygosity (that is, the probability that a randomly se- lected gene will be heterozygous for a randomly selected individual) is about 15% in Drosophila and other inverte- brates, between 5% and 8% in vertebrates, and around 8% in outcrossing plants. These high levels of genetic variabil- ity provide ample supplies of raw material for evolution. DNA Sequence Polymorphism With the advent of gene technology, it has become possible to assess genetic variation even more directly by sequenc- ing the DNA itself. In a pioneering study in 1989, Martin Kreitman sequenced ADH genes isolated from 11 individu- als of the fruit fly Drosophila melanogaster. He found 43 vari- able sites, only one of which had been detected by protein electrophoresis! In the following decade, numerous other studies of variation at the DNA level have confirmed these findings: abundant variation exists in both the coding re- gions of genes and in their nontranslated introns—consid- erably more variation than we can detect examining en- zymes with electrophoresis. Natural populations contain considerable amounts of genetic variation—more than can be accounted for by mutation alone. Chapter 20 Genes within Populations 423 FIGURE 20.3 Polymorphic variation. These Australian snails, all of the species Bankivia fasciata, exhibit considerable variation in pattern and color. Individual variations are heritable and passed on to offspring. Population genetics is the study of the properties of genes in populations. Genetic variation within natural popula- tions was a puzzle to Darwin and his contemporaries. The way in which meiosis produces genetic segregation among the progeny of a hybrid had not yet been discovered. Selec- tion, scientists then thought, should always favor an opti- mal form, and so tend to eliminate variation. Moreover, the theory of blending inheritance—in which offspring were expected to be phenotypically intermediate relative to their parents—was widely accepted. If blending inheritance were correct, then the effect of any new genetic variant would quickly be diluted to the point of disappearance in subse- quent generations. The Hardy–Weinberg Principle Following the rediscovery of Mendel’s research, two people in 1908 independently solved the puzzle of why genetic variation persists—G. H. Hardy, an English mathemati- cian, and G. Weinberg, a German physician. They pointed out that the original proportions of the genotypes in a pop- ulation will remain constant from generation to generation, as long as the following assumptions are met: 1. The population size is very large. 2. Random mating is occurring. 3. No mutation takes place. 4. No genes are input from other sources (no immigra- tion takes place). 5. No selection occurs. Dominant alleles do not, in fact, replace recessive ones. Because their proportions do not change, the genotypes are said to be in Hardy–Weinberg equilibrium. In algebraic terms, the Hardy–Weinberg principle is written as an equation. Consider a population of 100 cats, with 84 black and 16 white cats. In statistics, frequency is defined as the proportion of individuals falling within a certain category in relation to the total number of indi- viduals under consideration. In this case, the respective frequencies would be 0.84 (or 84%) and 0.16 (or 16%). Based on these phenotypic frequencies, can we deduce the underlying frequency of genotypes? If we assume that the white cats are homozygous recessive for an allele we designate b, and the black cats are therefore either ho- mozygous dominant BB or heterozygous Bb, we can cal- culate the allele frequencies of the two alleles in the population from the proportion of black and white indi- viduals. Let the letter p designate the frequency of one al- lele and the letter q the frequency of the alternative al- lele. Because there are only two alleles, p plus q must always equal 1. The Hardy-Weinberg equation can now be expressed in the form of what is known as a binomial expansion: (p + q) 2 = p 2 +2pq + q 2 (Individuals (Individuals (Individuals homozygous heterozygous homozygous for allele B) with alleles B+ b) for allele b) If q 2 = 0.16 (the frequency of white cats), then q = 0.4. Therefore, p, the frequency of allele B, would be 0.6 (1.0 – 0.4 = 0.6). We can now easily calculate the genotype fre- quencies: there are p 2 = (0.6) 2 H11003 100 (the number of cats in the total population), or 36 homozygous dominant BB indi- viduals. The heterozygous individuals have the Bb geno- type, and there would be 2pq, or (2 H11003 0.6 H11003 0.4) H11003 100, or 48 heterozygous Bb individuals. 424 Part VI Evolution 20.2 Why do allele frequencies change in populations? Sperm Eggs Phenotypes Genotypes BB Bb bb 0.36 0.48 0.16 0.36 + 0.24 = 0.6B 0.24 + 0.16 = 0.4b Frequency of genotype in population Frequency of gametes b B BB Bb Bb bb q 2 = 0.16 pq = 0.24 pq = 0.24 p 2 = 0.36 p = 0.6 q = 0.4 p = 0.6 q = 0.4 b B FIGURE 20.4 The Hardy–Weinberg equilibrium. In the absence of factors that alter them, the frequencies of gametes, genotypes, and phenotypes remain constant generation after generation. Using the Hardy–Weinberg Equation The Hardy–Weinberg equation is a simple extension of the Punnett square described in chapter 13, with two alleles as- signed frequencies p and q. Figure 20.4 allows you to trace genetic reassortment during sexual reproduction and see how it affects the frequencies of the B and b alleles during the next generation. In constructing this diagram, we have assumed that the union of sperm and egg in these cats is random, so that all combinations of b and B alleles occur. For this reason, the alleles are mixed randomly and repre- sented in the next generation in proportion to their original representation. Each individual egg or sperm in each gen- eration has a 0.6 chance of receiving a B allele (p = 0.6) and a 0.4 chance of receiving a b allele (q = 0.4). In the next generation, therefore, the chance of combin- ing two B alleles is p 2 , or 0.36 (that is, 0.6 H11003 0.6), and ap- proximately 36% of the individuals in the population will continue to have the BB genotype. The frequency of bb in- dividuals is q 2 (0.4 H11003 0.4) and so will continue to be about 16%, and the frequency of Bb individuals will be 2pq (2 H11003 0.6 H11003 0.4), or approximately 48%. Phenotypically, if the population size remains at 100 cats, we will still see approx- imately 84 black individuals (with either BB or Bb geno- types) and 16 white individuals (with the bb genotype) in the population. Allele, genotype, and phenotype frequen- cies have remained unchanged from one generation to the next. This simple relationship has proved extraordinarily useful in assessing actual situations. Consider the recessive allele responsible for the serious human disease cystic fi- brosis. This allele is present in North Americans of Cau- casian descent at a frequency q of about 22 per 1000 indi- viduals, or 0.022. What proportion of North American Caucasians, therefore, is expected to express this trait? The frequency of double recessive individuals (q 2 ) is ex- pected to be 0.022 H11003 0.022, or 1 in every 2000 individu- als. What proportion is expected to be heterozygous car- riers? If the frequency of the recessive allele q is 0.022, then the frequency of the dominant allele p must be 1 – 0.022, or 0.978. The frequency of heterozygous individu- als (2pq) is thus expected to be 2 H11003 0.978 H11003 0.022, or 43 in every 1000 individuals. How valid are these calculated predictions? For many genes, they prove to be very accurate. As we will see, for some genes the calculated predictions do not match the ac- tual values. The reasons they do not tell us a great deal about evolution. Why Do Allele Frequencies Change? According to the Hardy–Weinberg principle, both the al- lele and genotype frequencies in a large, random-mating population will remain constant from generation to gen- eration if no mutation, no gene flow, and no selection occur. The stipulations tacked onto the end of the state- ment are important. In fact, they are the key to the im- portance of the Hardy–Weinberg principle, because indi- vidual allele frequencies often change in natural popula- tions, with some alleles becoming more common and others decreasing in frequency. The Hardy–Weinberg principle establishes a convenient baseline against which to measure such changes. By looking at how various fac- tors alter the proportions of homozygotes and heterozy- gotes, we can identify the forces affecting particular situa- tions we observe. Many factors can alter allele frequencies. Only five, however, alter the proportions of homozygotes and het- erozygotes enough to produce significant deviations from the proportions predicted by the Hardy–Weinberg princi- ple: mutation, gene flow (including both immigration into and emigration out of a given population), nonrandom mating, genetic drift (random change in allele frequencies, which is more likely in small populations), and selection (table 20.1). Of these, only selection produces adaptive evo- lutionary change because only in selection does the result depend on the nature of the environment. The other fac- tors operate relatively independently of the environment, so the changes they produce are not shaped by environ- mental demands. The Hardy–Weinberg principle states that in a large population mating at random and in the absence of other forces that would change the proportions of the different alleles at a given locus, the process of sexual reproduction (meiosis and fertilization) alone will not change these proportions. Chapter 20 Genes within Populations 425 Table 20.1 Agents of Evolutionary Change Factor Description Mutation The ultimate source of variation. Individual mutations occur so rarely that mutation alone does not change allele frequency much. Gene flow A very potent agent of change. Populations exchange members. Nonrandom Inbreeding is the most common form. It mating does not alter allele frequency but decreases the proportion of heterozygotes. Genetic drift Statistical accidents. Usually occurs only in very small populations. Selection The only form that produces adaptive evolutionary changes. Five Agents of Evolutionary Change 1. Mutation Mutation from one allele to an- other can obviously change the proportions of particular alleles in a population. Mutation rates are generally so low that they have little effect on the Hardy–Weinberg proportions of common alleles. A single gene may mutate about 1 to 10 times per 100,000 cell divisions (al- though some genes mutate much more frequently than that). Be- cause most environments are constantly changing, it is rare for a population to be stable enough to accumulate changes in allele frequency produced by a process this slow. Nonetheless, mutation is the ultimate source of genetic variation and thus makes evolu- tion possible. It is important to remember, however, that the likelihood of a particular mu- tation occurring is not affected by natural selection; that is, mutations do not occur more frequently in situations in which they would be favored by natural selection. 2. Gene Flow Gene flow is the movement of alleles from one population to another. It can be a powerful agent of change because members of two different populations may exchange ge- netic material. Sometimes gene flow is obvious, as when an animal moves from one place to another. If the characteris- tics of the newly arrived animal differ from those of the an- imals already there, and if the newcomer is adapted well enough to the new area to survive and mate successfully, the genetic composition of the receiving population may be altered. Other important kinds of gene flow are not as ob- vious. These subtler movements include the drifting of ga- metes or immature stages of plants or marine animals from one place to another (figure 20.5). Male gametes of flower- ing plants are often carried great distances by insects and other animals that visit their flowers. Seeds may also blow in the wind or be carried by animals or other agents to new populations far from their place of origin. In addition, gene flow may also result from the mating of individuals belong- ing to adjacent populations. However it occurs, gene flow can alter the genetic char- acteristics of populations and prevent them from maintain- ing Hardy–Weinberg equilibrium. In addition, even low levels of gene flow tend to homogenize allele frequencies among populations and thus keep the populations from di- verging genetically. In some situations, gene flow can counter the effect of natural selection by bringing an allele into a population at a rate greater than that at which the al- lele is removed by selection. 3. Nonrandom Mating Individuals with certain genotypes sometimes mate with one another more commonly than would be expected on a random basis, a phenomenon known as nonrandom mat- ing. Inbreeding (mating with relatives) is a type of nonran- dom mating that causes the frequencies of particular geno- types to differ greatly from those predicted by the Hardy–Weinberg principle. Inbreeding does not change the frequency of the alleles, but rather increases the pro- portion of homozygous individuals because relatives are likely be genetically similar and thus produce offspring with two copies of the same allele. This is why populations of self-fertilizing plants consist primarily of homozygous individuals, whereas outcrossing plants, which interbreed with individuals different from themselves, have a higher proportion of heterozygous individuals. By increasing homozygosity in a population, inbreeding increases the expression of recessive alleles. It is for this reason that marriage between close relatives is discouraged and to some degree outlawed—it increases the possibility of producing children homozygous for an allele associated with one or more of the recessive genetic disorders dis- cussed in chapter 13. 426 Part VI Evolution (a) Mutation UV light DNA T A G G G G C C (b) Gene flow (c) Nonrandom mating (e) Selection(d) Genetic drift Self- fertilization FIGURE 20.5 Five agents of evolutionary change. (a) Mutation, (b) gene flow, (c) nonrandom mating, (d) genetic drift, and (e) selection. 4. Genetic Drift In small populations, frequencies of particular alleles may change drastically by chance alone. Such changes in allele frequencies occur randomly, as if the frequencies were drifting, and are thus known as genetic drift. For this rea- son, a population must be large to be in Hardy–Weinberg equilibrium. If the gametes of only a few individuals form the next generation, the alleles they carry may by chance not be representative of the parent population from which they were drawn, as illustrated in figure 20.6, where a small number of individuals are removed from a bottle contain- ing many. By chance, most of the individuals removed are blue, so the new population has a much higher population of blue individuals than the parent one had. A set of small populations that are isolated from one an- other may come to differ strongly as a result of genetic drift even if the forces of natural selection do not differ between the populations. Indeed, because of genetic drift, harmful alleles may increase in frequency in small populations, de- spite selective disadvantage, and favorable alleles may be lost even though selectively advantageous. It is interesting to realize that humans have lived in small groups for much of the course of their evolution; consequently, genetic drift may have been a particularly important factor in the evolu- tion of our species. Even large populations may feel the effect of genetic drift. Large populations may have been much smaller in the past, and genetic drift may have greatly altered allele fre- quencies at that time. Imagine a population containing only two alleles of a gene, B and b, in equal frequency (that is, p = q = 0.5). In a large Hardy–Weinberg population, the genotype frequencies are expected to be 0.25 BB, 0.50 Bb, and 0.25 bb. If only a small sample produces the next gener- ation, large deviations in these genotype frequencies can occur by chance. Imagine, for example, that four individu- als form the next generation, and that by chance they are two Bb heterozygotes and two BB homozygotes—the allele frequencies in the next generation are p = 0.75 and q = 0.25! If you were to replicate this experiment 1000 times, each time randomly drawing four individuals from the parental population, one of the two alleles would be missing entirely from about 8 of the 1000 populations. This leads to an im- portant conclusion: genetic drift leads to the loss of alleles in isolated populations. Two related causes of decreases in a population’s size are founder effects and bottlenecks. Founder Effects. Sometimes one or a few individuals disperse and become the founders of a new, isolated popu- lation at some distance from their place of origin. These pi- oneers are not likely to have all the alleles present in the source population. Thus, some alleles may be lost from the new population and others may change drastically in fre- quency. In some cases, previously rare alleles in the source population may be a significant fraction of the new popula- tion’s genetic endowment. This phenomenon is called the founder effect. Founder effects are not rare in nature. Many self-pollinating plants start new populations from a single seed. Founder effects have been particularly important in the evolution of organisms on distant oceanic islands, such as the Hawaiian Islands and the Galápagos Islands visited by Darwin. Most of the organisms in such areas probably de- rive from one or a few initial “founders.” In a similar way, isolated human populations are often dominated by genetic features characteristic of their particular founders. The Bottleneck Effect. Even if organisms do not move from place to place, occasionally their populations may be drastically reduced in size. This may result from flooding, drought, epidemic disease, and other natural forces, or from progressive changes in the environment. The few sur- viving individuals may constitute a random genetic sample of the original population (unless some individuals survive specifically because of their genetic makeup). The resultant alterations and loss of genetic variability has been termed the bottleneck effect. Some living species appear to be severely depleted ge- netically and have probably suffered from a bottleneck ef- fect in the past. For example, the northern elephant seal, which breeds on the western coast of North America and nearby islands, was nearly hunted to extinction in the nine- teenth century and was reduced to a single population con- taining perhaps no more than 20 individuals on the island of Guadalupe off the coast of Baja, California. As a result of this bottleneck, even though the seal populations have re- bounded and now number in the tens of thousands, this species has lost almost all of its genetic variation. Chapter 20 Genes within Populations 427 Parent population Bottleneck (drastic reduction in population) Surviving individuals Next generation FIGURE 20.6 Genetic drift: The bottleneck effect. The parent population contains roughly equal numbers of blue and yellow individuals. By chance, the few remaining individuals that comprise the next generation are mostly blue. The bottleneck occurs because so few individuals form the next generation, as might happen after an epidemic or catastrophic storm. 5. Selection As Darwin pointed out, some individuals leave behind more progeny than others, and the rate at which they do so is affected by phenotype and behavior. We describe the re- sults of this process as selection and speak of both artifi- cial selection and natural selection. In artificial selection, the breeder selects for the desired characteristics. In natural selection, environmental conditions determine which indi- viduals in a population produce the most offspring. For natural selection to occur and result in evolutionary change, three conditions must be met: 1. Variation must exist among individuals in a popu- lation. Natural selection works by favoring individ- uals with some traits over individuals with alternative traits. If no variation exists, natural selection cannot operate. 2. Variation among individuals results in differences in number of offspring surviving in the next gen- eration. This is the essence of natural selection. Be- cause of their phenotype or behavior, some individu- als are more successful than others in producing offspring and thus passing their genes on to the next generation. 3. Variation must be genetically inherited. For natural selection to result in evolutionary change, the selected differences must have a genetic basis. However, not all variation has a genetic basis—even genetically identical individuals may be phenotypi- cally quite distinctive if they grow up in different environments. Such environmental effects are com- mon in nature. In many turtles, for example, indi- viduals that hatch from eggs laid in moist soil are heavier, with longer and wider shells, than individu- als from nests in drier areas. As a result of these en- vironmental effects, variation within a population does not always indicate the existence of underlying genetic variation. When phenotypically different individuals do not differ genetically, then differ- ences in the number of their offspring will not alter the genetic composition of the population in the next generation and, thus, no evolutionary change will have occurred. It is important to remember that natural selection and evolution are not the same—the two concepts often are incorrectly equated. Natural selection is a process, whereas evolution is the historical record of change through time. Evolution is an outcome, not a process. Natural selection (the process) can lead to evolution (the outcome), but natural selection is only one of several processes that can produce evolutionary change. More- over, natural selection can occur without producing evo- lutionary change; only if variation is genetically based will natural selection lead to evolution. Selection to Avoid Predators. Many of the most dra- matic documented instances of adaptation involve genetic changes which decrease the probability of capture by a predator. The caterpillar larvae of the common sulphur butterfly Colias eurytheme usually exhibit a dull Kelly green color, providing excellent camouflage on the alfalfa plants on which they feed. An alternative bright blue color morph is kept at very low frequency because this color renders the larvae highly visible on the food plant, making it easier for bird predators to see them. In a similar fashion, the way the shell markings in the land snail Cepaea nemoralis match its background habitat reflects the same pattern of avoiding predation by camouflage. One of the most dramatic examples of background matching involves ancient lava flows in the middle of deserts in the American southwest. In these areas, the black rock formations produced when the lava cooled contrasts starkly to the surrounding bright glare of the desert sand. Populations of many species of animals—including lizards, rodents, and a variety of insects—occurring on these rocks are dark in color, whereas sand-dwelling populations in surrounding areas are much lighter (figure 20.7). Predation is the likely cause selecting for these differences in color. Laboratory studies have confirmed that predatory birds are adept at picking out individuals occurring on backgrounds to which they are not adapted. 428 Part VI Evolution (b) (a) FIGURE 20.7 Pocket mice from the Tularosa Basin of New Mexico whose color matches their background. (a) The rock pocket mouse lives on lava, (b) while the Apache pocket mouse lives on white sand. Selection to Match Climatic Conditions. Many studies of selection have focused on genes encoding en- zymes because in such cases the investigator can directly assess the consequences to the organism of changes in the frequency of alternative enzyme alleles. Often investiga- tors find that enzyme allele frequencies vary latitudinally, with one allele more common in northern populations but progressively less common at more southern locations. A superb example is seen in studies of a fish, the mummi- chog, Fundulus heteroclitus, which ranges along the eastern coast of North America. In this fish, allele frequencies of the gene that produces the enzyme lactase dehydrogenase, which catalyzes the conversion of pyruvate to lactate, vary geographically (figure 20.8). Biochemical studies show that the enzymes formed by these alleles function differ- ently at different temperatures, thus explaining their geo- graphic distributions. For example, the form of the en- zyme that is more frequent in the north is a better catalyst at low temperatures than the enzyme from the south. Moreover, functional studies indicate that at low tempera- tures, individuals with the northern allele swim faster, and presumably survive better, than individuals with the alter- native allele. Selection for Pesticide Resistance. A particularly clear example of selection in action in natural populations is pro- vided by studies of pesticide resistance in insects. The widespread use of insecticides has led to the rapid evolution of resistance in more than 400 pest species. For example, the resistance allele at the pen gene decreases the uptake of insecticide, whereas alleles at the kdr and dld-r genes de- crease the number of target sites, thus decreasing the bind- ing ability of the insecticide (figure 20.9). Other alleles en- hance the ability of the insects’ enzymes to identify and detoxify insecticide molecules. Single genes are also responsible for resistance in other organisms. The pigweed, Amaranthus hybridus, is one of about 28 agricultural weeds that have evolved resistance to the herbicide Triazine. Triazine inhibits photosynthe- sis by binding to a protein in the chloroplast membrane. Single amino acid substitutions in the gene encoding the protein diminish the ability of Triazine to decrease the plant’s photosynthetic capabilities. Similarly, Norway rats are normally susceptible to the pesticide Warfarin, which diminishes the clotting ability of the rat’s blood and leads to fatal hemorrhaging. However, a resistance allele at a single gene alters a metabolic pathway and renders War- farin ineffective. Five factors can bring about a deviation from the proportions of homozygotes and heterozygotes predicted by the Hardy-Weinberg principle. Only selection regularly produces adaptive evolutionary change, but the genetic constitution of individual populations, and thus the course of evolution, can also be affected by mutation, gene flow, nonrandom mating, and genetic drift. Chapter 20 Genes within Populations 429 1.0 0.8 0.6 0.4 0.2 44 42 40 38 36 34 32 30 Latitude (Degrees North) Frequen c y of cold-ad a p t ed al lele FIGURE 20.8 Selection to match climatic conditions. Frequency of the cold- adapted allele for lactase dehydrogenase in the mummichog (Fundulus heteroclitus) decreases at lower latitudes, which are warmer. Pesticide molecule Resistant target site Insect cell membrane Target site Target site (a) Insect cells with resistance allele at pen gene: decreased uptake of the pesticide (b) Insect cells with resistance allele at kdr gene: decreased number of target sites for the pesticide FIGURE 20.9 Selection for pesticide resistance. Resistance alleles at genes like pen and kdr allow insects to be more resistant to pesticides. Insects that possess these resistance alleles have become more common through selection. Identifying the Evolutionary Forces Maintaining Polymorphism The Adaptive Selection Theory As evidence began to accumulate in the 1970s that natural populations exhibit a great deal of genetic polymorphism (that is, many alleles of a gene exist in the population), the question arose: What evolutionary force is maintaining the polymorphism? As we have seen, there are in principle five processes that act on allele frequencies: mutation, migra- tion, nonrandom mating, genetic drift, and selection. Be- cause migration and nonrandom mating are not major in- fluences in most natural populations, attention focused on the other three forces. The first suggestion, advanced by R. C. Lewontin (one of the discovers of enzyme polymorphism) and many oth- ers, was that selection was the force acting to maintain the polymorphism. Natural environments are often quite het- erogeneous, so selection might reasonably be expected to pull gene frequencies in different directions within differ- ent microhabitats, generating a condition in which many alleles persist. This proposal is called the adaptive selec- tion theory. The Neutral Theory A second possibility, championed by the great Japanese geneticist Moto Kimura, was that a balance between mu- tation and genetic drift is responsible for maintaining polymorphism. Kimura used elegant mathematics to demonstrate that, even in the absence of selection, nat- ural populations could be expected to contain consider- able polymorphism if mutation rates (generating the vari- ation) were high enough and population sizes (promoting genetic drift) were small enough. In this proposal, selec- tion is not acting, differences between alleles being “neu- tral to selection.” The proposal is thus called the neutral theory. Kimura’s theory, while complex, can be stated simply: H ˉˉ = 1/(4N e μ +1) H ˉˉ , the mean heterozygosity, is the likelihood that a randomly selected member of the population will be het- erozygous at a randomly selected locus. In a population without selection, this value is influenced by two vari- ables, the effective population size (N e ) and the mutation rate (μ). The peculiar difficulty of the neutral theory is that the level of polymorphism, as measured by H ˉˉ , is determined by the product of a very large number, N e , and a very small number, μ, both very difficult to measure with pre- cision. As a result, the theory can account for almost any value of H ˉˉ , making it very difficult to prove or disprove. As you might expect, a great deal of controversy has resulted. Testing the Neutral Theory Choosing between the adaptive selection theory and the neutral theory is not simple, for they both appear to ac- count for much of the data on gene polymorphism in nat- ural populations. A few well-characterized instances where selection acts on enzyme alleles do not settle the more gen- eral issue. An attempt to test the neutral theory by examin- ing large-scale patterns of polymorphism sheds light on the difficulty of choosing between the two theories: Population size: According to the neutral theory, polymorphism as measured by H ˉˉ should be proportional to the effective population size N e , assuming the muta- tion rate among neutral alleles μ is constant. Thus, H ˉˉ should be much greater for insects than humans, as there are far more individuals in an insect population than in a human one. When DNA sequence variation is examined, the fruit fly Drosophila melanogaster indeed exhibits sixfold higher levels of variation, as the theory predicts; but when enzyme polymorphisms are exam- ined, levels of variation in fruit flies and humans are similar. If the level of DNA variation correctly mirrors the predictions of the neutral theory, then something (selection?) is increasing variation at the enzyme level in humans. These sorts of patterns argue for rejection of the neutral theory. The nearly neutral model: One way to rescue the neutral theory from these sorts of difficulties is to retreat from the assumption of strict neutrality, modifying the theory to assume that many of the variants are slightly deleterious rather than strictly neutral to selection. With this adjustment, it is possible to explain many of the population-size-dependent large-scale patterns. How- ever, little evidence exists that the wealth of enzyme polymorphism in natural populations is in fact slightly deleterious. As increasing amounts of DNA sequence data become available, a detailed picture of variation at the DNA level is emerging. It seems clear that most nucleotide substitutions that change amino acids are disadvantageous and are elimi- nated by selection. But what about the many protein alleles that are seen in natural populations? Are they nearly neu- tral or advantageous? No simple answer is yet available, al- though the question is being actively investigated. Levels of polymorphism at enzyme-encoding genes may depend on both the action of selection on the gene (the adaptive selec- tion theory) and on the population dynamics of the species (the nearly neutral theory), with the relative contribution varying from one gene to the next. Adaptive selection clearly maintains some enzyme poly- morphisms in natural populations. Genetic drift seems to play a major role in producing the variation we see at the DNA level. For most enzyme-level polymorphism, investi- gators cannot yet choose between the selection theory and the nearly neutral theory. 430 Part VI Evolution Interactions among Evolutionary Forces When alleles are not selectively neu- tral, levels of variation retained in a population may be determined by the relative strength of different evolution- ary processes. In theory, for example, if allele B mutates to allele b at a high enough rate, allele b could be main- tained in the population even if natural selection strongly favored allele B. In nature, however, mutation rates are rarely high enough to counter the ef- fects of natural selection. The effect of natural selection also may be countered by genetic drift. Both processes may act to remove vari- ation from a population. However, whereas selection is a deterministic process that operates to increase the representation of alleles that enhance survival and reproductive success, drift is a random process. Thus, in some cases, drift may lead to a decrease in the frequency of an allele that is favored by selection. In some extreme cases, drift may even lead to the loss of a favored allele from a population. Remember, how- ever, that the magnitude of drift is negatively related to population size; consequently, natural selection is expected to overwhelm drift except when populations are very small. Gene Flow versus Natural Selection Gene flow can be either a constructive or a constraining force. On one hand, gene flow can increase the adaptedness of a species by spreading a beneficial mutation that arises in one population to other populations within a species. On the other hand, gene flow can act to impede adaptation within a population by continually importing inferior alle- les from other populations. Consider two populations of a species that live in different environments. In this situation, natural selection might favor different alleles—B and b—in the different populations. In the absence of gene flow and other evolutionary processes, the frequency of B would be expected to reach 100% in one population and 0% in the other. However, if gene flow were going on between the two populations, then the less favored allele would continu- ally be reintroduced into each population. As a result, the frequency of the two alleles in each population would re- flect a balance between the rate at which gene flow brings the inferior allele into a population versus the rate at which natural selection removes it. A classic example of gene flow opposing natural selec- tion occurs on abandoned mine sites in Great Britain. Al- though mining activities ceased hundreds of years ago, the concentration of metal ions in the soil is still much greater than in surrounding areas. Heavy metal concentrations are generally toxic to plants, but alleles at certain genes confer resistance. The ability to tolerate heavy metals comes at a price, however; individuals with the resistance allele exhibit lower growth rates on non-polluted soil. Consequently, we would expect the resistance allele to occur with a frequency of 100% on mine sites and 0% elsewhere. Heavy metal tol- erance has been studied particularly intensively in the slen- der bent grass, Agrostis tenuis, in which researchers have found that the resistance allele occurs at intermediate levels in many areas (figure 20.10). The explanation relates to the reproductive system of this grass in which pollen, the male gamete (that is, the floral equivalent of sperm), is dispersed by the wind. As a result, pollen—and the alleles it carries— can be blown for great distances, leading to levels of gene flow between mine sites and unpolluted areas high enough to counteract the effects of natural selection. In general, the extent to which gene flow can hinder the effects of natural selection should depend on the relative strengths of the two processes. In species in which gene flow is generally strong, such as birds and wind-pollinated plants, the frequency of the less favored allele may be rela- tively high, whereas in more sedentary species which ex- hibit low levels of gene flow, such as salamanders, the fa- vored allele should occur at a frequency near 100%. Evolutionary processes may act to either remove or maintain genetic variation within a population. Allele frequency sometimes may reflect a balance between opposed processes, such as gene flow and natural selection. In such cases, observed frequencies will depend on the relative strength of the processes. Chapter 20 Genes within Populations 431 Index of copper tole r ance Distance in meters Non- mine Mine Non-mine 0 20 40 0 20 40 60 80 100 120 140 160 0 20 40 60 Prevailing wind Bent grass (Agrostis tenuis) FIGURE 20.10 Degree of copper tolerance in grass plants on and near ancient mine sites. Prevailing winds blow pollen containing nontolerant alleles onto the mine site and tolerant alleles beyond the site’s borders. Heterozygote Advantage In the previous pages, natural selection has been discussed as a process that removes variation from a population by fa- voring one allele over others at a genetic locus. However, if heterozygotes are favored over homozygotes, then natural selection actually will tend to maintain variation in the population. The reason is simple. Instead of tending to re- move less successful alleles from a population, such het- erozygote advantage will favor individuals with copies of both alleles, and thus will work to maintain both alleles in the population. Some evolutionary biologists believe that heterozygote advantage is pervasive and can explain the high levels of polymorphism observed in natural popula- tions. Others, however, believe that it is relatively rare. Sickle Cell Anemia The best documented example of heterozygote advantage is sickle cell anemia, a hereditary disease affecting hemo- globin in humans. Individuals with sickle cell anemia ex- hibit symptoms of severe anemia and contain abnormal red blood cells which are irregular in shape, with a great number of long and sickle-shaped cells. The disease is particularly common among African Americans. In chap- ter 13, we noted that this disorder, which affects roughly 3 African Americans out of every 1000, is associated with a particular recessive allele. Using the Hardy–Weinberg equation, you can calculate the frequency of the sickle cell allele in the African-American population; this frequency is the square root of 0.003, or approximately 0.054. In contrast, the frequency of the allele among white Ameri- cans is only about 0.001. Sickle cell anemia is often fatal. Until therapies were developed to more effectively treat its symptoms, almost all affected individuals died as children. Even today, 31% of patients in the United States die by the age of 15. The disease occurs because of a single amino acid change, re- peated in the two beta chains of the hemoglobin molecule. In this change, a valine replaces the usual glutamic acid at a location on the surface of the protein near the oxygen- binding site. Unlike glutamic acid, valine is nonpolar (hy- drophobic). Its presence on the surface of the molecule creates a “sticky” patch that attempts to escape from the polar water environment by binding to another similar patch. As long as oxygen is bound to the hemoglobin mol- ecule there is no problem, because the hemoglobin atoms shield the critical area of the surface. When oxygen levels fall, such as after exercise or when an individual is stressed, oxygen is not so readily bound to hemoglobin and the ex- posed sticky patch binds to similar patches on other hemo- globin molecules, eventually producing long, fibrous clumps (figure 20.11). The result is a deformed, “sickle- shaped” red blood cell. Individuals who are heterozygous or homozygous for the valine-specifying allele (designated allele S) are said to possess the sickle cell trait. Heterozygotes produce some sickle-shaped red blood cells, but only 2% of the number seen in homozygous individuals. The reason is that in het- erozygotes, one-half of the molecules do not contain va- line at the critical location. Consequently, when a mole- cule produced by the non-sickle cell allele is added to the chain, there is no further “sticky” patch available to add additional molecules and chain elongation stops. Hence, most chains in heterozygotes are too short to produce sickling of the cell. 432 Part VI Evolution Val 6 FIGURE 20.11 Why the sickle cell mutation causes hemoglobin to clump. The sickle cell mutation changes the sixth amino acid in the hemoglobin β chain (position B6) from glutamic acid (very polar) to valine (nonpolar). The unhappy result is that the nonpolar valine at position B6, protruding from a corner of the hemoglobin molecule, fits into a nonpolar pocket on the opposite side of another hemoglobin molecule, causing the two molecules to clump together. As each molecule has both a B6 valine and an opposite nonpolar pocket, long chains form. When polar glutamic acid (the normal allele) occurs at position B6, it is not attracted to the nonpolar pocket, and no clumping occurs. Copyright ? Irving Geis. Malaria and Heterozygote Advantage The average incidence of the S allele in the Central African population is about 0.12, far higher than that found among African Americans. From the Hardy–Weinberg principle, you can calculate that 1 in 5 Central African individuals are heterozygous at the S allele, and 1 in 100 develops the fatal form of the disorder. People who are homozygous for the sickle cell allele almost never reproduce because they usu- ally die before they reach reproductive age. Why is the S allele not eliminated from the Central African population by selection, rather than being maintained at such high lev- els? People who are heterozygous for the sickle cell allele are much less susceptible to malaria—one of the leading causes of illness and death in Central Africa, especially among young children—in the areas where the allele is common. The reason is that when the parasite that causes malaria, Plasmodium falciparum, enters a red blood cell, it causes extremely low oxygen tension in the cell, which leads to cell sickling even in heterozygotes. Such cells are quickly filtered out of the bloodstream by the spleen, thus eliminating the parasite (the spleen’s filtering effect is what leads to anemia in homozygotes as large numbers of red blood cells are removed). Consequently, even though most homozygous recessive individuals die before they have children, the sickle cell al- lele is maintained at high levels in these populations (it is se- lected for) because of its association with resistance to malaria in heterozygotes and also, for reasons not yet fully understood, with increased fertility in female heterozygotes. For people living in areas where malaria is common, having the sickle cell allele in the heterozygous condition has adaptive value (figure 20.12). Among African Ameri- cans, however, many of whose ancestors have lived for some 15 generations in a country where malaria has been relatively rare and is now essentially absent, the environ- ment does not place a premium on resistance to malaria. Consequently, no adaptive value counterbalances the ill ef- fects of the disease; in this nonmalarial environment, selec- tion is acting to eliminate the S allele. Only 1 in 375 African Americans develop sickle cell anemia, far less than in Central Africa. The hemoglobin allele S, responsible for sickle cell anemia in homozygotes, is maintained by heterozygote advantage in Central Africa, where heterozygotes for the S allele are resistant to malaria. Chapter 20 Genes within Populations 433 Sickle cell allele in Africa 1-5% 5-10% 10-20% P.falciparum malaria in Africa Malaria (b) (a) Normal red blood cells Sickled red blood cells FIGURE 20.12 Frequency of sickle cell allele and distribution of Plasmodium falciparum malaria. (a)The red blood cells of people homozygous for the sickle cell allele collapse into sickled shapes when the oxygen level in the blood is low. (b) The distribution of the sickle cell allele in Africa coincides closely with that of P.falciparum malaria. Forms of Selection In nature many traits, perhaps most, are affected by more than one gene. The interactions between genes are typi- cally complex, as you saw in chapter 13. For example, alle- les of many different genes play a role in determining human height (see figure 13.18). In such cases, selection operates on all the genes, influencing most strongly those that make the greatest contribution to the phenotype. How selection changes the population depends on which geno- types are favored. Disruptive Selection In some situations, selection acts to eliminate rather than to favor intermediate types. A clear example is the different beak sizes of the African fire-bellied seedcracker finch Py- ronestes ostrinus. Populations of these birds contain individ- uals with large and small beaks, but very few individuals with intermediate-sized beaks. As their name implies, these birds feed on seeds, and the available seeds fall into two size categories: large and small. Only large-beaked birds can open the tough shells of large seeds, whereas birds with the smallest beaks are most adept at handling small seeds. Birds with intermediate-sized beaks are at a disadvantage with both seed types: unable to open large seeds and too clumsy to efficiently process small seeds. Consequently, selection acts to eliminate the intermediate phenotypes, in effect par- titioning the population into two phenotypically distinct groups. This form of selection is called disruptive selec- tion (figure 20.13a). 434 Part VI Evolution 0 25 50 100 12575 Selection for small and large individuals Number of individuals (a) Disruptive selection Two peaks form Number of individuals 0 25 50 100 12575 (c) Stabilizing selection Peak gets narrower 0 25 50 100 12575 Selection for midsized individuals 0 25 50 100 12575 (b) Directional selection Peak shifts 0 25 50 100 12575 Selection for larger individuals 0 25 50 100 12575 FIGURE 20.13 Three kinds of natural selection. The top panels show the populations before selection has occurred, with the forms that will be selected against shaded red and the forms that will be favored shaded blue. The bottom panels indicate what the populations will look like after selection has occurred. (a) In disruptive selection, individuals in the middle of the range of phenotypes of a certain trait are selected against (red), and the extreme forms of the trait are favored (blue). (b) In directional selection, individuals concentrated toward one extreme of the array of phenotypes are favored. (c) In stabilizing selection, individuals with midrange phenotypes are favored, with selection acting against both ends of the range of phenotypes. 20.3 Selection can act on traits affected by many genes. Directional Selection When selection acts to eliminate one extreme from an array of phenotypes (figure 20.13b), the genes promoting this extreme become less frequent in the population. Thus, in the Drosophila population illustrated in figure 20.14, the elimination of flies that move toward light causes the popu- lation to contain fewer individuals with alleles promoting such behavior. If you were to pick an individual at random from the new fly population, there is a smaller chance it would spontaneously move toward light than if you had se- lected a fly from the old population. Selection has changed the population in the direction of lower light attraction. This form of selection is called directional selection. Stabilizing Selection When selection acts to eliminate both extremes from an array of phenotypes (figure 20.13c), the result is to increase the frequency of the already common intermediate type. In effect, selection is operating to prevent change away from this middle range of values. Selection does not change the most common phenotype of the population, but rather makes it even more common by eliminating extremes. Many examples are known. In humans, infants with inter- mediate weight at birth have the highest survival rate (fig- ure 20.15). In ducks and chickens, eggs of intermediate weight have the highest hatching success. This form of se- lection is called stabilizing selection. Components of Fitness Natural selection occurs when individuals with one pheno- type leave more surviving offspring in the next generation than individuals with an alternative phenotype. Evolution- ary biologists quantify reproductive success as fitness, the number of surviving offspring left in the next generation. Although selection is often characterized as “survival of the fittest,” differences in survival are only one component of fitness. Even if no differences in survival occur, selection may operate if some individuals are more successful than others in attracting mates. In many territorial animal species, large males mate with many females and small mates rarely get to mate. In addition, the number of off- spring produced per mating is also important. Large female frogs and fish lay more eggs than smaller females and thus may leave more offspring in the next generation. Selection on traits affected by many genes can favor both extremes of the trait, or intermediate values, or only one extreme. Chapter 20 Genes within Populations 435 0246810 Number of generations A v er age tendency to fly to w ard light 2 1 3 4 5 6 7 8 9 10 11 12 13 14 15 12 18 2014 16 Selected population that tends not to fly toward light Selected population that tends to fly toward light FIGURE 20.14 Directional selection for phototropism in Drosophila. In generation after generation, individuals of the fly Drosophilawere selectively bred to obtain two populations. When flies with a strong tendency to fly toward light (positive phototropism) were used as parents for the next generation, their offspring had a greater tendency to fly toward light (top curve). When flies that tended notto fly toward light were used as parents for the next generation, their offspring had an even greater tendency not to fly toward light (bottom curve). 20 15 10 5 10 20 30 50 70 100 5 7 3 2 23456 Birth weight in pounds P ercent of bir ths in population P ercent of inf ant mor tality 78910 FIGURE 20.15 Stabilizing selection for birth weight in human beings. The death rate among babies (red curve; right y-axis) is lowest at an intermediate birth weight; both smaller and larger babies have a greater tendency to die than those around the optimum weight (blue area; left y-axis) of between 7 and 8 pounds. Limits to What Selection Can Accomplish Although selection is perhaps the most powerful of the five principal agents of ge- netic change, there are limits to what it can accomplish. These limits arise because al- ternative alleles may interact in different ways with other genes and because alleles often affect multiple aspects of the pheno- type (the phenomena of epistasis and pleiotropy discussed in chapter 13). These interactions tend to set limits on how much a phenotype can be altered. For example, selecting for large clutch size in barnyard chickens eventually leads to eggs with thin- ner shells that break more easily. For this reason, we do not have gigantic cattle that yield twice as much meat as our leading strains, chickens that lay twice as many eggs as the best layers do now, or corn with an ear at the base of every leaf, instead of just at the base of a few leaves. Evolution Requires Genetic Variation Over 80% of the gene pool of the thor- oughbred horses racing today goes back to 31 known an- cestors from the late eighteenth century. Despite intense directional selection on thoroughbreds, their perfor- mance times have not improved for the last 50 years (fig- ure 20.16). Years of intense selection presumably have re- moved variation from the population at a rate greater than it could be replenished by mutation such that now no genetic variation remains and evolutionary change is not possible. In some cases, phenotypic variation for a trait may never have had a genetic basis. The compound eyes of in- sects are made up of hundreds of visual units, termed om- matidia. In some individuals, the left eye contains more ommatidia than the right eye. However, despite intense selection in the laboratory, scientists have never been able to produce a line of fruit flies that consistently have more ommatidia in the left eye than in the right. The reason is that separate genes do not exist for the left and right eyes. Rather, the same genes affect both eyes, and differences in the number of ommatidia result from dif- ferences that occur as the eyes are formed in the develop- ment process (figure 20.17). Thus, despite the existence of phenotypic variation, no genetic variation is available for selection to favor. 436 Part VI Evolution 1900 110 115 120 125 130 1920 1940 1960 Year Kentucky Derby winning speed (seconds) 1980 2000 FIGURE 20.16 Selection for increased speed in racehorses is no longer effective. Kentucky Derby winning speeds have not improved significantly since 1950. Right Left FIGURE 20.17 Phenotypic variation in insect ommatidia. In some individuals, the number of ommatidia in the left eye is greater than the number in the right eye. However, this difference is not genetically based; developmental processes cause the difference. Selection against Rare Alleles A second factor limits what selection can accomplish: selection acts only on pheno- types. For this reason, selection does not operate efficiently on rare recessive alle- les, simply because there is no way to se- lect against them unless they come to- gether as homozygotes. For example, when a recessive allele a is present at a frequency q equal to 0.2, only four out of a hundred individuals (q 2 ) will be double recessive and display the phenotype asso- ciated with this allele (figure 20.18). For lower allele frequencies, the effect is even more dramatic: if the frequency in the population of the recessive allele q = 0.01, the frequency of recessive homozygotes in that population will be only 1 in 10,000. The fact that selection acts on pheno- types rather than genotypes means that selection against undesirable genetic traits in humans or domesticated animals is difficult unless the heterozygotes can also be detected. For example, if a par- ticular recessive allele r (q = 0.01) was considered undesirable, and none of the homozygotes for this allele were allowed to breed, it would take 1000 generations, or about 25,000 years in humans, to lower the allele frequency by half to 0.005. At this point, after 25,000 years of work, the frequency of homozygotes would still be 1 in 40,000, or 25% of what it was initially. Selection in Laboratory Environments One way to assess the action of selection is to carry out artificial selection in the laboratory. Strains that are ge- netically identical except for the gene subject to selection can be crossed so that the possibility of linkage disequilib- rium does not confound the analysis. Populations of bac- teria provide a particularly powerful tool for studying se- lection in the laboratory because bacteria have a short generation time (less than an hour) and can be grown in huge numbers in growth vats called chemostats. In pio- neering studies, Dan Hartl and coworkers backcrossed bacteria with different alleles of the enzyme 6-PGD into a homogeneous genetic background, and then compared the growth of the different strains when they were fed only gluconate, the enzyme’s substrate. Hartl found that all of the alleles grew at the same rate! The different alle- les were thus selectively neutral in a normal genetic back- ground. However, when Hartl disabled an alternative bio- chemical pathway for the metabolism of gluconate, so that only 6-PGD mediated the utilization of this sole source of carbon, he obtained very different results: several alleles were markedly superior to others. Selection was clearly able to operate on these alleles, but only under certain conditions. The ability of selection to produce evolutionary change is hindered by a variety of factors, including multiple effects of single genes, gene interactions, and lack of genetic variation. Moreover, selection can only eliminate rare recessive alleles very slowly. Chapter 20 Genes within Populations 437 Genotype frequency Frequency of a 0.2 0.4 0.6 0.2 0 0.4 0.6 0.8 1.0 0.8 1.0AA Aa aa FIGURE 20.18 The relationship between allele frequency and genotype frequency. If allele ais present at a frequency of 0.2, the double recessive genotype aa is only present at a frequency of 0.04. In other words, only 4 in 100 individuals will have a homozygous recessive genotype, while 64 in 100 will have a homozygous dominant genotype. 438 Part VI Evolution Chapter 20 Summary Questions Media Resources 20.1 Genes vary in natural populations. ? Evolution is best defined as “descent with modification.” ? Darwin’s primary insight was to propose that evolutionary change resulted from the operation of natural selection. ? By the 1860s, natural selection was widely accepted as the correct explanation for the process of evolution. The field of evolution did not progress much further, however, until the 1920s because of the lack of a suitable explanation of how hereditary traits are transmitted. ? Invertebrates and outcrossing plants are often heterozygous at about 12 to 15% of their loci; the corresponding value for vertebrates is about 4 to 8%. 1. What is the difference between natural selection and evolution? 2. What is adaptation? How does it fit into Darwin’s concept of evolution? 3. What is genetic polymorphism? What has polymorphism to do with evolution? ? Studies of how allele frequencies shift within populations allow investigators to study evolution in action. ? Meiosis does not alter allele frequencies within populations. Unless selection or some other force acts on the genes, the frequencies of their alleles remain unchanged from one generation to the next. ? A variety of processes can lead to evolutionary change within a population, including genetic drift, inbreeding, gene flow, and natural selection. ? For evolution to occur by natural selection, three conditions must be met: 1. variation must exist in the population; 2. the variation must have a genetic basis; and 3. variation must be related to the number of offspring left in the next generation. ? Natural selection can usually overpower the effects of genetic drift, except in very small populations. ? Natural selection can overwhelm the effects of gene flow in some cases, but not in others. 4. Given that allele A is present in a large random-mating population at a frequency of 54 per 100 individuals, what is the proportion of individuals in that population expected to be heterozygous for the allele? homozygous dominant? homozygous recessive? 5. Why does the founder effect have such a profound influence on a population’s genetic makeup? How does the bottleneck effect differ from the founder effect? 6. What effect does inbreeding have on allele frequency? Why is marriage between close relatives discouraged? 20.2 Why do allele frequencies change in populations? ? Directional selection acts to eliminate one extreme from an array of phenotypes; stabilizing selection acts to eliminate both extremes; and disruptive selection acts to eliminate rather than to favor the intermediate type. ? Natural selection is not all powerful; genetic variation is required for natural selection to produce evolutionary change. 7. Define selection. How does it alter allele frequencies? What are the three types of selection? Give an example of each. 8. Why are there limitations to the success of selection? 20.3 Selection can act on traits affected by many genes. www.mhhe.com/raven6e www.biocourse.com ? Scientists on Science: from Butterflies to Global Preservation ? Student Research: Cotton Boll Weevil ? Book Review: The Evolution of Jane by Schine ? Hardy Weinberg Equilibrium ? Activity: Natural Selection ? Activity: Allele Frequencies ? Activity: Genetic Drift ? Types of Selection ? Evolutionary Variation ? Other Processes of Evolution ? Adaptation 439 21 The Evidence for Evolution Concept Outline 21.1 Fossil evidence indicates that evolution has occurred. The Fossil Record. When fossils are arranged in the order of their age, a continual series of change is seen, new changes being added at each stage. The Evolution of Horses. The record of horse evolution is particularly well-documented and instructive. 21.2 Natural selection can produce evolutionary change. The Beaks of Darwin’s Finches. Natural selection favors stouter bills in dry years, when large tough-to-crush seeds are the only food available to finches. Peppered Moths and Industrial Melanism. Natural selection favors dark-colored moths in areas of heavy pollution, while light-colored moths survive better in unpolluted areas. Artificial Selection. Artificial selection practiced in laboratory studies, agriculture, and domestication demonstrate that selection can produce substantial evolutionary change. 21.3 Evidence for evolution can be found in other fields of biology. The Anatomical Record. When anatomical features of living animals are examined, evidence of shared ancestry is often apparent. The Molecular Record. When gene or protein sequences from organisms are arranged, species thought to be closely related based on fossil evidence are seen to be more similar than species thought to be distantly related. Convergent and Divergent Evolution. Evolution favors similar forms under similar circumstances. 21.4 The theory of evolution has proven controversial. Darwin’s Critics. Critics have raised seven objections to Darwin’s theory of evolution by natural selection. O f all the major ideas of biology, the theory that to- day’s organisms evolved from now-extinct ancestors (figure 21.1) is perhaps the best known to the general pub- lic. This is not because the average person truly under- stands the basic facts of evolution, but rather because many people mistakenly believe that it represents a challenge to their religious beliefs. Similar highly publicized criticisms of evolution have occurred ever since Darwin’s time. For this reason, it is important that, during the course of your study of biology, you address the issue squarely: Just what is the evidence for evolution? FIGURE 21.1 A window into the past. The fossil remains of the now- extinct reptile Mesosaurus found in Permian sediments in Africa and South America provided one of the earliest clues to a former connection between the two continents. Mesosaurus was a freshwater species and so clearly incapable of a transatlantic swim. Therefore, it must have lived in the lakes and rivers of a formerly contiguous landmass that later became divided as Africa and South America drifted apart in the Cretaceous. Dating Fossils By dating the rocks in which fossils occur, we can get an ac- curate idea of how old the fossils are. In Darwin’s day, rocks were dated by their position with respect to one an- other (relative dating); rocks in deeper strata are generally older. Knowing the relative positions of sedimentary rocks and the rates of erosion of different kinds of sedimentary rocks in different environments, geologists of the nine- teenth century derived a fairly accurate idea of the relative ages of rocks. Today, rocks are dated by measuring the degree of decay of certain radioisotopes contained in the rock (ab- solute dating); the older the rock, the more its isotopes have decayed. Because radioactive isotopes decay at a constant rate unaltered by temperature or pressure, the isotopes in a rock act as an internal clock, measuring the time since the rock was formed. This is a more accurate way of dating rocks and provides dates stated in millions of years, rather than relative dates. A History of Evolutionary Change When fossils are arrayed according to their age, from oldest to youngest, they often provide evidence of succes- sive evolutionary change. At the largest scale, the fossil record documents the progression of life through time, from the origin of eukaryotic organisms, through the evolution of fishes, the rise of land-living organisms, the reign of the dinosaurs, and on to the origin of humans (figure 21.2). 440 Part VI Evolution At its core, the case for evolution is built upon two pillars: first, evidence that natural selection can produce evolution- ary change and, second, evidence from the fossil record that evolution has occurred. In addition, information from many different areas of biology—including fields as differ- ent as embryology, anatomy, molecular biology, and bio- geography (the study of the geographic distribution of species)—can only be interpreted sensibly as the outcome of evolution. The Fossil Record The most direct evidence that evolution has occurred is found in the fossil record. Today we have a far more com- plete understanding of this record than was available in Darwin’s time. Fossils are the preserved remains of once- living organisms. Fossils are created when three events occur. First, the organism must become buried in sedi- ment; then, the calcium in bone or other hard tissue must mineralize; and, finally, the surrounding sediment must eventually harden to form rock. The process of fossilization probably occurs rarely. Usually, animal or plant remains will decay or be scavenged before the process can begin. In addition, many fossils occur in rocks that are inaccessible to scientists. When they do become available, they are often destroyed by erosion and other natural processes before they can be collected. As a result, only a fraction of the species that have ever existed (estimated by some to be as many as 500 million) are known from fossils. Nonetheless, the fossils that have been discovered are sufficient to pro- vide detailed information on the course of evolution through time. 21.1 Fossil evidence indicates that evolution has occurred. Millions of years ago Eukaryotes Vertebrates Colonization of land Reptiles Amphibians Mammals and dinosaurs Flowering plants and first birds First hominids 1002003004005006001500 Extinction of the dinosaurs FIGURE 21.2 Timeline of the history of life as revealed by the fossil record. Gaps in the Fossil Record This is not to say that the fossil record is complete. Given the low likelihood of fossil preservation and recovery, it is not surprising that there are gaps in the fossil record. Nonetheless, paleontologists (the scientists who study fossils) continue to fill in the gaps in the fossil record. While many gaps interrupted the fossil record in Darwin’s era, even then, scientists knew of the Ar- chaeopteryx fossil transitional between dinosaurs and birds. Today, the fos- sil record is far more complete, par- ticularly among the vertebrates; fos- sils have been found linking all the major groups. Recent years have seen spectacular discoveries closing some of the major remaining gaps in our understanding of vertebrate evo- lution. For example, recently a four- legged aquatic mammal was discov- ered that provides important insights concerning the evolution of whales and dolphins from land-living, hoofed ancestors (figure 21.3). Simi- larly, a fossil snake with legs has shed light on the evolution of snakes, which are descended from lizards that gradually became more and more elongated with simultaneous reduction and eventual disappear- ance of the limbs. On a finer scale, evolutionary change within some types of animals is known in exceptional detail. For example, about 200 million years ago, oysters underwent a change from small curved shells to larger, flatter ones, with progressively flat- ter fossils being seen in the fossil record over a period of 12 million years (figure 21.4). A host of other examples all illustrate a record of successive change. The demonstra- tion of this successive change is one of the strongest lines of evidence that evolution has occurred. The fossil record provides a clear record of the major evolutionary transitions that have occurred through time. Chapter 21 The Evidence for Evolution 441 Present 10 million years ago 20 million years ago 30 million years ago 40 million years ago 50 million years ago 60 million years ago Hypothetical mesonychid skeleton Modern toothed whales Ambulocetus natans probably walked on land (as do modern sea lions) and swam by flexing its backbone and paddling with its hind limbs (as do modern otters) Rodhocetus kasrani's reduced hind limbs could not have aided it in walking or swimming. Rodhocetus swam with an up-and-down motion, as do modern whales FIGURE 21.3 Whale “missing links.” The recent discoveries of Ambulocetus and Rodhocetus have filled in the gaps between the mesonychids, the hypothetical ancestral link between the whales and the hoofed mammals, and present-day whales. G. arcuata obliquata G. arcuata incurva G. mecullochii G. gigantea FIGURE 21.4 Evolution of shell shape in oysters. Over 12 million years of the Early Jurassic Period, the shells of this group of coiled oysters became larger, thinner, and flatter. These animals rested on the ocean floor in a special position called the “life position,” and it may be that the larger, flatter shells were more stable in disruptive water movements. The Evolution of Horses One of the best-studied cases in the fossil record concerns the evolution of horses. Modern-day members of the Equidae include horses, zebras, donkeys and asses, all of which are large, long-legged, fast-running animals adapted to living on open grasslands. These species, all classified in the genus Equus, are the last living descendants of a long lineage that has produced 34 genera since its origin in the Eocene Period, approximately 55 million years ago. Exam- ination of these fossils has provided a particularly well- documented case of how evolution has proceeded by adap- tation to changing environments. The First Horse The earliest known members of the horse family, species in the genus Hyracotherium, didn’t look much like horses at all. Small, with short legs and broad feet (figure 21.5), these species occurred in wooded habitats, where they probably browsed on leaves and herbs and escaped predators by dodging through openings in the forest vegetation. The evolutionary path from these diminutive creatures to the workhorses of today has involved changes in a variety of traits, including: Size. The first horses were no bigger than dogs, with some considerably smaller. By contrast, modern equids can weigh more than a half ton. Examination of the fos- sil record reveals that horses changed little in size for their first 30 million years, but since then, a number of different lineages exhibited rapid and substantial in- creases. However, trends toward decreased size were also exhibited among some branches of the equid evolu- tionary tree (figure 21.6). Toe reduction. The feet of modern horses have a sin- gle toe, enclosed in a tough, bony hoof. By contrast, Hyracotherium had four toes on its front feet and three on its hindfeet. Rather than hooves, these toes were en- cased in fleshy pads. Examination of the fossils clearly shows the transition through time: increase in length of the central toe, development of the bony hoof, and re- duction and loss of the other toes (figure 21.7). As with body size, these trends occurred concurrently on several different branches of the horse evolutionary tree. At the same time as these developments, horses were evolving changes in the length and skeletal structure of the limbs, leading to animals capable of running long distances at high speeds. Tooth size and shape. The teeth of Hyracotherium were small and relatively simple in shape. Through time, horse teeth have increased greatly in length and have de- veloped a complex pattern of ridges on their molars and premolars (figure 21.7). The effect of these changes is to produce teeth better capable of chewing tough and gritty vegetation, such as grass, which tends to wear teeth down. Accompanying these changes have been al- terations in the shape of the skull that strengthened the skull to withstand the stresses imposed by continual chewing. As with body size, evolutionary change has not been constant through time. Rather, much of the change in tooth shape has occurred within the past 20 million years. All of these changes may be understood as adaptations to changing global climates. In particular, during the late 442 Part VI Evolution FIGURE 21.5 Hyracotherium sandrae, one of the earliest horses, was the size of a housecat. ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? Body s i ze ( k g) Millions of years ago 50 100 150 200 250 300 350 400 450 500 550 60 55 50 45 40 35 30 25 20 15 10 5 0 Equus Hyracotherium Mesohippus Merychippus Nannippus FIGURE 21.6 Evolutionary change in body size of horses. Lines show the broad outline of evolutionary relationships. Although most change involved increases in size, some decreases also occurred. Miocene and early Oligocene (approximately 20 to 25 mil- lion years ago), grasslands became widespread in North America, where much of horse evolution occurred. As horses adapted to these habitats, long-distance and high- speed locomotion probably became more important to es- cape predators and travel great distances. By contrast, the greater flexibility provided by multiple toes and shorter limbs, which was advantageous for ducking through com- plex forest vegetation, was no longer beneficial. At the same time, horses were eating grasses and other vegetation that contained more grit and other hard substances, thus favoring teeth and skulls better suited for withstanding such materials. Evolutionary Trends For many years, horse evolution was held up as an example of constant evolutionary change through time. Some even saw in the record of horse evolution evidence for a progres- sive, guiding force, consistently pushing evolution to move in a single direction. We now know that such views are misguided; evolutionary change over millions of years is rarely so simple. Rather, the fossils demonstrate that, although there have been overall trends evident in a variety of characteristics, evolutionary change has been far from constant and uni- form through time. Instead, rates of evolution have varied widely, with long periods of little change and some periods of great change. Moreover, when changes happen, they often occur simultaneously in different lineages of the horse evolutionary tree. Finally, even when a trend exists, exceptions, such as the evolutionary decrease in body size exhibited by some lineages, are not uncommon. These pat- terns, evident in our knowledge of horse evolution, are usu- ally discovered for any group of plants and animals for which we have an extensive fossil record, as we shall see when we discuss human evolution in chapter 23. Horse Diversity One reason that horse evolution was originally conceived of as linear through time may be that modern horse diver- sity is relatively limited. Thus, it is easy to mentally pic- ture a straight line from Hyracotherium to modern-day Equus. However, today’s limited horse diversity—only one surviving genus—is unusual. Indeed, at the peak of horse diversity in the Miocene, as many as 13 genera of horses could be found in North America alone. These species differed in body size and in a wide variety of other characteristics. Presumably, they lived in different habi- tats and exhibited different dietary preferences. Had this diversity existed to modern times, early workers presum- ably would have had a different outlook on horse evolu- tion, a situation that is again paralleled by the evolution of humans. The extensive fossil record for horses provides a detailed view of the evolutionary diversification of this group from small forest dwellers to the large and fast modern grassland species. Chapter 21 The Evidence for Evolution 443 Hyracotherium Mesohippus Merychippus Pliohippus Equus FIGURE 21.7 Evolutionary changes in horses through time. As we saw in chapter 20, a variety of different processes can result in evolutionary change. Nonetheless, in agreement with Darwin, most evolutionary biologists would agree that natural selection is the process responsible for most of the major evolutionary changes that have occurred through time. Although we cannot travel back through time, a vari- ety of modern-day evidence confirms the power of natural selection as an agent of evolutionary change. These data come from both the field and the laboratory and from nat- ural and human-altered situations. The Beaks of Darwin’s Finches Darwin’s finches are a classic example of evolution by nat- ural selection. Darwin collected 31 specimens of finch from three islands when he visited the Galápagos Islands off the coast of Ecuador in 1835. Darwin, not an expert on birds, had trouble identifying the specimens, believing by examin- ing their bills that his collection contained wrens, “gross- beaks,” and blackbirds. You can see Darwin’s sketches of four of these birds in figure 21.8. The Importance of the Beak Upon Darwin’s return to England, ornithologist John Gould examined the finches. Gould recognized that Dar- win’s collection was in fact a closely related group of dis- tinct species, all similar to one another except for their bills. In all, there were 13 species. The two ground finches with the larger bills in figure 21.8 feed on seeds that they crush in their beaks, whereas the two with narrower bills eat insects. One species is a fruit eater, another a cactus eater, yet another a “vampire” that creeps up on seabirds and uses its sharp beak to drink their blood. Perhaps most remarkable are the tool users, woodpecker finches that pick up a twig, cactus thorn, or leaf stalk, trim it into shape with their bills, and then poke it into dead branches to pry out grubs. The correspondence between the beaks of the 13 finch species and their food source immediately suggested to Darwin that evolution had shaped them: “Seeing this gradation and diversity of structure in one small, intimately related group of birds, one might really fancy that from an original paucity of birds in this archi- pelago, one species has been taken and modified for dif- ferent ends.” Was Darwin Wrong? If Darwin’s suggestion that the beak of an ancestral finch had been “modified for different ends” is correct, then it ought to be possible to see the different species of finches acting out their evolutionary roles, each using their bills to acquire their particular food specialty. The four species that crush seeds within their bills, for example, should feed on different seeds, those with stouter beaks specializing on harder-to-crush seeds. 444 Part VI Evolution 21.2 Natural selection can produce evolutionary change. FIGURE 21.8 Darwin’s own sketches of Galápagos finches. From Darwin’s Journal of Researches: (1) large ground finch Geospiza magnirostris; (2) medium ground finch Geospiza fortis; (3) small tree finch Camarhynchus parvulus; (4) warbler finch Certhidea olivacea. Many biologists visited the Galápagos after Darwin, but it was 100 years before any tried this key test of his hypothesis. When the great naturalist David Lack finally set out to do this in 1938, observing the birds closely for a full five months, his observations seemed to contradict Darwin’s proposal! Lack often observed many different species of finch feeding together on the same seeds. His data indicated that the stout-beaked species and the slender-beaked species were feeding on the very same array of seeds. We now know that it was Lack’s misfortune to study the birds during a wet year, when food was plentiful. The finch’s beak is of little importance in such flush times; small seeds are so abundant that birds of all species are able to get enough to eat. Later work has revealed a very different picture during leaner, dry years, when few seeds are avail- able and the difference between survival and starvation de- pends on being able to efficiently gather enough to eat. In such times, having beaks designed to be maximally effective for a particular type of food becomes critical and the species diverge in their diet, each focusing on the type of food to which it is specialized. A Closer Look The key to successfully testing Darwin’s proposal that the beaks of Galápagos finches are adaptations to different food sources proved to be patience. Starting in 1973, Peter and Rosemary Grant of Princeton University and generations of their students have studied the medium ground finch Geospiza fortis on a tiny island in the center of the Galápa- gos called Daphne Major. These finches feed preferentially on small tender seeds, produced in abundance by plants in wet years. The birds resort to larger, drier seeds, which are harder to crush, only when small seeds become depleted during long periods of dry weather, when plants produce few seeds. The Grants quantified beak shape among the medium ground finches of Daphne Major by carefully measuring beak depth (width of beak, from top to bottom, at its base) on individual birds. Measuring many birds every year, they were able to assemble for the first time a detailed portrait of evolution in action. The Grants found that beak depth changed from one year to the next in a predictable fashion. During droughts, plants produced few seeds and all avail- able small seeds quickly were eaten, leaving large seeds as the major remaining source of food. As a result, birds with large beaks survived better, because they were better able to break open these large seeds. Consequently, the average beak depth of birds in the population increased the next year, only to decrease again when wet seasons returned (figure 21.9). Could these changes in beak dimension reflect the ac- tion of natural selection? An alternative possibility might be that the changes in beak depth do not reflect changes in gene frequencies, but rather are simply a response to diet— perhaps during lean times the birds become malnourished and then grow stouter beaks, for example. To rule out this possibility, the Grants measured the relation of parent bill size to offspring bill size, examining many broods over sev- eral years. The depth of the bill was passed down faithfully from one generation to the next, regardless of environmen- tal conditions, suggesting that the differences in bill size in- deed reflected genetic differences. Darwin Was Right After All If the year-to-year changes in beak depth indeed reflect ge- netic changes, as now seems likely, and these changes can be predicted by the pattern of dry years, then Darwin was right after all—natural selection does seem to be operating to adjust the beak to its food supply. Birds with stout beaks have an advantage during dry periods, for they can break the large, dry seeds that are the only food available. When small seeds become plentiful once again with the return of wet weather, a smaller beak proves a more efficient tool for harvesting the more abundant smaller seeds. Among Darwin’s finches, natural selection adjusts the shape of the beak in response to the nature of the available food supply, adjustments that can be seen to be occurring even today. Chapter 21 The Evidence for Evolution 445 1977 1980 1982 1984 Dry year Dry year Dry year Wet year Beak depth FIGURE 21.9 Evidence that natural selection alters beak size in Geospiza fortis. In dry years, when only large, tough seeds are available, the mean beak size increases. In wet years, when many small seeds are available, smaller beaks become more common. Peppered Moths and Industrial Melanism When the environment changes, natural selection often may favor new traits in a species. The example of the Dar- win’s finches clearly indicates how natural variation can lead to evolutionary change. Humans are greatly altering the environment in many ways; we should not be surprised to see organisms attempting to adapt to these new condi- tions. One classic example concerns the peppered moth, Biston betularia. Until the mid-nineteenth century, almost every individual of this species captured in Great Britain had light-colored wings with black specklings (hence the name “peppered” moth). From that time on, individuals with dark-colored wings increased in frequency in the moth populations near industrialized centers until they made up almost 100% of these populations. Black individu- als had a dominant allele that was present but very rare in populations before 1850. Biologists soon noticed that in in- dustrialized regions where the dark moths were common, the tree trunks were darkened almost black by the soot of pollution. Dark moths were much less conspicuous resting on them than were light moths. In addition, the air pollu- tion that was spreading in the industrialized regions had killed many of the light-colored lichens on tree trunks, making the trunks darker. Selection for Melanism Can Darwin’s theory explain the increase in the frequency of the dark allele? Why did dark moths gain a survival ad- vantage around 1850? An amateur moth collector named J. W. Tutt proposed what became the most commonly accepted hypothesis explaining the decline of the light- colored moths. He suggested that peppered forms were more visible to predators on sooty trees that have lost their lichens. Consequently, birds ate the peppered moths resting on the trunks of trees during the day. The black forms, in contrast, were at an advantage because they were camouflaged (figure 21.10). Although Tutt initially had no evidence, British ecologist Bernard Kettlewell tested the hypothesis in the 1950s by rearing populations of peppered moths with equal numbers of dark and light individuals. Kettlewell then released these populations into two sets of woods: one, near heavily polluted Birm- ingham, the other, in unpolluted Dorset. Kettlewell set up rings of traps around the woods to see how many of both kinds of moths survived. To evaluate his results, he had marked the released moths with a dot of paint on the un- derside of their wings, where birds could not see it. In the polluted area near Birmingham, Kettlewell trapped 19% of the light moths, but 40% of the dark ones. This indicated that dark moths had a far better chance of surviving in these polluted woods, where the tree trunks were dark. In the relatively unpolluted Dorset woods, Ket- tlewell recovered 12.5% of the light moths but only 6% of the dark ones. This indicated that where the tree trunks were still light-colored, light moths had a much better chance of survival. Kettlewell later solidified his argument by placing hidden blinds in the woods and actually filming birds eating the moths. Sometimes the birds Kettlewell ob- served actually passed right over a moth that was the same color as its background. Industrial Melanism Industrial melanism is a term used to describe the evolu- tionary process in which darker individuals come to pre- dominate over lighter individuals since the industrial revo- lution as a result of natural selection. The process is widely believed to have taken place because the dark organisms are better concealed from their predators in habitats that have been darkened by soot and other forms of industrial pollu- tion, as suggested by Kettlewell’s research. 446 Part VI Evolution FIGURE 21.10 Tutt’s hypothesis explaining industrial melanism. These photographs show color variants of the peppered moth, Biston betularia. Tutt proposed that the dark moth is more visible to predators on unpolluted trees (top), while the light moth is more visible to predators on bark blackened by industrial pollution (bottom). Dozens of other species of moths have changed in the same way as the peppered moth in industrialized areas throughout Eurasia and North America, with dark forms becoming more common from the mid-nineteenth century onward as indus- trialization spread. Selection against Melanism In the second half of the twentieth cen- tury, with the widespread implementa- tion of pollution controls, these trends are reversing, not only for the peppered moth in many areas in England, but also for many other species of moths throughout the northern continents. These examples provide some of the best documented instances of changes in al- lelic frequencies of natural populations as a result of natural selection due to specific factors in the environment. In England, the pollution promoting industrial melanism began to reverse following enactment of Clean Air legis- lation in 1956. Beginning in 1959, the Biston population at Caldy Common outside Liverpool has been sampled each year. The frequency of the melanic (dark) form has dropped from a high of 94% in 1960 to its current (1994) low of 19% (figure 21.11). Similar reversals have been documented at numerous other locations throughout England. The drop correlates well with a drop in air pollution, particularly with tree-darkening sulfur dioxide and suspended particulates. Interestingly, the same reversal of industrial melanism appears to have occurred in America during the same time that it was happening in England. Industrial melanism in the American subspecies of the peppered moth was not as widespread as in England, but it has been well-documented at a rural field station near Detroit. Of 576 peppered moths collected there from 1959 to 1961, 515 were melanic, a fre- quency of 89%. The American Clean Air Act, passed in 1963, led to significant reductions in air pollution. Resam- pled in 1994, the Detroit field station peppered moth pop- ulation had only 15% melanic moths (see figure 21.11)! The moths in Liverpool and Detroit, both part of the same natural experiment, exhibit strong evidence of natural se- lection. Reconsidering the Target of Natural Selection Tutt’s hypothesis, widely accepted in the light of Ket- tlewell’s studies, is currently being reevaluated. The prob- lem is that the recent selection against melanism does not appear to correlate with changes in tree lichens. At Caldy Common, the light form of the peppered moth began its increase in frequency long before lichens began to reappear on the trees. At the Detroit field station, the lichens never changed significantly as the dark moths first became domi- nant and then declined over the last 30 years. In fact, inves- tigators have not been able to find peppered moths on De- troit trees at all, whether covered with lichens or not. Wherever the moths rest during the day, it does not appear to be on tree bark. Some evidence suggests they rest on leaves on the treetops, but no one is sure. The action of selection may depend less on the presence of lichens and more on other differences in the environ- ment resulting from industrial pollution. Pollution tends to cover all objects in the environment with a fine layer of particulate dust, which tends to decrease how much light surfaces reflect. In addition, pollution has a particularly se- vere effect on birch trees, which are light in color. Both ef- fects would tend to make the environment darker and thus would favor darker color in moths. Natural selection has favored the dark form of the peppered moth in areas subject to severe air pollution, perhaps because on darkened trees they are less easily seen by moth-eating birds. Selection has in turn favored the light form as pollution has abated. Chapter 21 The Evidence for Evolution 447 Year 0 10 20 30 40 60 50 80 70 90 100 P ercentage of melanic moths 59 63 67 71 75 79 83 87 91 95 FIGURE 21.11 Selection against melanism. The circles indicate the frequency of melanic Biston moths at Caldy Common in England, sampled continuously from 1959 to 1995. Diamonds indicate frequencies in Michigan from 1959 to 1962 and from 1994 to 1995. Source: Data from Grant, et al., “Parallel Rise and Fall of Melanic Peppered Moths” in Journal of Heredity, vol. 87, 1996, Oxford University Press. Artificial Selection Humans have imposed selection upon plants and animals since the dawn of civilization. Just as in natural selection, artificial selection operates by favoring individuals with cer- tain phenotypic traits, allowing them to reproduce and pass their genes into the next generation. Assuming that pheno- typic differences are genetically determined, such selection should lead to evolutionary change and, indeed, it has. Arti- ficial selection, imposed in laboratory experiments, agricul- ture, and the domestication process, has produced substan- tial change in almost every case in which it has been applied. This success is strong proof that selection is an ef- fective evolutionary process. Laboratory Experiments With the rise of genetics as a field of science in the 1920s and 1930s, researchers began conducting experiments to test the hypothesis that selection can produce evolutionary change. A favorite subject was the now-famous laboratory fruit fly, Drosophila melanogaster. Geneticists have imposed selection on just about every conceivable aspect of the fruit fly—including body size, eye color, growth rate, life span, and exploratory behavior—with a consistent result: selec- tion for a trait leads to strong and predictable evolutionary response. In one classic experiment, scientists selected for fruit flies with many bristles (stiff, hairlike structures) on their abdomen. At the start of the experiment, the average num- ber of bristles was 9.5. Each generation, scientists picked out the 20% of the population with the greatest number of bristles and allowed them to reproduce, thus establishing the next generation. After 86 generations of such selection, the average number of bristles had quadrupled, to nearly 40. In a similar experiment, fruit flies were selected for ei- ther the most or the fewest numbers of bristles. Within 35 generations, the populations did not overlap at all in range of variation (figure 21.12). Similar experiments have been conducted on a wide va- riety of other laboratory organisms. For example, by select- ing for rats that were resistant to tooth decay, scientists were able to increase in less than 20 generations the aver- age time for onset of decay from barely over 100 days to greater than 500 days. Agriculture Similar methods have been practiced in agriculture for many centuries. Familiar livestock, such as cattle and pigs, and crops, like corn and strawberries, are greatly different from their wild ancestors (figure 21.13). These differences have resulted from generations of selection for desirable traits like milk production and corn stalk size. An experimental study with corn demonstrates the abil- ity of artificial selection to rapidly produce major change in crop plants. In 1896, agricultural scientists began selecting on oil content of corn kernels, which initially was 4.5%. As in the fruit fly experiments, the top 20% of all individuals were allowed to reproduce. In addition, a parallel experi- ment selected for the individuals with the lowest oil con- tent. By 1986, at which time 90 generations had passed, av- erage oil content had increased approximately 450% in the high-content experiment; by contrast, oil content in the low experiment had decreased to about 0.5%, a level at which it is difficult to get accurate readings. 448 Part VI Evolution Mean Mean Mean High population Bristle number in Drosophila 0 1020304050607080901010 Numbe r of individ u a l s Low population Initial population FIGURE 21.12 Artificial selection in the laboratory. In this experiment, one population of Drosophila was selected for low numbers of bristles and the other for high numbers. Note that not only did the means of the populations change greatly in 35 generations, but also that all individuals in both experimental populations lie outside the range of the initial population. Teosinte Intermediates Modern corn FIGURE 21.13 Corn looks very different from its ancestor. The tassels and seeds of a wild grass, such as teosinte, evolved into the male tassels and female ears of modern corn. Domestication Artificial selection has also been responsible for the great variety of breeds of cats, dogs (figure 21.14), pigeons, cattle and other do- mestic animals. In some cases, breeds have been developed for particular purposes. Grey- hound dogs, for example, were bred by select- ing for maximal running abilities, with the end result being an animal with long legs and tail (the latter used as a rudder), an arched back (to increase the length of its stride), and great muscle mass. By contrast, the odd proportions of the ungainly basset hound resulted from se- lection for dogs that could enter narrow holes in pursuit of rabbits and other small game. In other cases, breeds have been developed pri- marily for their appearance, such as the many colorful and ornamented varieties of pigeons or the breeds of cats. Domestication also has led to unintentional selection for some traits. In recent years, as part of an attempt to domesticate the silver fox, Russian scientists each generation have chosen the most docile animals and allowed them to reproduce. Within 40 years, the vast majority of foxes born were exceptionally docile, not only allowing themselves to be pet- ted, but also whimpering to get attention and sniffing and licking their caretakers. In many respects, they had become no different than domestic dogs! However, it was not only be- havior that changed. These foxes also began to exhibit dif- ferent color patterns, floppy ears, curled tails, and shorter legs and tails. Presumably, the genes responsible for docile behavior have other effects as well (the phenomenon of pleiotropy discussed in the last chapter); as selection has fa- vored docile animals, it has also led to the evolution of these other traits. Can Selection Produce Major Evolutionary Changes? Given that we can observe the results of selection operating over relatively short periods of time, most scientists believe that natural selection is the process responsible for the evo- lutionary changes documented in the fossil record. Some critics of evolution accept that selection can lead to changes within a species, but contend that such changes are rela- tively minor in scope and not equivalent to the substantial changes documented in the fossil record. In other words, it is one thing to change the number of bristles on a fruit fly or the size of a corn stalk, and quite another to produce an entirely new species. This argument does not fully appreciate the extent of change produced by artificial selection. Consider, for ex- ample, the breeds of dogs, all of which have been pro- duced since wolves were first domesticated, perhaps 10,000 years ago. If the various dog breeds did not exist and a paleontologist found fossils of animals similar to dachshunds, greyhounds, mastiffs, Chihuahuas, and pomeranians, there is no question that they would be con- sidered different species. Indeed, these breeds are so dif- ferent that they would probably be classified in different genera. In fact, the diversity exhibited by dog breeds far outstrips the differences observed among wild members of the family Canidae—such as coyotes, jackals, foxes, and wolves. Consequently, the claim that artificial selection produces only minor changes is clearly incorrect. Indeed, if selection operating over a period of only 10,000 years can produce such substantial differences, then it would seem powerful enough, over the course of many millions of years, to produce the diversity of life we see around us today. Artificial selection often leads to rapid and substantial results over short periods of time, thus demonstrating the power of selection to produce major evolutionary change. Chapter 21 The Evidence for Evolution 449 Greyhound Mastiff Dachshund Chihuahua FIGURE 21.14 Breeds of dogs. The differences between these dogs are greater than the differences displayed between any wild species of canids. The Anatomical Record Much of the power of the theory of evolution is its ability to provide a sensible framework for understanding the diversity of life. Many observa- tions from a wide variety of fields of biology simply cannot be understood in any meaningful way except as a re- sult of evolution. Homology As vertebrates evolved, the same bones were sometimes put to differ- ent uses. Yet the bones are still seen, their presence betraying their evolu- tionary past. For example, the fore- limbs of vertebrates are all homolo- gous structures, that is, structures with different appearances and func- tions that all derived from the same body part in a common ancestor. You can see in figure 21.15 how the bones of the forelimb have been modified in different ways for different verter- bates. Why should these very differ- ent structures be composed of the same bones? If evolution had not oc- curred, this would indeed be a riddle. But when we consider that all of these animals are descended from a common ancestor, it is easy to under- stand that natural selection has modi- fied the same initial starting blocks to serve very different purposes. Development Some of the strongest anatomical evi- dence supporting evolution comes from comparisons of how organisms develop. In many cases, the evolu- tionary history of an organism can be seen to unfold during its develop- ment, with the embryo exhibiting characteristics of the embryos of its ancestors (figure 21.16). For example, early in their development, human embryos possess gill slits, like a fish; at a later stage, every human embryo has a long bony tail, the vestige of which we carry to adulthood as the coccyx at the end of our spine. Human fetuses even possess a fine fur (called lanugo) during the fifth month of development. These relict developmental forms suggest strongly that our development has evolved, with new in- structions layered on top of old ones. 450 Part VI Evolution 21.3 Evidence for evolution can be found in other fields of biology. Human Cat Bat Porpoise Horse FIGURE 21.15 Homology among the bones of the forelimb. Although these structures show considerable differences in form and function, the same basic bones are present in the forelimbs of humans, cats, bats, porpoises, and horses. Gill slits Tail Fish Reptile Bird Human Tail Gill slits FIGURE 21.16 Our embryos show our evolutionary history. The embryos of various groups of vertebrate animals show the features they all share early in development, such as gill slits (in purple) and a tail. The observation that seemingly different organisms may exhibit similar embryological forms pro- vides indirect but convincing evi- dence of a past evolutionary rela- tionship. Slugs and giant ocean squids, for example, do not bear much superficial resemblance to each other, but the similarity of their embryological forms pro- vides convincing evidence that they are both mollusks. Vestigial Structures Many organisms possess vestigial structures that have no apparent function, but that resemble struc- tures their presumed ancestors had. Humans, for example, possess a complete set of muscles for wig- gling their ears, just as a coyote does (table 21.1). Boa constrictors have hip bones and rudimentary hind legs. Manatees (a type of aquatic mammal often referred to as “sea cows”) have fingernails on their fins (which evolved from legs). Figure 21.17 illustrates the skeleton of a baleen whale, which contains pelvic bones, as other mammal skeletons do, even though such bones serve no known function in the whale. The human vermiform appendix is apparently vesti- gial; it represents the degenerate terminal part of the cecum, the blind pouch or sac in which the large intestine begins. In other mammals such as mice, the cecum is the largest part of the large intestine and functions in storage— usually of bulk cellulose in herbivores. Although some sug- gestions have been made, it is difficult to assign any current function to the vermiform appendix. In many respects, it is a dangerous organ: quite often it becomes infected, leading to an inflammation called appendicitis; without surgical re- moval, the appendix may burst, allowing the contents of the gut to come in contact with the lining of the body cav- ity, a potentially fatal event. It is difficult to understand ves- tigial structures such as these as anything other than evolu- tionary relicts, holdovers from the evolutionary past. They argue strongly for the common ancestry of the members of the groups that share them, regardless of how different they have subsequently become. Comparisons of the anatomy of different living animals often reveal evidence of shared ancestry. In some instances, the same organ has evolved to carry out different functions, in others, an organ loses its function altogether. Sometimes, different organs evolve in similar ways when exposed to the same selective pressures. Chapter 21 The Evidence for Evolution 451 FIGURE 21.17 Vestigial features. The skeleton of a baleen whale, a representative of the group of mammals that contains the largest living species, contains pelvic bones. These bones resemble those of other mammals, but are only weakly developed in the whale and have no apparent function. Table 21.1 Some Vestigial Traits in Humans Trait Description Ear-wiggling muscles Three small muscles around each ear that are large and important in some mammals, such as dogs, turning the ears toward a source of sound. Few people can wiggle their ears, and none can turn them toward sound. Tail Present in human and all vertebrate embryos. In humans, the tail is reduced; most adults only have three to five tiny tail bones and, occasionally, a trace of a tail-extending muscle. Appendix Structure which presumably had a digestive function in some of our ancestors, like the cecum of some herbivores. In humans, it varies in length from 5–15 cm, and some people are born without one. Wisdom teeth Molars that are often useless and sometimes even trapped in the jawbone. Some people never develop wisdom teeth. Based on a suggestion by Dr. Leslie Dendy, Department of Science and Technology, University of New Mexico, Los Alamos. The Molecular Record Traces of our evolutionary past are also evident at the molecular level. If you think about it, the fact that organ- isms have evolved successively from relatively simple ancestors implies that a record of evolutionary change is pre- sent in the cells of each of us, in our DNA. When an ancestral species gives rise to two or more descendants, those descendants will initially exhibit fairly high overall similarity in their DNA. However, as the descendants evolve in- dependently, they will accumulate more and more differences in their DNA. Consequently, organisms that are more distantly related would be ex- pected to accumulate a greater number of evolutionary differences, whereas two species that are more closely re- lated should share a greater portion of their DNA. To examine this hypothesis, we need an estimate of evolutionary rela- tionships that has been developed from data other than DNA (it would be a circular argument to use DNA to estimate relationships and then con- clude that closely related species are more similar in their DNA than are distantly related species). Such an hypothesis of evolu- tionary relationships is provided by the fossil record, which indicates when particular types of organisms evolved. In addition, by examining the anatomical struc- tures of fossils and of modern species, we can infer how closely species are related to each other. When degree of genetic similarity is compared with our ideas of evolutionary relationships based on fossils, a close match is evident. For example, when the human he- moglobin polypeptide is compared to the corresponding molecule in other species, closely related species are found to be more similar. Chimpanzees, gorillas, orang- utans, and macaques, vertebrates thought to be more closely related to humans, have fewer differences from humans in the 146-amino-acid hemoglobin β chain than do more distantly related mammals, like dogs. Nonmam- malian vertebrates differ even more, and nonvertebrate hemoglobins are the most different of all (figure 21.18). Similar patterns are also evident when the DNA itself is compared. For example, chimps and humans, which are thought to have descended from a common ancestor that lived approximately 6 million years ago, exhibit few differ- ences in their DNA. Why should closely related species be similar in DNA? Because DNA is the genetic code that produces the struc- ture of living organisms, one might expect species that are similar in overall appearance and structure, such as humans and chimpanzees, to be more similar in DNA than are more dissimilar species, such as humans and frogs. This ex- pectation would hold true even if evolution had not oc- curred. However, there are some noncoding stretches of DNA (sometimes called “junk DNA”) that have no func- tion and appear to serve no purpose. If evolution had not occurred, there would be no reason to expect similar- appearing species to be similar in their junk DNA. How- ever, comparisons of such stretches of DNA provide the same results as for other parts of the genome: more closely related species are more similar, an observation that only makes sense if evolution has occurred. Comparison of the DNA of different species provides strong evidence for evolution. Species deduced from the fossil record to be closely related are more similar in their DNA than are species thought to be more distantly related. 452 Part VI Evolution Number of amino acid differences between this hemoglobin polypeptide and a human one 10 20 30 40 50 60 70 67 125 45 32 8 80 90 100 110 120 T ime LampreyFrogBirdDogMacaqueHuman FIGURE 21.18 Molecules reflect evolutionary divergence. You can see that the greater the evolutionary distance from humans (white cladogram), the greater the number of amino acid differences in the vertebrate hemoglobin polypeptide. Convergent and Divergent Evolution Different geographical areas some- times exhibit groups of plants and an- imals of strikingly similar appearance, even though the organisms may be only distantly related. It is difficult to explain so many similarities as the re- sult of coincidence. Instead, natural selection appears to have favored par- allel evolutionary adaptations in simi- lar environments. Because selection in these instances has tended to favor changes that made the two groups more alike, their phenotypes have converged. This form of evolutionary change is referred to as convergent evolution, or sometimes, parallel evolution. The Marsupial-Placental Convergence In the best-known case of conver- gent evolution, two major groups of mammals, marsupials and placentals, have evolved in a very similar way, even though the two lineages have been living independently on sepa- rate continents. Australia separated from the other continents more than 50 million years ago, after marsupi- als had evolved but before the ap- pearance of placental mammals. As a result, the only mammals in Aus- tralia (other than bats and a few col- onizing rodents) have been marsupi- als, members of a group in which the young are born in a very immature condition and held in a pouch until they are ready to emerge into the outside world. Thus, even though placental mammals are the dominant mammalian group throughout most of the world, marsupials retained su- premacy in Australia. What are the Australian marsupials like? To an aston- ishing degree, they resemble the placental mammals living today on the other continents (figure 21.19). The similarity between some individual members of these two sets of mammals argues strongly that they are the result of conver- gent evolution, similar forms having evolved in different, isolated areas because of similar selective pressures in simi- lar environments. Homology versus Analogy How do we know when two similar characters are homolo- gous and when they are analogous? As we have seen, adap- tation favoring different functions can obscure homologies, while convergent evolution can create analogues that ap- pear as similar as homologues. There is no hard-and-fast answer to this question; the determination of homologues is often a thorny issue in biological classification. As we have seen in comparing vertebrate embryos, and again in comparing slugs and squids, studies of embryonic develop- ment often reveal features not apparent when studying adult organisms. In general, the more complex two struc- tures are, the less likely they evolved independently. Chapter 21 The Evidence for Evolution 453 Niche Placental Mammals Australian Marsupials Burrower Mole Lesser anteater Mouse Lemur Flying squirrel Ocelot Wolf Tasmanian wolf Tasmanian "tiger cat" Flying phalanger Spotted cuscus Numbat (anteater) Marsupial mole Marsupial mouse Anteater Mouse Climber Glider Cat Wolf FIGURE 21.19 Convergent evolution. Marsupials in Australia resemble placental mammals in the rest of the world. They evolved in isolation after Australia separated from other continents. Darwin and Patterns of Recent Divergence Darwin was the first to present evidence that animals and plants living on oceanic islands resemble most closely the forms on the nearest continent—a relationship that only makes sense as reflecting common ancestry. The Galápagos turtle in figure 21.20 is more similar to South American turtles than to those of any other continent. This kind of relationship strongly suggests that the island forms evolved from individuals that came from the adjacent mainland at some time in the past. Thus, the Galápagos finches of fig- ure 21.8 have different beaks than their South American relatives. In the absence of evolution, there seems to be no logical explanation of why individual kinds of island plants and animals would be clearly related to others on the near- est mainland, but still have some divergent features. As Darwin pointed out, this relationship provides strong evi- dence that macroevolution has occurred. A similar resemblance to mainland birds can be seen in an island finch Darwin never saw—a solitary finch species living on Cocos Island, a tiny, remote volcanic island lo- cated 630 kilometers to the northeast of the Galápagos. This finch does not resemble the finches of Europe, Aus- tralia, Africa, or North America. Instead, it resembles the finches of Costa Rica, 500 kilometers to the east. Of course, because of adaptation to localized habitats, is- land forms are not identical to those on the nearby conti- nents. The turtles have evolved different shell shapes, for example; those living in moist habitats have dome-shaped shells while others living in dry places have low, saddle- backed shells with the front of the shell bent up to expose the head and neck. Similarly, the Galápagos finches have evolved from a single presumptive ancestor into 13 species, each specialized in a different way. These Galápagos turtles and finches have evolved in concert with the continental forms, from the same ancestors, but the two lineages have diverged rather than converged. It is fair to ask how Darwin knew that the Galápagos tortoises and finches do not represent the convergence of unrelated island and continental forms (analogues) rather than the divergence of recently isolated groups (homo- logues). While either hypothesis would argue for natural selection, Darwin chose divergence of homologues as by far the simplest explanation, because the turtles and finches differ by only a few traits, and are similar in many. In sum total, the evidence for macroevolution is over- whelming. In the next chapter, we will consider Darwin’s proposal that microevolutionary changes have led directly to macroevolutionary changes, the key argument in his the- ory that evolution occurs by natural selection. Evolution favors similar forms under similar circumstances. Convergence is the evolution of similar forms in different lineages when exposed to the same selective pressures. Divergence is the evolution of different forms in the same lineage when exposed to different selective pressures. 454 Part VI Evolution FIGURE 21.20 A Galápagos tortoise most closely resembles South American tortoises. Isolated on these remote islands, the Galápagos tortoise has evolved distinctive forms. This natural experiment is being terminated, however. Since Darwin’s time, much of the natural habitat of the larger islands has been destroyed by human intrusion. Goats introduced by settlers, for example, have drastically altered the vegetation. Darwin’s Critics In the century since he proposed it, Darwin's theory of evolution by natural selection has become nearly univer- sally accepted by biologists, but has proven controversial among the general public. Darwin's critics raise seven prin- cipal objections to teaching evolution: 1. Evolution is not solidly demonstrated. “Evolution is just a theory,” Darwin's critics point out, as if theory meant lack of knowledge, some kind of guess. Scien- tists, however, use the word theory in a very different sense than the general public does. Theories are the solid ground of science, that of which we are most certain. Few of us doubt the theory of gravity because it is "just a theory." 2. There are no fossil intermediates. “No one ever saw a fin on the way to becoming a leg,” critics claim, pointing to the many gaps in the fossil record in Dar- win's day. Since then, however, most fossil intermedi- ates in vertebrate evolution have indeed been found. A clear line of fossils now traces the transition be- tween whales and hoofed mammals, between reptiles and mammals, between dinosaurs and birds, between apes and humans. The fossil evidence of evolution between major forms is compelling. 3. The intelligent design argument. “The organs of living creatures are too complex for a random process to have produced—the existence of a clock is evidence of the existence of a clockmaker.” Biologists do not agree. The intermediates in the evolution of the mam- malian ear can be seen in fossils, and many interme- diate “eyes” are known in various invertebrates. These intermediate forms arose because they have value—being able to detect light a little is better than not being able to detect it at all. Complex structures like eyes evolved as a progression of slight improvements. 4. Evolution violates the Second Law of Thermody- namics. “A jumble of soda cans doesn't by itself jump neatly into a stack—things become more disorganized due to random events, not more organized.” Biologists point out that this argument ignores what the second law really says: disorder increases in a closed system, which the earth most certainly is not. Energy contin- ually enters the biosphere from the sun, fueling life and all the processes that organize it. 5. Proteins are too improbable. “Hemoglobin has 141 amino acids. The probability that the first one would be leucine is 1/20, and that all 141 would be the ones they are by chance is (1/20) 141 , an impossibly rare event.” This is statistical foolishness—you cannot use probability to argue backwards. The probability that a student in a classroom has a particular birthday is 1/365; arguing this way, the probability that everyone in a class of 50 would have the birthdays they do is (1/365) 50 , and yet there the class sits. 6. Natural selection does not imply evolution. “No scientist has come up with an experiment where fish evolve into frogs and leap away from predators.” Is microevolu- tion (evolution within a species) the mechanism that has produced macroevolution (evolution among species)? Most biologists that have studied the prob- lem think so. Some kinds of animals produced by ar- tificial selection are remarkably distinctive, such as Chihuahuas, dachshunds, and greyhounds. While all dogs are in fact the same species and can interbreed, laboratory selection experiments easily create forms that cannot interbreed and thus would in nature be considered different species. Thus, production of rad- ically different forms has indeed been observed, re- peatedly. To object that evolution still does not ex- plain really major differences, like between fish and amphibians, simply takes us back to point 2—these changes take millions of years, and are seen clearly in the fossil record. 7. The irreducible complexity argument. The in- tricate molecular machinery of the cell cannot be ex- plained by evolution from simpler stages. Because each part of a complex cellular process like blood clotting is es- sential to the overall process, how can natural selection fashion any one part? What's wrong with this argu- ment is that each part of a complex molecular ma- chine evolves as part of the system. Natural selection can act on a complex system because at every stage of its evolution, the system functions. Parts that im- prove function are added, and, because of later changes, become essential. The mammalian blood clotting system, for example, has evolved from much simpler systems. The core clotting system evolved at the dawn of the vertebrates 600 million years ago, and is found today in lampreys, the most primitive fish. One hundred million years later, as vertebrates evolved, proteins were added to the clotting system making it sensitive to substances released from dam- aged tissues. Fifty million years later, a third compo- nent was added, triggering clotting by contact with the jagged surfaces produced by injury. At each stage as the clotting system evolved to become more complex, its overall performance came to depend on the added elements. Thus, blood clotting has be- come "irreducibly complex"—as the result of Dar- winian evolution. Darwin’s theory of evolution has proven controversial among the general public, although the commonly raised objections are without scientific merit. Chapter 21 The Evidence for Evolution 455 21.4 The theory of evolution has proven controversial. 456 Part VI Evolution Chapter 21 Summary Questions Media Resources 21.1 Fossil evidence indicates that evolution has occurred. ? Fossils of many extinct species have never been discovered. Nonetheless, the fossil record is complete enough to allow a detailed understanding of the evolution of life through time. The evolution of the major vertebrate groups is quite well known. ? Although evolution of groups like horses may appear to be a straight-line progression, in fact there have been many examples of parallel evolution, and even reversals from overall trends. 1. Why do gaps exist in the fossil record? What lessons can be learned from the fossil record of horse evolution? 2. How did scientists date fossils in Darwin’s day? Why are scientists today able to date rocks more accurately? ? Natural populations provide clear evidence of evolutionary change. ? Darwin’s finches have different-sized beaks, which are adaptations to eating different kinds of seeds. In particularly dry years, natural selection favors birds with stout beaks within one species, Geospiza fortis. As a result, the average bill size becomes larger in the next generation. ? The British populations of the peppered moth, Biston betularia, consisted mostly of light-colored individuals before the Industrial Revolution. Over the last two centuries, populations that occur in heavily polluted areas, where the tree trunks are darkened with soot, have come to consist mainly of dark-colored (melanic) individuals—a result of rapid natural selection. 3. Why did the average beak size of the medium ground finch increase after a particularly dry year? 4. Why did the frequency of light-colored moths decrease and that of dark-colored moths increase with the advent of industrialism? What is industrial melanism? 5. What can artificial selection tell us about evolution? Is artificial selection a good analogy for the selection that occurs in nature? 21.2 Natural selection can produce evolutionary change. ? Several indirect lines of evidence argue that macroevolution has occurred, including successive changes in homologous structures, developmental patterns, vestigial structures, parallel patterns of evolution, and patterns of distribution. ? When differences in genes or proteins are examined, species that are thought to be closely related based on the fossil record may be more similar than species thought to be distantly related. 6. What is homology? How does it support evolutionary theory? 7. What is convergent evolution? Give examples. 8. How did Darwin’s studies of island populations provide evidence for evolution? 21.3 Evidence for evolution can be found in other fields of biology. ? The objections raised by Darwin’s critics are easily answered. 9. Is “Darwinism” really science? Explain. 21.4 The theory of evolution has proven controversial. ? On Science Article: featherd Dinosaurs Book Reviews: ? In Search of Deep Time by Gee ? Digging Dinosaurs by Horner ? Activity: Evolution of Fish ? Exploration: Evolution of the Heart ? Molecular Clock ? Activity: Divergence ? Student Research: Evolution of Insect Diets On Science Articles: ? Darwinism at the Cellular Level ? Was Darwin Wrong? ? On Science Article: Answering Evolution’s Critics ? Bioethics Case Study: Creationism Book Reviews: ? Mr. Darwin’s Shooter by McDonald http://www.mhhe.com/raven6e http://www.biocourse.com 457 22 The Origin of Species Concept Outline 22.1 Species are the basic units of evolution. The Nature of Species. Species are groups of actually or potentially interbreeding natural populations which are reproductively isolated from other such groups and that maintain connectedness over geographic distances. 22.2 Species maintain their genetic distinctiveness through barriers to reproduction. Prezygotic Isolating Mechanisms. Some breeding barriers prevent the formation of zygotes. Postzygotic Isolating Mechanisms. Other breeding barriers prevent the proper development or reproduction of the zygote after it forms. 22.3 We have learned a great deal about how species form. Reproductive Isolation May Evolve as a By-Product of Evolutionary Change. Speciation can occur in the absence of natural selection, but reproductive isolation generally occurs more quickly when populations are adapting to different environments. The Geography of Speciation. Speciation occurs most readily when populations are geographically isolated. Sympatric speciation can occur by polyploidy and, perhaps, by other means. 22.4 Clusters of species reflect rapid evolution. Darwin’s Finches. Thirteen species of finches, all descendants of one ancestral finch, occupy diverse niches. Hawaiian Drosophila. More than a quarter of the world’s fruit fly species are found on the Hawaiian Islands. Lake Victoria Cichlid Fishes. Isolation has led to extensive species formation among these small fishes. New Zealand Alpine Buttercups. Repeated glaciations have fostered waves of species formation in alpine plants. Diversity of Life through Time. The number of species has increased through time, despite a number of mass extinction events. The Pace of Evolution. The idea that evolution occurs in spurts is controversial. Problems with the Biological Species Concept. This concept is not as universal as previously thought. A lthough Darwin titled his book On the Origin of Species, he never actually discussed what he referred to as that “mystery of mysteries” of how one species gives rise to an- other. Rather, his argument concerned evolution by natural selection; that is, how one species evolves through time to adapt to its changing environment. Although of fundamen- tal importance to evolutionary biology, the process of adap- tation does not explain how one species becomes another (figure 22.1); much less can it explain how one species can give rise to many descendant species. As we shall see, adap- tation may be involved in this process of speciation, but it need not be. FIGURE 22.1 A group of Galápagos iguanas bask in the sun on their isolated island. How does geographic isolation contribute to the formation of new species? Occasionally, two species occur together that appear to be nearly identical, and are thus called sibling species. In most cases, however, our inability to distinguish the two re- flects our own reliance on vision as our primary sense. When the mating calls or chemicals exuded by such species are examined, they usually reveal great differences. In other words, even though we have trouble separating them, the animals themselves have no such difficulties! Geographic Variation within Species Within the units classified as species, populations that occur in different areas may be more or less distinct from one an- other. Such groups of distinctive individuals may be classi- fied taxonomically as subspecies or varieties (the vague term “race” has a similar connotation, but is no longer com- monly used). In areas where these populations approach one another, individuals often exhibit combinations of features characteristic of both populations. In other words, even though geographically distant populations may appear dis- tinct, they usually are connected by intervening populations that are intermediate in their characteristics (figure 22.3). The Biological Species Concept What can account both for the distinctiveness of sympatric species and the connectedness of geographic populations of the same species? One obvious possibility is that each species exchanges genetic material only with other mem- bers of its species. If sympatric species commonly ex- 458 Part VI Evolution The Nature of Species Before we can discuss how one species gives rise to another, we need to understand exactly what a species is. Even though definition of what constitutes a species is of funda- mental importance to evolutionary biology, this issue has still not been completely settled and is currently the subject of considerable research and debate. However, any concept of a species must account for two phenomena: the distinc- tiveness of species that occur together at a single locality, and the connection that exists among populations of the same species that are geographically separated. The Distinctiveness of Sympatric Species Put out a birdfeeder on your balcony or back porch and you will attract a wide variety of different types of birds (es- pecially if you put out a variety of different kinds of foods). In the midwestern United States, for example, you might routinely see cardinals, blue jays, downy woodpeckers, house finches—even hummingbirds in the summer (figure 22.2). Although it might take a few days of careful observa- tion, you would soon be able to readily distinguish the many different species. The reason is that species that occur together (termed sympatric from the Greek sym for “same” and patria for “species”) are distinctive entities that are phenotypically different, utilize different parts of the habitat, and behave separately. This observation is gener- ally true not only for birds, but also for most other types of organisms in most places. 22.1 Species are the basic units of evolution. Northern cardinal Blue jay Downy woodpecker House finch Ruby-throated hummingbird FIGURE 22.2 Common birds in the midwestern United States. No one would doubt that these birds are distinct species. Each can be distinguished from the others by many ecological, behavioral, and phenotypic traits. changed genes, we might expect such species to rapidly lose their distinctions as the gene pools of the different species became homogenized. Conversely, the ability of geographi- cally distant populations to share genes through the process of gene flow may keep these populations integrated as members of the same species. Based on these ideas, the evolutionary biologist Ernst Mayr coined the biological species concept which defines species as: “. . . groups of actually or potentially interbreeding natural populations which are reproductively isolated from other such groups.” In other words, the biological species concept says that a species is all individuals that are capable of interbreeding and producing fertile offspring. Conversely, individuals that cannot produce fertile offspring are said to be repro- ductively isolated and, thus, members of different species. Occasionally, members of different species will inter- breed, a process termed hybridization. If the species are reproductively isolated, either no offspring will result, or if offspring are produced, they will be either unhealthy or sterile. In this way, genes from one species generally will not be able to enter the gene pool of another species. Problems with Applying the Biological Species Concept The biological species concept has proven to be an effec- tive way of understanding the existence of species in nature. Nonetheless, the concept has some practical difficulties. For example, it can be difficult to apply the concept to pop- ulations that do not occur together in nature (and are thus said to be allopatric). Because individuals of these popula- tions do not encounter each other, it is not possible to ob- serve whether they would interbreed naturally. Although experiments can determine whether fertile hybrids can be produced, this information is not enough. The reason is that many species that will coexist without interbreeding in nature will readily hybridize in the artificial settings of the laboratory or zoo. Consequently, evaluating whether al- lopatric populations constitute different species is ulti- mately a judgment call. In addition, the concept is more limited than its name would imply. Many organisms are asexual and reproduce without mating; reproductive isolation has no meaning for such organisms. Moreover, despite its name, the concept is really a zoo- logical species concept and applies less readily to plants. Even among animals, the biological species concept ap- pears to apply more successfully to some groups than to others. As we will see in section 22.4, biologists are cur- rently reevaluating this and other approaches to the study of species. Species are groups of organisms that are distinct from other co-occurring species and that are interconnected geographically. The ability to exchange genes appears to be a hallmark of such species. Chapter 22 The Origin of Species 459 Red milk snake (Lampropeltis triangulum syspila) Eastern milk snake (Lampropeltis triangulum triangulum) Scarlet kingsnake (Lampropeltis triangulum elapsoides) “Intergrade” form FIGURE 22.3 Geographic variation in the milk snake, Lampropeltis triangulum. Although each subspecies appears phenotypically quite distinctive from the others, they are connected by populations that are phenotypically intermediate. Prezygotic Isolating Mechanisms How do species keep their separate identities? Reproduc- tive isolating mechanisms fall into two categories: prezy- gotic isolating mechanisms, which prevent the formation of zygotes; and postzygotic isolating mechanisms, which prevent the proper functioning of zygotes after they form. In the following sections we will discuss various isolating mechanisms in these two categories and offer examples that illustrate how the isolating mechanisms operate to help species retain their identities. Ecological Isolation Even if two species occur in the same area, they may utilize different portions of the environment and thus not hy- bridize because they do not encounter each other. For ex- ample, in India, the ranges of lions and tigers overlapped until about 150 years ago. Even when they did, however, there were no records of natural hybrids. Lions stayed mainly in the open grassland and hunted in groups called prides; tigers tended to be solitary creatures of the forest (figure 22.4). Because of their ecological and behavioral dif- ferences, lions and tigers rarely came into direct contact with each other, even though their ranges overlapped over thousands of square kilometers. In another example, the ranges of two toads, Bufo wood- housei and B. americanus, overlap in some areas. Although these two species can produce viable hybrids, they usually do not interbreed because they utilize different portions of the habitat for breeding. Whereas B. woodhousei prefers to breed in streams, B. americanus breeds in rainwater puddles. Similarly, the ranges of two species of dragon- flies overlap in Florida. However, the dragonfly Progom- phus obscurus lives near rivers and streams, and P. alachue- nis lives near lakes. Similar situations occur among plants. Two species of oaks occur widely in California: the valley oak, Quercus lo- bata, and the scrub oak, Q. dumosa. The valley oak, a graceful deciduous tree that can be as tall as 35 meters, occurs in the fertile soils of open grassland on gentle slopes and valley floors. In contrast, the scrub oak is an evergreen shrub, usually only 1 to 3 meters tall, which often forms the kind of dense scrub known as chaparral. The scrub oak is found on steep slopes in less fertile soils. Hybrids between these different oaks do occur and are fully fertile, but they are rare. The sharply distinct habi- tats of their parents limit their occurrence together, and there is no intermediate habitat where the hybrids might flourish. 460 Part VI Evolution 22.2 Species maintain their genetic distinctiveness through barriers to reproduction. FIGURE 22.4 Lions and tigers are ecologically isolated. The ranges of lions and tigers used to overlap in India. However, lions and tigers do not hybridize in the wild because they utilize different portions of the habitat. (a) Lions live in open grassland. (b) Tigers are solitary animals that live in the forest. (c) Hybrids, such as this tiglon, have been successfully produced in captivity, but hybridization does not occur in the wild. (a) (b) (c) Behavioral Isolation In chapter 27, we will consider the often elaborate courtship and mating rituals of some groups of animals. Related species of organisms such as birds often differ in their courtship rituals, which tends to keep these species distinct in nature even if they inhabit the same places (fig- ure 22.5). For example, mallard and pintail ducks are per- haps the two most common freshwater ducks in North America. In captivity, they produce completely fertile off- spring, but in nature they nest side-by-side and only rarely hybridize. More than 500 species of flies of the genus Drosophila live in the Hawaiian Islands. This is one of the most re- markable concentrations of species in a single animal genus found anywhere. The genus occurs throughout the world, but nowhere are the flies more diverse in external appearance or behavior than in Hawaii. Many of these flies differ greatly from other species of Drosophila, ex- hibiting characteristics that can only be described as bizarre. The Hawaiian species of Drosophila are long-lived and often very large compared with their relatives on the main- land. The females are more uniform than the males, which are often bizarrely distinctive. The males display complex territorial behavior and elaborate courtship rituals. The mating behavior patterns among Hawaiian species of Drosophila are of great importance in maintaining the distinctiveness of the individual species. For example, de- spite the great differences between them, D. heteroneura and D. silvestris are very closely related. Hybrids between them are fully fertile. The two species occur together over a wide area on the island of Hawaii, yet hybridiza- tion has been observed at only one locality. The very dif- ferent and complex behavioral characteristics of these flies obviously play a major role in maintaining their dis- tinctiveness. Other Prezygotic Isolating Mechanisms Temporal Isolation. Lactuca graminifolia and L. canadensis, two species of wild lettuce, grow together along roadsides throughout the southeastern United States. Hybrids between these two species are easily made experimentally and are completely fertile. But such hybrids are rare in nature because L. graminifolia flowers in early spring and L. canadensis flowers in summer. When their blooming periods overlap, as they do occa- sionally, the two species do form hybrids, which may be- come locally abundant. Many species of closely related amphibians have differ- ent breeding seasons that prevent hybridization between the species. For example, five species of frogs of the genus Rana occur together in most of the eastern United States, but hybrids are rare because the peak breeding time is dif- ferent for each of them. Mechanical Isolation. Structural differences prevent mating between some related species of animals. Aside from such obvious features as size, the structure of the male and female copulatory organs may be incompatible. In many insect and other arthropod groups, the sexual organs, particularly those of the male, are so diverse that they are used as a primary basis for classification. Similarly, flowers of related species of plants often differ significantly in their proportions and structures. Some of these differences limit the transfer of pollen from one plant species to another. For example, bees may pick up the pollen of one species on a certain place on their bodies; if this area does not come into contact with the receptive structures of the flowers of another plant species, the pollen is not transferred. Prevention of Gamete Fusion. In animals that shed their gametes directly into water, eggs and sperm derived from different species may not attract one another. Many land animals may not hybridize successfully because the sperm of one species may function so poorly within the re- productive tract of another that fertilization never takes place. In plants, the growth of pollen tubes may be im- peded in hybrids between different species. In both plants and animals the operation of such isolating mechanisms prevents the union of gametes even following successful mating. Prezygotic isolating mechanisms lead to reproductive isolation by preventing the formation of hybrid zygotes. Chapter 22 The Origin of Species 461 FIGURE 22.5 Differences in courtship rituals can isolate related bird species. These Galápagos blue-footed boobies select their mates only after an elaborate courtship display. This male is lifting his feet in a ritualized high-step that shows off his bright blue feet. The display behavior of other species of boobies, some of which also occur in the Galápagos, is much different. Postzygotic Isolating Mechanisms All of the factors we have discussed up to this point tend to prevent hybridization. If hybrid matings do occur and zy- gotes are produced, many factors may still prevent those zygotes from developing into normally functioning, fertile individuals. Development in any species is a complex process. In hybrids, the genetic complements of two species may be so different that they cannot function together nor- mally in embryonic development. For example, hybridiza- tion between sheep and goats usually produces embryos that die in the earliest developmental stages. Leopard frogs (Rana pipiens complex) of the eastern United States are a group of similar species, assumed for a long time to constitute a single species (figure 22.6). How- ever, careful examination revealed that although the frogs appear similar, successful mating between them is rare be- cause of problems that occur as the fertilized eggs develop. Many of the hybrid combinations cannot be produced even in the laboratory. Examples of this kind, in which similar species have been recognized only as a result of hybridization experi- ments, are common in plants. Sometimes the hybrid em- bryos can be removed at an early stage and grown in an ar- tificial medium. When these hybrids are supplied with extra nutrients or other supplements that compensate for their weakness or inviability, they may complete their de- velopment normally. Even if hybrids survive the embryo stage, however, they may not develop normally. If the hybrids are weaker than their parents, they will almost certainly be elimi- nated in nature. Even if they are vigorous and strong, as in the case of the mule, a hybrid between a horse and a donkey, they may still be sterile and thus incapable of contributing to succeeding generations. Sterility may re- sult in hybrids because the development of sex organs may be abnormal, the chromosomes derived from the re- spective parents may not pair properly, or from a variety of other causes. Postzygotic isolating mechanisms are those in which hybrid zygotes fail to develop or develop abnormally, or in which hybrids cannot become established in nature. 462 Part VI Evolution (1) (2) (3) (4) FIGURE 22.6 Postzygotic isolation in leopard frogs. Numbers indicate the following species in the geographical ranges shown: (1) Rana pipiens; (2) Rana blairi; (3) Rana utricularia; (4) Rana berlandieri. These four species resemble one another closely in their external features. Their status as separate species was first suspected when hybrids between them produced defective embryos in some combinations. Subsequent research revealed that the mating calls of the four species differ substantially, indicating that the species have both pre- and postzygotic isolating mechanisms. Chapter 22 The Origin of Species 463 One of the oldest questions in the field of evo- lution is: how does one ancestral species be- come divided into two descendant species? If species are defined by the existence of repro- ductive isolation, then the process of speciation equates with the evolution of reproductive iso- lating mechanisms. How do reproductive isolat- ing mechanisms evolve? Reproductive Isolation May Evolve as a By-Product of Evolutionary Change Most reproductive isolating mechanisms ini- tially arise for some reason other than to pro- vide reproductive isolation. For example, a population that colonizes a new habitat may evolve adaptations for living in that habitat. As a result, individuals from that population might never encounter individuals from the ancestral population. Even if they do meet, the population in the new habitat may have evolved new phenotypes or behavior so that members of the two populations no longer recognize each other as potential mates (figure 22.7). For this reason, some biologists believe that the term “isolating mechanisms” is mis- guided, because it implies that the traits evolved specifically for the purpose of geneti- cally isolating a species, which in most cases is probably incorrect. 22.3 We have learned a great deal about how species form. Prezygotic isolating mechanisms Postzygotic isolating mechanisms Fertilization Mating Geographic isolation Species occur in different places Behavioral isolation Species have different mating rituals Temporal isolation Mating or flowering occur during different seasons or at different times of the day Species 1 Species 2 Ecological isolation Species utilize different resources in the habitat Prevention of gamete fusion Gametes fail to attract each other or function poorly Hybrid embryos do not develop properly Fertile hybrid offspring Mechanical isolation Structural differences prevent mating or pollen transfer Hybrid adults do not survive in nature Hybrid adults are sterile or have reduced fertility FIGURE 22.7 Reproductive isolating mechanisms. A variety of different mechanisms can prevent successful reproduction between individuals of different species. Selection May Reinforce Isolating Mechanisms The formation of species is a continuous process, one that we can understand because of the existence of intermediate stages at all levels of differentiation. If populations that are partly differentiated come into contact with one another, they may still be able to interbreed freely, and the differ- ences between them may disappear over the course of time as genetic exchange homogenizes the populations. Con- versely, if the populations are reproductively isolated, then no genetic exchange will occur and the two populations will be different species. However, there is an intermediate situation in which reproductive isolation has partially evolved, but is not complete. As a result, hybridization will occur at least occasionally. If they are partly sterile, or not as well adapted to the existing habitats as their parents, these hy- brids will be at a disadvantage. As a result, selection would favor any alleles in the parental populations that prevented hybridization because individuals that avoided hybridizing would be more successful in passing their genes on to the next generation. The result would be the continual improvement of prezygotic isolating mecha- nisms until the two populations were completely repro- ductively isolated. This process is termed reinforcement because initially incomplete isolating mechanisms are re- inforced by natural selection until they are completely effective. Reinforcement is by no means inevitable, however. When incompletely isolated populations come together, gene flow immediately begins to occur between the species. Although hybrids may be inferior, they are not, in this case, completely inviable or infertile (if they were, then the species would be reproductively isolated); hence, when these hybrids reproduce with members of either population, they will serve as a conduit of genetic ex- change from one population to the other. As a result, the two populations will tend to lose their genetic distinctive- ness. Thus, a race ensues: can reproductive isolation be perfected before gene flow destroys the differences be- tween the populations? Experts disagree on the likely out- come, but many believe that reinforcement is the much less common outcome. The Role of Natural Selection in Speciation What role does natural selection play in the speciation process? Certainly, the process of reinforcement is driven by natural selection favoring the perfection of reproductive isolation. But, as we have seen, reinforcement may not be common. Is natural selection necessarily involved in the initial evolution of isolating mechanisms? Random Changes May Cause Reproductive Isolation As we discussed in chapter 20, populations may diverge for purely random reasons. Genetic drift in small popula- tions, founder effects, and population bottlenecks all may lead to changes in traits that cause reproductive isolation. For example, in the Hawaiian Islands, closely related species of Drosophila often differ greatly in their courtship behavior. Colonization of new islands by these fruit flies probably involves a founder effect, in which one or a few fruit flies—perhaps only a single pregnant female—is blown by strong winds to a new island. Changes in courtship behavior between ancestor and descendant populations may be the result of such founder events. Given long enough periods of time, any two isolated populations will diverge due to genetic drift. In some cases, this random divergence may affect traits responsi- ble for reproductive isolation, and speciation will have occurred. Adaptation and Speciation Nonetheless, adaptation and speciation are probably re- lated in many cases. As species adapt to different circum- stances, they will accumulate many differences that may lead to reproductive isolation. For example, if one popula- tion of flies adapts to wet conditions and another to dry conditions, then the populations will evolve a variety of dif- ferences in physiological and sensory traits; these differ- ences may promote ecological and behavioral isolation and may cause any hybrids they produce to be poorly adapted to either habitat. Selection might also act directly on mating behavior. Male Anolis lizards, for example, court females by extend- ing a colorful flap of skin, called a “dewlap,” that is lo- cated under their throat (figure 22.8). The ability of one lizard to see the dewlap of another lizard depends not only on the color of the dewlap, but the environment in which they occur. As a result, a light-colored dewlap is most effective in reflecting light in a dim forest, whereas dark colors are more apparent in the bright glare of open habitats. As a result, when these lizards occupy new habi- tats, natural selection will favor evolutionary change in dewlap color because males whose dewlaps cannot be seen will attract few mates. However, the lizards also distin- guish members of their own species from those of other species by the color of the dewlap. Hence, adaptive change in mating behavior could have the incidental con- sequence of causing speciation. Laboratory scientists have conducted experiments on fruit flies and other organisms in which they isolate popula- 464 Part VI Evolution tions in different laboratory chambers and measure how much reproductive isolation evolves. These experiments in- dicate that genetic drift by itself can lead to some degree of reproductive isolation, but, in general, reproductive isola- tion evolves more rapidly when the populations are forced to adapt to different laboratory environments (such as tem- perature or food type). Reproductive isolating mechanisms can evolve either through random changes or as an incidental by- product of adaptive evolution. Under some circumstances, however, natural selection can directly select for traits that increase the reproductive isolation of a species. Chapter 22 The Origin of Species 465 FIGURE 22.8 Dewlaps of several different species of Caribbean Anolis lizards. Males use their dewlaps in both territorial and courtship displays. Coexisting species almost always differ in their dewlaps, which are used in species recognition. Some dewlaps are easier to see in open habitats, whereas others are more visible in shaded environments. (a) Anolis carolinensis. (b) Anlois sagrei. (c) Anolis grahami. (d) Species name to come. The Geography of Speciation Speciation is a two-part process. First, initially identical populations must diverge and, second, reproductive isola- tion must evolve to maintain these differences. The diffi- culty with this process, as we have seen, is that the homog- enizing effect of gene flow between populations will constantly be acting to erase any differences that may arise, either by genetic drift or natural selection. Of course, gene flow only occurs between populations that are in contact. Consequently, evolutionary biologists have long recognized that speciation is much more likely in geographically iso- lated populations. Allopatric Divergence Is the Primary Means of Speciation Ernst Mayr was the first biologist to strongly make the case for allopatric speciation. Marshalling data from a wide variety of organisms and localities, Mayr was clearly able to demonstrate that geographically separated popu- lations appear much more likely to have evolved substan- tial differences leading to speciation. For example, the Papuan kingfisher, Tanysiptera hydrocharis, varies little throughout its wide range in New Guinea despite the great variation in the island’s topography and climate. By contrast, isolated populations on nearby islands are strik- ingly different from each other and from the mainland population (figure 22.9). Many other examples indicate that speciation can occur in allopatry. Given that one would expect isolated populations to diverge over time by either drift or selec- tion, this result is not surprising. Rather, the question be- comes: Is geographic isolation required for speciation to occur? Whether Speciation Can Occur in Sympatry Is Controversial As we saw in chapter 20, disruptive selection can cause a population to contain individuals exhibiting two different phenotypes. One might think that if selection were strong enough, these two phenotypes would evolve into different species. However, before the two phenotypes could be- come different species, they would have to evolve repro- ductive isolating mechanisms. Because the two phenotypes would initially not be reproductively isolated at all, genetic exchange between individuals of the two phenotypes would tend to prevent genetic divergence in mating preferences or other isolating mechanisms. As a result, the two pheno- 466 Part VI Evolution PACIFIC OCEAN New Guinea FIGURE 22.9 Phenotypic differentiation in the Papuan kingfisher in New Guinea. Isolated island populations (above left) are quite distinctive, showing variation in tail feather structure and length, plumage coloration, and bill size, whereas kingfishers on the mainland (above right) show little variation. types would be retained as polymorphisms within a single population. For this reason, most biologists consider sym- patric speciation a rare event. Nonetheless, in recent years, a number of cases have appeared that appear difficult to interpret in any way other than sympatric speciation. For example, the vol- canic crater lake Barombi Mbo in Cameroon is extremely small and ecologically homogeneous, with no opportunity for within-lake isolation. Nonetheless, 11 species of closely related cichlid fish occur in the lake; all of the species are more closely related evolutionarily to each other than to any species outside of the crater. The most reasonable explanation is that an ancestral species colo- nized the crater and subsequently speciated in sympatry multiple times. Genetic Changes Underlying Speciation How much divergence does it take to create a new species? How many gene changes does it take? Since Dar- win, the traditional view has been that new species arise by the accumulation of many small genetic differences. While there is little doubt that many species have formed in this gradual way, new techniques of molecular biology suggest that in at least some cases, the evolution of a new species may involve very few genes. Studying two species of monkeyflower found in the western United States, re- searchers found that only a few genes separate the two species, even though at first glance the two species appear to be very different (figure 22.10). Using gene technolo- gies like those described in chapter 19, the researchers found that all of the major differences in the flowers, in- cluding not only flower shape and color, but also nectar production, were attributable to several genes, each of which had great phenotypic effects. Because individual genes have such powerful effects, species as different as these two can evolve in relatively few steps. The Role of Polyploidy in Species Formation Among plants, fertile individuals often arise from sterile ones through polyploidy, which doubles the chromo- some number of the original sterile hybrid individual. A polyploid cell, tissue, or individual has more than two sets of chromosomes. Polyploid cells and tissues occur spontaneously and reasonably often in all organisms, al- though in many they are soon eliminated. A hybrid may be sterile simply because its sets of chromosomes, de- rived from male and female parents of different species, do not pair with one another. If the chromosome num- ber of such a hybrid doubles, the hybrid, as a result of the doubling, will have a duplicate of each chromosome. In that case, the chromosomes will pair, and the fertility of the polyploid hybrid individual may be restored. It is estimated that about half of the approximately 260,000 species of plants have a polyploid episode in their his- tory, including many of great commercial importance, such as bread wheat, cotton, tobacco, sugarcane, ba- nanas, and potatoes. As you might imagine, the advan- tages a polyploid plant offers for natural selection can be substantial as a result of their great levels of genetic vari- ation; hence, the significance of polyploidy in the evolu- tion of plants. Because polyploid plants cannot reproduce with their ancestors, reproductive isolation can evolve in one step. Consequently, speciation by polyploidy is one uncontro- versial means of sympatric speciation. Although much rarer than in plants, speciation by polyploidy is also known from a variety of animals, including insects, fish, and salamanders. Speciation occurs much more readily in the absence of gene flow among populations. However, speciation can occur in sympatry by means of polyploidy, and perhaps in other cases also. Chapter 22 The Origin of Species 467 FIGURE 22.10 Differences between species can result from a few genes that have major effects. (a) Mimulus lewisii has pale pink flowers and concentrated nectar, which are optimal for attracting bumblebees to serve as pollinators. (b) By contrast, M. cardinalis has the red flowers and copious dilute nectar typical of hummingbird-pollinated plants. Differences in flower shape and color are the result of a few genes of large effect. (a) Mimulus lewisii (b) Mimulus cardinalis Darwin’s Finches One of the most visible manifestations of evolution is the existence of groups of closely related species that have re- cently evolved from a common ancestor by occupying different habitats. This type of adaptive radiation oc- curred among the 13 species of Darwin’s finches on the Galápagos Islands. Presumably, the ancestor of Darwin’s finches reached these islands before other land birds, and all of the types of habitats where birds occur on the mainland were unoccupied. As the new arrivals moved into these vacant ecological niches and adopted new lifestyles, they were subjected to diverse sets of selective pressures. Under these circumstances, and aided by the geographic isolation afforded by the many islands of the Galápagos archipelago, the ancestral finches rapidly split into a series of diverse populations, some of which evolved into separate species. These species now occupy many different kinds of habitats on the Galápagos Islands (figure 22.11), habitats comparable to those several dis- tinct groups of birds occupy on the mainland. The 13 species comprise four groups: 1. Ground finches. There are six species of Geospiza ground finches. Most of the ground finches feed on seeds. The size of their bills is related to the size of the seeds they eat. Some of the ground finches feed primarily on cactus flowers and fruits and have a longer, larger, more pointed bill than the others. 2. Tree finches. There are five species of insect- eating tree finches. Four species have bills that are suitable for feeding on insects. The woodpecker finch has a chisel-like beak. This unusual bird carries around a twig or a cactus spine, which it uses to probe for insects in deep crevices. 3. Warbler finch. This unusual bird plays the same ecological role in the Galápagos woods that warblers play on the mainland, searching continually over the leaves and branches for insects. It has a slender, warbler-like beak. 4. Vegetarian finch. The very heavy bill of this bud- eating bird is used to wrench buds from branches. Darwin’s finches, all derived from one similar mainland species, have radiated widely on the Galápagos Islands in the absence of competition. 468 Part VI Evolution 22.4 Clusters of species reflect rapid evolution. G r o u n d f i n c h e s W a rb ler fi n ch T r e e f i n c h e s Ca ct u s ea te r G r a s p i n g b i l l s P a r r o t - l i k e b i l l C r u s h i n g b i l l s Warbler finch (Certhidea olivacea) Woodpecker finch (Cactospiza pallida) Small insectivorous tree finch (C. parvulus) Large insectivorous tree finch (C. psittacula) Vegetarian tree finch (Platyspiza crassirostris) Cactus ground finch (Geospiza scandens) Sharp-beaked ground finch (G. difficilis) Small ground finch (G. fuliginosa) Medium ground finch (G. fortis) Large ground finch (G. magnirostris) Insect eaters Bud eater Seed eaters P ro b in g b ills FIGURE 22.11 Darwin’s finches. Ten of the 13 Galápagos species of Darwin’s finches occur on Isla Santa Cruz, one of the Galápagos Islands. These species show differences in bills and feeding habits. The bills of several of these species resemble those of distinct families of birds on the mainland. This condition presumably arose when the finches evolved new species in habitats lacking small birds. The woodpecker finch uses cactus spines to probe in crevices of bark and rotten wood for food. Scientists believe all of these birds derived from a single common ancestor. Hawaiian Drosophila Our second example of a cluster of species is the fly genus Drosophila on the Hawaiian Islands, which we men- tioned earlier as an example of behavioral isolation. There are at least 1250 species of this genus throughout the world, and more than a quarter are found only in the Hawaiian Islands (figure 22.12). New species of Drosophila are still being discovered in Hawaii, although the rapid destruction of the native vegetation is making the search more difficult. Aside from their sheer number, Hawaiian Drosophila species are unusual because of the morphological and behavioral traits discussed earlier. No comparable species of Drosophila are found anywhere else in the world. A second, closely related genus of flies, Scaptomyza, also forms a species cluster in Hawaii, where it is represented by as many as 300 species. A few species of Scaptomyza are found outside of Hawaii, but the genus is better repre- sented there than elsewhere. In addition, species intermedi- ate between Scaptomyza and Drosophila exist in Hawaii, but nowhere else. The genera are so closely related that scien- tists have suggested that all of the estimated 800 species of these two genera that occur in Hawaii may have derived from a single common ancestor. The native Hawaiian flies are closely associated with the remarkable native plants of the islands and are often abundant in the native vegetation. Evidently, when their ancestors first reached these islands, they encountered many “empty” habitats that other kinds of insects and other animals occupied elsewhere. The evolutionary op- portunities the ancestral Drosophila flies found were simi- lar to those the ancestors of Darwin’s finches in the Galá- pagos Islands encountered, and both groups evolved in a similar way. Many of the Hawaiian Drosophila species are highly selective in their choice of host plants for their lar- vae and in the part of the plant they use. The larvae of various species live in rotting stems, fruits, bark, leaves, or roots, or feed on sap. New islands have continually arisen from the sea in the region of the Hawaiian Islands. As they have done so, they appear to have been invaded successively by the various Drosophila groups present on the older islands. New species have evolved as new islands have been colonized. The Hawaiian species of Drosophila have had even greater evolu- tionary opportunities than Darwin’s finches because of their restricted ecological niches and the variable ages of the islands. They clearly tell one of the most unusual evolu- tionary stories found anywhere in the world. The adaptive radiation of about 800 species of the flies Drosophila and Scaptomyza on the Hawaiian Islands, probably from a single common ancestor, is one of the most remarkable examples of intensive species formation found anywhere on earth. Chapter 22 The Origin of Species 469 (a) Drosophila mulli (b) Drosophila digressa FIGURE 22.12 Hawaiian Drosophila. The hundreds of species that have evolved on the Hawaiian Islands are extremely variable in appearance, although genetically almost identical. Lake Victoria Cichlid Fishes Lake Victoria is an immense shallow freshwater sea about the size of Switzerland in the heart of equatorial East Africa, until recently home to an incredibly diverse collec- tion of over 300 species of cichlid fishes. Recent Radiation This cluster of species appears to have evolved recently and quite rapidly. By sequencing the cytochrome b gene in many of the lake’s fish, scientists have been able to estimate that the first cichlids entered Lake Victoria only 200,000 years ago, colonizing from the Nile. Dramatic changes in water level encouraged species formation. As the lake rose, it flooded new areas and opened up new habitat. Many of the species may have originated after the lake dried down 14,000 years ago, isolating local populations in small lakes until the water level rose again. Cichlid Diversity These small, perchlike fishes range from 2 to 10 inches in length, and the males come in endless varieties of colors. The most diverse assembly of vertebrates known to sci- ence, the Lake Victoria cichlids defy simple description. We can gain some sense of the vast range of types by looking at how different species eat. There are mud biters, algae scrapers, leaf chewers, snail crushers, snail shellers (who pounce on slow-crawling snails and spear their soft parts with long curved teeth before the snail can retreat into its shell), zooplankton eaters, insect eaters, prawn eaters, and fish eaters. Scale-scraping cich- lids rasp slices of scales off of other fish. There are even cichlid species that are “pedophages,” eating the young of other cichlids. Cichlid fish have a remarkable trait that may have been instrumental in this evolutionary radiation: a second set of functioning jaws occurs in the throats of cichlid fish (figure 22.13)! The ability of these jaws to manipulate and process food has freed the oral jaws to evolve for other purposes, and the result has been the incredible diversity of ecologi- cal roles filled by these fish. Abrupt Extinction Much of this diversity is gone. In the 1950s, the Nile perch, a commercial fish with a voracious appetite, was introduced on the Ugandan shore of Lake Victoria. Since then it has spread through the lake, eating its way through the cich- lids. By 1990 all the open-water cichlid species were ex- tinct, as well as many living in rocky shallow regions. Over 70% of all the named Lake Victoria cichlid species had dis- appeared, as well as untold numbers of species that had yet to be described. Very rapid speciation occurred among cichlid fishes isolated in Lake Victoria, but widespread extinction followed when the isolation ended. 470 Part VI Evolution Fish eater Snail eater Algae scraper Zooplankton eater Leaf eater Second set of jaws Insect eater FIGURE 22.13 Cichlid fishes of Lake Victoria. These fishes have evolved adaptations to use a variety of different habitats. The second set of jaws located in the throat of these fish has provided evolutionary flexibility, allowing oral jaws to be modified in many ways. New Zealand Alpine Buttercups Adaptive radiations as we have described in Galápagos finches, Hawaiian Drosophila, and cichlid fishes seem to be favored by periodic isolation. Finches and Drosophila invade new islands, local species evolve, and they in turn reinvade the home island, in a cycle of expanding diversity. Simi- larly, cichlids become isolated by falling water levels, evolv- ing separate species in isolated populations that later are merged when the lake’s water level rises again. A clear example of the role periodic isolation plays in species formation can be seen in the alpine buttercups (genus Ranunculus) which grow among the glaciers of New Zealand (figure 22.14). More species of alpine buttercup grow on the two islands of New Zealand than in all of North and South America combined. Detailed studies by the Canadian taxonomist Fulton Fisher revealed that the evolutionary mechanism responsible for inducing this di- versity is recurrent isolation associated with the recession of glaciers. The 14 species of alpine Ranunculus occupy five distinctive habitats within glacial areas: snowfields (rocky crevices among outcrops in permanent snowfields at 7000 to 9000 feet elevation); snowline fringe (rocks at lower mar- gin of snowfields between 4000 and 7000 ft); stony debris (scree slopes of exposed loose rocks at 2000 to 6000 ft); sheltered situations (shaded by rock or shrubs at 1000 to 6000 ft); and boggy habitats (sheltered slopes and hollows, poorly drained tussocks at elevations between 2500 and 5000 ft). Ranunculus speciation and diversification has been pro- moted by repeated cycles of glacial advance and retreat. As the glaciers retreat, populations become isolated on moun- tain peaks, permitting speciation (figure 22.15). In the next advance, these new species can expand throughout the mountain range, coming into contact with their close rela- tives. In this way, one initial species could give rise to many descendants. Moreover, on isolated mountaintops during glacial retreats, species have convergently evolved to oc- cupy similar habitats; these distantly related but ecologi- cally similar species have then been brought back into con- tact in subsequent glacial advances. Recurrent isolation promotes species formation. Chapter 22 The Origin of Species 471 FIGURE 22.14 A New Zealand alpine buttercup. Fourteen species of alpine Ranunculus grow among the glaciers and mountains of New Zealand, including this R. lyallii, the giant buttercup. Glaciers link alpine zones into one continuous range. Mountain populations become isolated, permitting divergence and speciation. Alpine zones are reconnected. Separately evolved species come back into contact. Glaciers recede Glaciation FIGURE 22.15 Periodic glaciation encouraged species formation among alpine buttercups in New Zealand. The formation of extensive glaciers during the Pleistocene linked the alpine zones of many mountains together. When the glaciers receded, these alpine zones were isolated from one another, only to become reconnected with the advent of the next glacial period. During periods of isolation, populations of alpine buttercups diverged in the isolated habitats. Diversity of Life through Time Although eukaryotes evolved nearly 3 billion years ago, the diversity of life didn’t increase substantially until approxi- mately 550 million years ago. Then, almost all of the extant types of animals evolved in a geologically short period termed the “Cambrian explosion.” In addition to organisms whose descendants are recognizable today, a wide variety of other types of organisms also evolved (figure 22.16). The biology of these creatures, which quickly disappeared with- out leaving any descendants, is poorly understood. The Cambrian explosion seems to have been a time of evolu- tionary experimentation and innovation, in which many types of organisms appeared, but most were quickly weeded out. What prompted this explosion of diversity is still a subject of considerable controversy. 472 Part VI Evolution 2 3 6 5 1 4 7 8 9 10 11 12 13 14 15 16 17 FIGURE 22.16 Diversity of animals that evolved during the Cambrian explosion. In addition to the appearance of the ancestors of many present-day groups, such as insects and vertebrates, a variety of bizarre creatures evolved that left no descendants, such as Wiwaxia, Marrella, Opabinia, and the aptly named Hallucigenia. The natural history of these species is open to speculation. Key: (1) Amiskwia, (2) Odontogriphus, (3) Eldonia, (4) Halichondrites, (5) Anomalocaris canadensis, (6) Pikaia, (7) Canadia, (8) Marrella splendens, (9) Opabinia, (10) Ottoia, (11) Wiwaxia, (12) Yohoia, (13) Xianguangia, (14) Aysheaia, (15) Sidneyia, (16) Dinomischus, (17) Hallucigenia. Trends in Species Diversity The number of species in the world has increased vastly since the Cambrian. However, the trend has been far from consistent (figure 22.17). After a rapid rise, the number of species reached a plateau for about 200 million years ago; since then, the number has risen steadily. Interspersed in these patterns, however, have been a number of major setbacks, termed mass extinctions, in which the number of species has greatly decreased. Five major mass extinctions have been identified, the most se- vere of which occurred at the end of the Permian Period, approximately 225 million years ago, at which time more than half of all families and as many as 96% of all species may have perished. The most famous and well-studied extinction, though not as drastic, occurred at the end of the Cretaceous Period (63 million years ago), at which time the dinosaurs and a variety of other organisms went extinct. Recent studies have provided support for the hypothesis that this extinc- tion event was triggered by a large asteroid which slammed into the earth, perhaps causing global forest fires and ob- scuring the sun for months by throwing particles into the air. This mass extinction did have one positive effect, though: with the disappearance of dinosaurs, mammals, which previously had been small and inconspicuous, quickly experienced a vast evolutionary radiation, which ul- timately produced a wide variety of organisms, including elephants, tigers, whales, and humans. Indeed, a general observation is that biological diversity tends to rebound quickly after mass extinctions, reaching comparable levels of species richness, even if the organisms making up that diversity are not the same. A Sixth Extinction The number of species in the world in recent times is greater than it has ever been. Unfortunately, that number is decreasing at an alarming rate due to human activities. Some estimate that as many as one-fourth of all species will become extinct in the next 50 years, a rate of extinction not seen on earth since the Cretaceous mass extinction. The number of species has increased through time, although not at constant rates. Several major extinction events have substantially, though briefly, reduced the number of species. Chapter 22 The Origin of Species 473 Number o f fa milies Cambrian (570-505) Ordovician (505-438) Silurian (438-408) Devonian (408-360) Carboniferous (360-280) Permian (280-248) Triassic (248-213) Jurassic (213-144) Cretaceous (144-65) Tertiary (65-2) Millions of years ago 800 600 400 200 0 600 500 400 300 200 100 0 FIGURE 22.17 Diversity through time. Taxonomic diversity of families of marine animals since the Cambrian Period. The fossil record is most complete for marine organisms because they are more readily fossilized than terrestrial species. Families are shown, rather than species, because many species are known from only one specimen, thus introducing error into estimates of time of extinction. The Pace of Evolution Different kinds of organisms evolve at different rates. Mammals, for exam- ple, evolve relatively slowly. On the basis of a relatively complete fossil record, it has been estimated that an average value for the duration of a “typical” mammal species, from for- mation of the species to its extinction, might be about 200,000 years. Ameri- can paleontologist George Gaylord Simpson has pointed out that certain groups of animals, such as lungfishes, are apparently evolving even more slowly than mammals. In fact, Simp- son estimated that there has been lit- tle evolutionary change among lung- fishes over the past 150 million years, and even slower rates of evolution occur in other groups. Evolution in Spurts? Not only does the rate of evolution differ greatly from group to group, but evolution within a group appar- ently proceeds rapidly during some periods and relatively slowly during others. The fossil record provides evi- dence for such variability in evolution- ary rates, and evolutionists are very interested in understanding the factors that account for it. In 1972, paleontol- ogists Niles Eldredge of the American Museum of Natural History in New York and Stephen Jay Gould of Harvard University proposed that evolution normally proceeds in spurts. They claimed that the evo- lutionary process is a series of punctuated equilibria. Evolutionary innovations would occur and give rise to new lines; then these lines might persist unchanged for a long time, in “equilibrium.” Eventually there would be a new spurt of evolution, creating a “punctuation” in the fossil record. Eldredge and Gould contrast their theory of punctuated equilibrium with that of gradualism, or gradual evolutionary change, which they claimed was what Darwin and most earlier students of evolution had considered normal (figure 22.18). Eldredge and Gould proposed that stasis, or lack of evolutionary change, would be expected in large popula- tions experiencing stabilizing selection over long periods of time. In contrast, rapid evolution of new species might occur if populations colonized new areas. Such popula- tions would be small, isolated, and possibly already dif- fering from their parental population as a result of the founder effect. This, combined with selective pressures from a new environment, could bring about rapid change. Unfortunately, the distinctions are not as clear-cut as implied by this discussion. Some well-documented groups such as African mammals clearly have evolved gradually, and not in spurts. Other groups, like marine bryozoa, seem to show the irregular pattern of evolutionary change the punctuated equilibrium model predicts. It appears, in fact, that gradualism and punctuated equilibrium are two ends of a continuum. Although some groups appear to have evolved solely in a gradual manner and others only in a punctuated mode, many other groups appear to show evi- dence of both gradual and punctuated episodes at different times in their evolutionary history. The punctuated equilibrium model assumes that evolution occurs in spurts, between which there are long periods in which there is little evolutionary change. The gradualism model assumes that evolution proceeds gradually, with successive change in a given evolutionary line. 474 Part VI Evolution (a) Punctuated equilibrium (b) Gradualism T ime FIGURE 22.18 Two views of the pace of macroevolution. (a) Punctuated equilibrium surmises that species formation occurs in bursts, separated by long periods of quiet, while (b) gradualism surmises that species formation is constantly occurring. Problems with the Biological Species Concept Since the biological species concept was first proposed by Ernst Mayr in the 1940s, it has been the predominant idea of how to recognize and define species. However, in recent years, workers from a variety of fields have begun to ques- tion how universally applicable the concept really is. The Extent of Hybridization The crux of the matter concerns hybridization. Biological species are reproductively isolated, so that hybridization should be rare. If hybridization is common, one would ex- pect one of two quick outcomes: either reinforcement would occur, leading to the perfection of isolating mecha- nisms and an end to hybridization, or the two populations would merge together into a single homogeneous gene pool. However, in recent years biologists have detected much greater amounts of hybridization than previously realized between populations that seem to neither be experiencing reinforcement nor losing their specific identities. Botanists have always been aware that species can often experience substantial amounts of hybridization. One study found that more than 50% of the plant species surveyed in California were not well defined by genetic isolation. For example, the fossil record indicates that balsam poplars and cotton- woods have been phenotypically distinct for 12 million years, but throughout this time, they have routinely pro- duced hybrids. Consequently, for many years, many botanists have felt that the biological species concept only applies to animals. What is becoming increasingly evident, however, is that hybridization is not all that uncommon in animals, either. One recent survey indicated that almost 10% of the world’s 9500 bird species are known to have hy- bridized in nature. Recent years have seen the documen- tation of more and more cases in which substantial hy- bridization occurs between animal species. Again, the Galápagos finches provide a particularly well-studied ex- ample. Three species on the island of Daphne Major—the medium ground finch, the cactus finch, and the small ground finch—are clearly distinct morphologically and occupy different ecological niches. Careful studies over the past 20 years by Peter and Rosemary Grant found that, on average, 2% of the medium ground finches and 1% of the cactus finches mated with other species every year. Furthermore, hybrid offspring appeared to be at no disadvantage either in terms of survival or subsequent re- production. This is not a trivial amount of genetic ex- change, and one might expect to see the species coalesc- ing into one variable population, but the species are nonetheless maintaining their distinctiveness. Alternatives to the Biological Species Concept This is not to say hybridization is rampant throughout the animal world. As the bird survey indicated, 90% of bird species are not known to hybridize, and even fewer proba- bly experience significant amounts of hybridization. Still, it is a common enough occurrence to cast doubt about whether reproductive isolation is the only force maintain- ing the integrity of species. An alternative hypothesis is that the distinctions among species are maintained by natural selection. The idea is that each species has adapted to its own specific part of the envi- ronment. Stabilizing selection then maintains the species’ adaptations; hybridization has little effect because alleles introduced into the gene pool from other species quickly would be eliminated by natural selection. We have already seen in chapter 20 that the interac- tion between gene flow and natural selection can have many outcomes. In some cases, strong selection can over- whelm any effects of gene flow, but in other situations, gene flow can prevent populations from eliminating less successful alleles from a population. As a general explana- tion, then, natural selection is not likely to have any fewer exceptions than the biological species concept, al- though it may prove more successful for certain types of organisms or habitats. A variety of other ideas have been put forward to estab- lish criteria for defining species. Many of these are spe- cific to a particular type of organism and none has univer- sal applicability. In truth, it may be that there is no single explanation for what maintains the identity of species. Given the incredible variation evident in plants, animals, and microorganisms in all aspects of their biology, it is perhaps not surprising that different processes are operat- ing in different organisms. This is an area of active re- search that demonstrates the dynamic nature of the field of evolutionary biology. Hybridization has always been recognized to be widespread among plants, but recent research reveals that it is surprisingly high in animals, too. Because of the diversity of living organisms, no single definition of what constitutes a species may be universally applicable. Chapter 22 The Origin of Species 475 476 Part VI Evolution Chapter 22 Summary Questions Media Resources 22.1 Species are the basic units of evolution. ? Species are groups of organisms that differ from one another in one or more characteristics and do not hybridize freely when they come into contact in their natural environment. Many species cannot hybridize with one another at all. ? Species exhibit geographic variation, yet phenotypically distinctive populations are connected by intermediate forms. 1. Define the term sympatry. Why is sympatric speciation thought by many to be unlikely? 2. What is the biological species concept? ? Among the factors that separate populations and species are geographical, ecological, temporal, behavioral, and mechanical isolation, as well as factors that inhibit the fusion of gametes or the normal development of the hybrid organisms. ? Some isolating mechanisms (prezygotic) prevent hybrid formation; others (postzygotic) prevent hybrids from surviving and reproducing. 3. What is the difference between prezygotic and postzygotic isolating mechanisms? 4. What barriers exist to hybrid formation and success? Which are prezygotic and which are postzygotic isolating mechanisms? Why do some people think the term “isolating mechanism” is misleading? 22.2 Species maintain their genetic distinctiveness through barriers to reproduction. ? Reproductive isolation can arise as populations differentiate by adaptation to different environments, as well as by random genetic drift, founder effects, or population bottlenecks. ? Natural selection may favor changes in the mating system when a species occupies a new habitat, so that the species becomes reproductively isolated from other species. ? When two species are not completely reproductively isolated, natural selection may favor the evolution of more effective isolating mechanisms to prevent hybridization, a process termed “reinforcement.” 5. How does selection relate to population divergence? 6. How many genes are involved in the speciation process? 7. When are hybrids at a disadvantage? What can be the result of this disadvantage? 8. Define the term polyploidy. 22.3 We have learned a great deal about how species form. ? Clusters of species arise when populations differentiate to fill several niches. On islands, differentiation is often rapid because of numerous open habitats. ? The pace of evolution is not constant among all organisms. Some scientists believe it occurs in spurts, others argue that it proceeds gradually. ? Hybridization occurs commonly among plants and even among animals. The biological species concept may not apply to all organisms. 9. What is adaptive radiation? What types of habitats encourage it? Why? 10. What is the difference between gradualism and punctuated equilibrium? 11. Why is the biological species concept no longer considered to be universally applicable? 22.4 Clusters of species reflect rapid evolution. www.mhhe.com/raven6e www.biocourse.com ? Activity: Allopatric Speciation ? Introduction to Speciation ? Sympatric Speciation ? Allopatric Speciation ? Constructing Phylogenies ? Student Research: Evolution in Ferns ? Evolutionary Trends Book Reviews ? Darwin’s Dreampond by Goldschmidt ? The Beak of the Finch by Weiner 477 23 How Humans Evolved Concept Outline 23.1 The evolutionary path to humans starts with the advent of primates. The Evolutionary Path to Apes. Primates first evolved 65 million years ago, giving rise first to prosimians and then to monkeys. How the Apes Evolved. Apes, including our closest relatives, the chimpanzees, arose from an ancestor common to Old World monkeys. 23.2 The first hominids to evolve were australopithecines. An Evolutionary Tree with Many Branches. The first hominids were australopithecines, of which there were several different kinds. The Beginning of Hominid Evolution. The ability to walk upright on two legs marks the beginning of hominid evolution. One can draw the hominid family tree in two very different ways, either lumping variants together or splitting them into separate species. 23.3 The genus Homo evolved in Africa. African Origin: Early Homo. There may have been several species of early Homo,with brains significantly larger than those of australopithecines. Out of Africa: Homo erectus. The first hominid species to leave Africa was the relatively large-brained H. erectus, the longest lived species of Homo. 23.4 Modern humans evolved quite recently. The Last Stage of Hominid Evolution. Modern humans evolved within the last 600,000 years, our own species within the last 200,000 years. Our Own Species: Homo sapiens. Our species appears to have evolved in Africa, and then migrated to Europe and Asia. Human Races. Our species is unique in evolving culturally. Differences in populations in skin color reflect adaptation to different environments, rather than genetic differentiation among populations. I n 1871 Charles Darwin published another ground- breaking book, The Descent of Man. In this book, he sug- gested that humans evolved from the same African ape an- cestors that gave rise to the gorilla and the chimpanzee. Although little fossil evidence existed at that time to sup- port Darwin’s case, numerous fossil discoveries made since then strongly support his hypothesis (figure 23.1). Human evolution is the part of the evolution story that often inter- ests people most, and it is also the part about which we know the most. In this chapter we follow the evolutionary journey that has led to humans, telling the story chronolog- ically. It is an exciting story, replete with controversy. FIGURE 23.1 The trail of our ancestors. These fossil footprints, made in Africa 3.7 million years ago, look as if they might have been left by a mother and child walking on the beach. But these tracks, preserved in volcanic ash, are not human. They record the passage of two individuals of the genus Australopithecus, the group from which our genus, Homo, evolved. Origin of the Anthropoids The anthropoids, or higher primates, include monkeys, apes, and humans (figure 23.3). Anthropoids are almost all diurnal—that is, active during the day—feeding mainly on fruits and leaves. Evolution favored many changes in eye design, including color vision, that were adaptations to day- time foraging. An expanded brain governs the improved senses, with the braincase forming a larger portion of the head. Anthropoids, like the relatively few diurnal prosimi- ans, live in groups with complex social interactions. In ad- dition, the anthropoids tend to care for their young for prolonged periods, allowing for a long childhood of learn- ing and brain development. The early anthropoids, now extinct, are thought to have evolved in Africa. Their direct descendants are a very suc- cessful group of primates, the monkeys. New World Monkeys. About 30 million years ago, some anthropoids migrated to South America, where they evolved in isolation. Their descendants, known as the New World monkeys, are easy to identify: all are arboreal, they have flat spreading noses, and many of them grasp objects with long prehensile tails (figure 23.4a). 478 Part VI Evolution The Evolutionary Path to Apes The story of human evolution begins around 65 million years ago, with the explosive radiation of a group of small, arboreal mammals called the Archonta. These primarily in- sectivorous mammals had large eyes and were most likely nocturnal (active at night). Their radiation gave rise to dif- ferent types of mammals, including bats, tree shrews, and primates, the order of mammals that contains humans. The Earliest Primates Primates are mammals with two distinct features that al- lowed them to succeed in the arboreal, insect-eating envi- ronment: 1. Grasping fingers and toes. Unlike the clawed feet of tree shrews and squirrels, primates have grasping hands and feet that let them grip limbs, hang from branches, seize food, and, in some primates, use tools. The first digit in many primates is opposable and at least some, if not all, of the digits have nails. 2. Binocular vision. Unlike the eyes of shrews and squirrels, which sit on each side of the head so that the two fields of vision do not overlap, the eyes of pri- mates are shifted forward to the front of the face. This produces overlapping binocular vision that lets the brain judge distance precisely—important to an animal moving through the trees. Other mammals have binocular vision, but only pri- mates have both binocular vision and grasping hands, mak- ing them particularly well adapted to their environment. While early primates were mostly insectivorous, their den- tition began to change from the shearing, triangular- shaped molars specialized for insect eating to the more flattened, square-shaped molars and rodentlike incisors specialized for plant eating. Primates that evolved later also show a continuous reduction in snout length and number of teeth. The Evolution of Prosimians About 40 million years ago, the earliest primates split into two groups: the prosimians and the anthropoids. The prosimians (“before monkeys”) looked something like a cross between a squirrel and a cat and were common in North America, Europe, Asia, and Africa. Only a few prosimians survive today, lemurs, lorises and tarsiers (figure 23.2). In addition to having grasping digits and binocular vision, prosimians have large eyes with increased visual acu- ity. Most prosimians are nocturnal, feeding on fruits, leaves, and flowers, and many lemurs have long tails for balancing. 23.1 The evolutionary path to humans starts with the advent of primates. FIGURE 23.2 A prosimian. This tarsier, a prosimian native to tropical Asia, shows the characteristic features of primates: grasping fingers and toes and binocular vision. Old World Monkeys. Around 25 million years ago, anthropoids that remained in Africa split into two lin- eages: one gave rise to the Old World monkeys and one gave rise to the hominoids (see page 480). Old World monkeys include ground- dwelling as well as arboreal species. None of the Old World monkeys have prehensile tails. Their nostrils are close together, their noses point downward, and some have toughened pads of skin for prolonged sitting (figure 23.4b). The earliest primates arose from small, tree-dwelling, insect-eaters and gave rise to prosimians and then anthropoids. Early anthropoids gave rise to New World monkeys and Old World monkeys. Chapter 23 How Humans Evolved 479 0 10 20 30 40 Mi l l ions of years a go Homi n i ds Chi m p a n z e e s G o r i l l a s O r a n g u t a n s G i b b o n s O l d W o r l d M o n k e y s N e w W o r l d M o n k e y s Ta r s i e r s L e mu rs a n d lor i s es Prosimians Anthropoids Hominoids FIGURE 23.3 A primate evolutionary tree. The most ancient of the primates are the prosimians, while the hominids were the most recent to evolve. FIGURE 23.4 New and Old World monkeys. (a) New World monkeys, such as this golden lion tamarin, are arboreal, and many have prehensile tails. (b) Old World monkeys lack prehensile tails, and many are ground dwellers. (a) (b) How the Apes Evolved The other African anthropoid lineage is the hominoids, which includes the apes and the hominids (humans and their direct ancestors). The living apes consist of the gib- bon (genus Hylobates), orangutan (Pongo), gorilla (Gorilla), and chimpanzee (Pan) (figure 23.5). Apes have larger brains than monkeys, and they lack tails. With the excep- tion of the gibbon, which is small, all living apes are larger than any monkey. Apes exhibit the most adaptable behav- ior of any mammal except human beings. Once wide- spread in Africa and Asia, apes are rare today, living in relatively small areas. No apes ever occurred in North or South America. The First Hominoid Considerable controversy exists about the identity of the first hominoid. During the 1980s it was commonly believed that the common ancestor of apes and hominids was a late Miocene ape living 5 to 10 million years ago. In 1932, a candidate fossil, an 8-million-year-old jaw with teeth, was unearthed in India. It was called Ramapithecus (after the Hindi deity Rama). However, these fossils have never been found in Africa, and more complete fossils discovered in 1981 made it clear that Ramapithecus is in fact closely re- lated to the orangutan. Attention has now shifted to an earlier Miocene ape, Proconsul, which has many of the char- acteristics of Old World monkeys but lacks a tail and has apelike hands, feet, and pelvis. However, because very few fossils have been recovered from the period 5 to 10 million years ago, it is not yet possible to identify with certainty the first hominoid ancestor. 480 Part VI Evolution (a) (b) (c) (d) FIGURE 23.5 The living apes. (a) Mueller gibbon, Hylobates muelleri. (b) Orangutan, Pongo pygmaeus. (c) Gorilla, Gorilla gorilla. (d) Chimpanzee, Pan troglodytes. Which Ape Is Our Closest Relative? Studies of ape DNA have explained a great deal about how the living apes evolved. The Asian apes evolved first. The line of apes leading to gibbons diverged from other apes about 15 million years ago, while orangutans split off about 10 million years ago (see figure 23.3). Neither are closely related to humans. The African apes evolved more recently, between 6 and 10 million years ago. These apes are the closest liv- ing relatives to humans; some taxonomists have even ad- vocated placing humans and the African apes in the same zoological family, the Hominidae. Fossils of the earliest hominids, described later in the chapter, suggest that the common ancestor of the hominids was more like a chim- panzee than a gorilla. Based on genetic differences, sci- entists estimate that gorillas diverged from the line lead- ing to chimpanzees and humans some 8 million years ago. Sometime after the gorilla lineage diverged, the com- mon ancestor of all hominids split off from chimpanzee line to begin the evolutionary journey leading to humans. Because this split was so recent, the genes of humans and chimpanzees have not had time to evolve many genetic dif- ferences. For example, a human hemoglobin molecule dif- fers from its chimpanzee counterpart in only a single amino acid. In general, humans and chimpanzees exhibit a level of genetic similarity normally found between closely related sibling species of the same genus! Comparing Apes to Hominids The common ancestor of apes and hominids is thought to have been an arboreal climber. Much of the subsequent evolution of the hominoids reflected different approaches to locomotion. Hominids became bipedal, walking up- right, while the apes evolved knuckle-walking, supporting their weight on the back sides of their fingers (monkeys, by contrast, use the palms of their hands). Humans depart from apes in several areas of anatomy re- lated to bipedal locomotion (figure 23.6). Because humans walk on two legs, their vertebral column is more curved than an ape’s, and the human spinal cord exits from the bottom rather than the back of the skull. The human pelvis has be- come broader and more bowl-shaped, with the bones curving forward to center the weight of the body over the legs. The hip, knee, and foot (in which the human big toe no longer splays sideways) have all changed proportions. Being bipedal, humans carry much of the body’s weight on the lower limbs, which comprise 32 to 38% of the body’s weight and are longer than the upper limbs; human upper limbs do not bear the body’s weight and make up only 7 to 9% of human body weight. African apes walk on all fours, with the upper and lower limbs both bearing the body’s weight; in gorillas, the longer upper limbs account for 14 to 16% of body weight, the somewhat shorter lower limbs for about 18%. Hominoids, the apes and hominids, arose from Old World monkeys. Among living apes, chimpanzees seem the most closely related to humans. Chapter 23 How Humans Evolved 481 Skull attaches posteriorly Spine slightly curved Long, narrow pelvis Arms longer than legs and also used for walking Femur angled out Skull attaches inferiorly Chimpanzee Australopithecine Spine S-shaped Bowl-shaped pelvis Arms shorter than legs and not used for walking Femur angled in FIGURE 23.6 A comparison of ape and hominid skeletons. Early humans, such as australopithecines, were able to walk upright because their arms were shorter, their spinal cord exited from the bottom of the skull, their pelvis was bowl-shaped and centered the body weight over the legs, and their femurs angled inward, directly below the body, to carry its weight. An Evolutionary Tree with Many Branches Five to 10 million years ago, the world’s climate began to get cooler, and the great forests of Africa were largely re- placed with savannas and open woodland. In response to these changes, a new kind of hominoid was evolving, one that was bipedal. These new hominoids are classified as hominids—that is, of the human line. There are two major groups of hominids: three to seven species of the genus Homo (depending how you count them) and seven species of the older, smaller-brained genus Australopithecus. In every case where the fossils allow a de- termination to be made, the hominids are bipedal, walking upright. Bipedal locomotion is the hallmark of hominid evolution. We will first discuss Australopithecus, and then Homo. Discovery of Australopithecus The first hominid was discovered in 1924 by Raymond Dart, an anatomy professor at Johannesburg in South Africa. One day, a mine worker brought him an unusual chunk of rock—actually, a rock-hard mixture of sand and soil. Picking away at it, Professor Dart uncovered a skull unlike that of any ape he had ever seen. Beautifully pre- served, the skull was of a five-year-old individual, still with its milk teeth. While the skull had many apelike fea- tures such as a projecting face and a small brain, it had distinctly human features as well—for example, a rounded jaw unlike the pointed jaw of apes. The ventral position of the foramen magnum (the hole at the base of the skull from which the spinal cord emerges) suggested that the creature had walked upright. Dart concluded it was a human ancestor. What riveted Dart’s attention was that the rock in which the skull was embedded had been collected near other fos- sils that suggested that the rocks and their fossils were sev- eral million years old! At that time, the oldest reported fos- sils of hominids were less than 500,000 years old, so the antiquity of this skull was unexpected and exciting. Scien- tists now estimate Dart’s skull to be 2.8 million years old. Dart called his find Australopithecus africanus (from the Latin australo, meaning “southern” and the Greek pithecus, meaning “ape”), the ape from the south of Africa. Today, fossils are dated by the relatively new process of single-crystal laser-fusion dating. A laser beam melts a sin- gle potassium feldspar crystal, releasing argon gas, which is measured in a gas mass spectrometer. Because the argon in the crystal has accumulated at a known rate, the amount re- leased reveals the age of the rock and thus of nearby fossils. The margin of error is less than 1%. 482 Part VI Evolution 23.2 The first hominids to evolve were australopithecines. A. afarensis A. africanus FIGURE 23.7 Nearly human. These four skulls, all photographed from the same angle, are among the best specimens available of the key Australopithecus species. Other Kinds of Australopithecus In 1938, a second, stockier kind of Australopithecus was un- earthed in South Africa. Called A. robustus, it had massive teeth and jaws. In 1959, in East Africa, Mary Leakey dis- covered a third kind of Australopithecus—A. boisei (after Charles Boise, an American-born businessman who con- tributed to the Leakeys’ projects)—who was even more stockily built. Like the other australopithecines, A. boisei was very old—almost 2 million years. Nicknamed “Nut- cracker man,” A. boisei had a great bony ridge—a Mohawk haircut of bone—on the crest of the head to anchor its im- mense jaw muscles (figure 23.7). In 1974, anthropologist Don Johanson went to the re- mote Afar Desert of Ethiopia in search of early human fossils and hit the jackpot. He found the most complete, best preserved australopithecine skeleton known. Nick- named “Lucy,” the skeleton was 40% complete and over 3 million years old. The skeleton and other similar fossils have been assigned the scientific name Australopithecus afarensis (from the Afar Desert). The shape of the pelvis indicated that Lucy was a female, and her leg bones proved she walked upright. Her teeth were distinctly ho- minid, but her head was shaped like an ape’s, and her brain was no larger than that of a chimpanzee, about 400 cubic centimeters, about the size of a large orange. More than 300 specimens of A. afarensis have since been discovered. In the last 10 years, three additional kinds of australo- pithecines have been reported. These seven species pro- vide ample evidence that australopithecines were a di- verse group, and additional species will undoubtedly be described by future investigators. The evolution of ho- minids seems to have begun with an initial radiation of numerous species. Early Australopithecines Were Bipedal We now know australopithecines from hundreds of fossils. The structure of these fossils clearly indicates that australo- pithecines walked upright. These early hominids weighed about 18 kilograms and were about 1 meter tall. Their den- tition was distinctly hominid, but their brains were not any larger than those of apes, generally 500 cc or less. Homo brains, by comparison, are usually larger than 600 cc; mod- ern H. sapiens brains average 1350 cc. Australopithecine fossils have been found only in Africa. Although all the fos- sils to date come from sites in South and East Africa (ex- cept for one specimen from Chad), it is probable that they lived over a much broader area of Africa. Only in South and East Africa, however, are sediments of the proper age exposed to fossil hunters. The australopithecines were hominids that walked upright and lived in Africa over 3 million years ago. Chapter 23 How Humans Evolved 483 A. robustus A. boisei FIGURE 23.7 (continued). The Beginning of Hominid Evolution The Origins of Bipedalism For much of this century, biologists have debated the se- quence of events that led to the evolution of hominids. A key element may have been bipedalism. Bipedalism seems to have evolved as our ancestors left dense forests for grass- lands and open woodland (figure 23.8). One school of thought proposes that hominid brains enlarged first, and then hominids became bipedal. Another school sees bipedalism as a precursor to bigger brains. Those who favor the brain-first hypothesis speculate that human intel- ligence was necessary to make the decision to walk upright and move out of the forests and onto the grassland. Those who favor the bipedalism-first hypothesis argue that bipedalism freed the forelimbs to manufacture and use tools, favoring the subsequent evolution of bigger brains. A treasure trove of fossils unearthed in Africa has settled the debate. These fossils demonstrate that bipedalism ex- tended back 4 million years ago; knee joints, pelvis, and leg bones all exhibit the hallmarks of an upright stance. Sub- stantial brain expansion, on the other hand, did not appear until roughly 2 million years ago. In hominid evolution, upright walking clearly preceded large brains. Remarkable evidence that early hominids were bipedal is a set of some 69 hominid footprints found at Laetoli, East Africa. Two individuals, one larger than the other, walked upright side-by-side for 27 meters, their footprints pre- served in 3.7-million-year-old volcanic ash (see figure 23.1). Importantly, the big toe is not splayed out to the side as in a monkey or ape—the footprints were clearly made by a hominid. The evolution of bipedalism marks the beginning of the hominids. The reason why bipedalism evolved in hominids remains a matter of controversy. No tools appeared until 2.5 million years ago, so toolmaking seems an unlikely cause. Alternative ideas suggest that walking upright is faster and uses less energy than walking on four legs; that an upright posture permits hominids to pick fruit from trees and see over tall grass; that being upright reduces the body surface exposed to the sun’s rays; that an upright stance aided the wading of aquatic hominids, and that bipedalism frees the forelimbs of males to carry food back to females, encouraging pair-bonding. All of these sugges- tions have their proponents, and none are universally ac- cepted. The origin of bipedalism, the key event in the evo- lution of hominids, remains a mystery. The Root of the Hominid Tree The Oldest Known Hominid. In 1994, a remarkable, nearly complete fossil skeleton was unearthed in Ethiopia. The skeleton is still being painstakingly assembled, but it seems almost certainly to have been bipedal; the foramen magnum, for example, is situated far forward, as in other bipedal hominids. Some 4.4 million years old, it is the most ancient hominid yet discovered. It is significantly more apelike than any australopithecine and so has been assigned to a new genus, Ardipithecus from the local Afar language ardi for “ground” and the Greek pithecus for “ape” (figure 23.9a). The First Australopithecine. In 1995, hominid fossils of nearly the same age, 4.2 million years old, were found in the Rift Valley in Kenya. The fossils are fragmentary, but they include complete upper and lower jaws, a piece of the 484 Part VI Evolution FIGURE 23.8 A reconstruction of an early hominid walking upright. These articulated plaster skeletons, made by Owen Lovejoy and his students at Kent State University, depict an early hominid (Australopithecus afarensis) walking upright. skull, arm bones, and a partial leg bone. The fossils were assigned to the species Australopithecus anamensis (fig- ure 23.9b); anam is the Turkana word for lake. They were categorized in the genus Australopithecus rather than Ardipithecus because the fossils have bipedal characteristics and are much less apelike than A. ramidus. Although clearly australopithecine, the fossils are intermediate in many ways between apes and A. afarensis. Numerous frag- mentary specimens of A. anamensis have since been found. Most re- searchers agree that these slightly built A. anamensis individuals represent the true base of our family tree, the first members of the genus Australopithecus, and thus ancestor to A. afarensis and all other australopithecines. Differing Views of the Hominid Family Tree Investigators take two different philo- sophical approaches to characterizing the diverse group of African hominid fossils. One group focuses on common elements in different fossils, and tends to lump together fossils that share key characters. Differences between the fossils are attributed to diversity within the group. Other investigators focus more pointedly on the differences between hominid fos- sils. They are more inclined to assign fossils that exhibit differences to different species. The hominid phyloge- netic tree in figure 23.10 presents such a view. Where the “lumpers” tree presents three species of Homo, for ex- ample, the “splitters” tree presents no fewer than seven! At this point, it is not possible to decide which view is correct; more fossils are needed to determine how much of the differences between fossils represents within- species variation and how much characterizes between- species differences. The evolution of bipedalism—walking upright—marks the beginning of hominid evolution, although no one is quite sure why bipedalism evolved. The root of the hominid evolutionary tree is only imperfectly known. The earliest australopithecine yet described is A. anamensis, over 4 million years old. Chapter 23 How Humans Evolved 485 FIGURE 23.9 Hominid fossils. (a) Our earliest known ancestor. A tooth from Ardipithecus ramidus, discovered in 1994. The name ramidusis from the Latin word for “root,” as this is thought to be the root of the hominid family tree. The earliest known hominid, at 4.4 million years old, A. ramidus was about the size of a chimpanzee and apparently could walk upright. (b) The earliest australopithecine. This fossil jaw of Australopithecus is about 4.2 million years old, making A. anamensis the oldest known australopithecine. Classified by some scientists as the single species Homo sapiens Classified by some scientists as the single species Homo habilis Millions of years ago H. sapiens H. neanderthalensis H. heidelbergensis H. habilis H. erectus H. ergaster A. afarensis H. rudolfensis A. africanus Australopithecus anamensis Ardipithecus ramidus A. aethiopicus A. robustus A. boisei 4.5 4 3.5 3 2.5 2 1.5 1 0.5 0 FIGURE 23.10 A hominid evolutionary tree. In this tree, the most widely accepted, the vertical bars show the known dates of first and last appearances of proposed species; bars are broken where dates are uncertain. Six species of Australopithecusand seven of Homoare included. (a) (b) African Origin: Early Homo The first humans evolved from australopithecine ancestors about 2 million years ago. The exact ancestor has not been clearly defined, but is commonly thought to be A. afarensis. Only within the last 30 years have a significant number of fossils of early Homo been uncovered. An explosion of in- terest has fueled intensive field exploration in the last few years, and new finds are announced regularly; every year, our picture of the base of the human evolutionary tree grows clearer. The account given here will undoubtedly be outdated by future discoveries, but it provides a good ex- ample of science at work. Homo habilis In the early 1960s, stone tools were found scattered among hominid bones close to the site where A. boisei had been unearthed. Although the fossils were badly crushed, painstaking reconstruction of the many pieces suggested a skull with a brain volume of about 680 cubic centimeters, larger than the australopithecine range of 400 to 550 cubic centimeters. Because of its association with tools, this early human was called Homo habilis, meaning “handy man.” Par- tial skeletons discovered in 1986 indicate that H. habilis was small in stature, with arms longer than legs and a skeleton much like Australopithecus. Because of its general similarity to australopithecines, many researchers at first questioned whether this fossil was human. Homo rudolfensis In 1972, Richard Leakey, working east of Lake Rudolf in northern Kenya, discovered a virtually complete skull about the same age as H. habilis. The skull, 1.9 million years old, had a brain volume of 750 cubic centimeters and many of the characteristics of human skulls—it was clearly human and not australopithecine. Some anthropologists assign this skull to H. habilis, arguing it is a large male. Other an- thropologists assign it to a separate species, H. rudolfensis, because of its substantial brain expansion. Homo ergaster Some of the early Homo fossils being discovered do not eas- ily fit into either of these species (figure 23.11). They tend to have even larger brains than H. rudolfensis, with skeletons less like an australopithecine and more like a modern human in both size and proportion. Interestingly, they also have small cheek teeth, as modern humans do. Some an- thropologists have placed these specimens in a third species of early Homo, H. ergaster (ergaster is from the Greek for “workman”). How Diverse Was Early Homo? Because so few fossils have been found of early Homo, there is lively debate about whether they should all be lumped into H. habilis or split into the three species H. rudolfensis, H. habilis, and H. ergaster. If the three species designations are accepted, as increasing numbers of researchers are doing, then it would appear that Homo underwent an adap- tive radiation (as described in chapter 22) with H. rudolfensis the most ancient species, followed by H. habilis and then H. ergaster. Because of its modern skeleton, H. ergaster is thought the most likely ancestor to later species of Homo (see figure 23.10). Early species of Homo, the oldest members of our genus, had a distinctly larger brain than australopithecines and most likely used tools. There may have been several different species. 486 Part VI Evolution 23.3 The genus Homo evolved in Africa. FIGURE 23.11 Early Homo. This skull of a boy, who apparently died in early adolescence, is 1.6 million years old and has been assigned to the species Homo ergaster(a form of Homo habilisrecognized by some as a separate species). Much larger than earlier hominids, he was about 1.5 meters in height and weighed approximately 47 kilograms. Out of Africa: Homo erectus Our picture of what early Homo was like lacks detail, be- cause it is based on only a few specimens. We have much more information about the species that replaced it, Homo erectus. Java Man After the publication of Darwin’s book On the Origin of Species in 1859, there was much public discussion about “the missing link,” the fossil ancestor common to both hu- mans and apes. Puzzling over the question, a Dutch doctor and anatomist named Eugene Dubois decided to seek fossil evidence of the missing link in the home country of the orangutan, Java. Dubois set up practice in a river village in eastern Java. Digging into a hill that villagers claimed had “dragon bones,” he unearthed a skull cap and a thighbone in 1891. He was very excited by his find, informally called Java man, for three reasons: 1. The structure of the thigh bone clearly indicated that the individual had long, straight legs and was an ex- cellent walker. 2. The size of the skull cap suggested a very large brain, about 1000 cubic centimeters. 3. Most surprisingly, the bones seemed as much as 500,000 years old, judged by other fossils Dubois un- earthed with them. The fossil hominid that Dubois had found was far older than any discovered up to that time, and few scientists were willing to accept that it was an ancient species of human. Peking Man Another generation passed before scientists were forced to admit that Dubois had been right all along. In the 1920s a skull was discovered near Peking (now Beijing), China, that closely resembled Java man. Continued excavation at the site eventually revealed 14 skulls, many excellently pre- served. Crude tools were also found, and most important of all, the ashes of campfires. Casts of these fossils were dis- tributed for study to laboratories around the world. The originals were loaded onto a truck and evacuated from Peking at the beginning of World War II, only to disap- pear into the confusion of history. No one knows what happened to the truck or its priceless cargo. Fortunately, Chinese scientists have excavated numerous additional skulls of Peking man since 1949. A Very Successful Species Java man and Peking man are now recognized as belonging to the same species, Homo erectus. Homo erectus was a lot larger than Homo habilis—about 1.5 meters tall. It had a large brain, about 1000 cubic centimeters (figure 23.12), and walked erect. Its skull had prominent brow ridges and, like modern humans, a rounded jaw. Most interesting of all, the shape of the skull interior suggests that H. erectus was able to talk. Where did H. erectus come from? It should come as no surprise to you that it came out of Africa. In 1976 a com- plete H. erectus skull was discovered in East Africa. It was 1.5 million years old, a million years older than the Java and Peking finds. Far more successful than H. habilis, H. erectus quickly became widespread and abundant in Africa, and within 1 million years had migrated into Asia and Europe. A social species, H. erectus lived in tribes of 20 to 50 people, often dwelling in caves. They success- fully hunted large animals, butchered them using flint and bone tools, and cooked them over fires—the site in China contains the remains of horses, bears, elephants, deer, and rhinoceroses. Homo erectus survived for over a million years, longer than any other species of human. These very adaptable humans only disappeared in Africa about 500,000 years ago, as modern humans were emerging. Interestingly, they survived even longer in Asia, until about 250,000 years ago. Homo erectus evolved in Africa, and migrated from there to Europe and Asia. Chapter 23 How Humans Evolved 487 Hominid cranial capacity (cc) 4.0 3.5 3.0 2.5 Millions of years ago 2.0 1.5 1.0 0.5 0 1500 1000 500 A. afarensis A. africanus H. rudolfensis H. ergaster A. boisei A. robustus H. habilis H. erectus H. heidelbergensis H. neanderthalensis H. sapiens FIGURE 23.12 Brain size increased as hominids evolved. Homo erectus had a larger brain than early Homo, which in turn had larger brains than those of the australopithecines with which they shared East African grasslands. Maximum brain size (and apparently body size) was attained by H. neanderthalensis. Both brain and body size appear to have declined some 10% in recent millennia. The Last Stage of Hominid Evolution The evolutionary journey to modern humans entered its final phase when modern humans first appeared in Africa about 600,000 years ago. Investigators who focus on human diversity consider there to have been three species of mod- ern humans: Homo heidelbergensis, H. neanderthalensis, and H. sapiens (see figure 23.10). Other investigators lump the three species into one, H. sapiens (“wise man”). The oldest modern human, Homo heidelbergensis, is known from a 600,000-year-old fossil from Ethiopia. Although it coex- isted with H. erectus in Africa, H. heidelbergensis has more advanced anatomical features, such as a bony keel running along the midline of the skull, a thick ridge over the eye sockets, and a large brain. Also, its forehead and nasal bones are very like those of H. sapiens. As H. erectus was becoming rarer, about 130,000 years ago, a new species of human arrived in Europe from Africa. Homo neanderthalensis likely branched off from the ancestral line leading to modern humans as long as 500,000 years ago. Compared with modern humans, Neanderthals were short, stocky, and powerfully built. Their skulls were mas- sive, with protruding faces, heavy, bony ridges over the brows (figure 23.13), and larger brain-cases. Out of Africa—Again? The oldest fossil known of Homo sapiens, our own species, is from Ethiopia and is about 130,000 years old. Other fossils from Israel appear to be between 100,000 and 120,000 years old. Outside of Africa and the Middle East, there are no clearly dated H. sapiens fossils older than roughly 40,000 years of age. The implication is that H. sapiens evolved in Africa, then migrated to Europe and Asia, the Out-of-Africa model. An opposing view, the Multiregional model, argues that the human races inde- pendently evolved from H. erectus in different parts of the world. Recently, scientists studying human mitochondrial DNA have added fuel to the fire of this controversy. Be- cause DNA accumulates mutations over time, the oldest populations should show the greatest genetic diversity. It turns out that the greatest number of different mitochon- drial DNA sequences occur among modern Africans. This result is consistent with the hypothesis that humans have been living in Africa longer than on any other conti- nent, and from there spread to all parts of the world, re- tracing the path taken by H. erectus half a million years before (figure 23.14). 488 Part VI Evolution 23.4 Modern humans evolved quite recently. H. erectus H. habilis FIGURE 23.13 Our own genus. These four skulls illustrate the changes that have occurred during the evolution of the genus Homo. The Homo sapiensis essentially the same as human skulls today. The skulls were photographed from the same angle. A clearer analysis is possible using chro- mosomal DNA, segments of which are far more variable than mitochondrial DNA, providing more “markers” to compare. When a variable segment of DNA from human chromosome 12 was analyzed in 1996, a clear picture emerged. A total of 24 different versions of this segment were found. Fully 21 of them were present in human populations in Africa, while three were found in Europeans and only two in Asians and in Americans. This result argues strongly that chromosome 12 has existed in Africa far longer than among non-African humans, strongly supporting an African ori- gin of H. sapiens. Recently discovered fossils of early H. sapiens from Africa also lend strong support to this hypothesis. Homo sapiens, our species, seems to have evolved in Africa and then, like H. erectus before it, migrated to Europe and Asia. Chapter 23 How Humans Evolved 489 av“J a man” “Peking man” Neanderthal man FIGURE 23.14 Out of Africa—many times. A still-controversial theory suggests that Homo spread from Africa to Europe and Asia repeatedly. First, Homo erectus (white arrow) spread as far as Java and China. Later, H. erectus was followed and replaced by Homo neanderthalensis, a pattern repeated again still later by Homo sapiens (red arrow). H. neanderthalensis H. sapiens (Cro-Magnon) FIGURE 23.13 (continued) Our Own Species: Homo sapiens H. sapiens is the only surviving species of the genus Homo, and indeed is the only surviving hominid. Some of the best fossils of Homo sapiens are 20 well-preserved skele- tons with skulls found in a cave near Nazareth in Israel. Modern dating techniques date these humans to between 90,000 and 100,000 years old. The skulls are modern in appearance, with high, short braincases, vertical fore- heads with only slight brow ridges, and a cranial capacity of roughly 1550 cc, well within the range of modern humans. Cro-Magnons Replace the Neanderthals The Neanderthals (classified by many paleontologists as a separate species Homo neanderthalensis) were named after the Neander Valley of Germany where their fossils were first discovered in 1856. Rare at first outside of Africa, they became progressively more abundant in Europe and Asia, and by 70,000 years ago had become common. The Nean- derthals made diverse tools, including scrapers, spearheads, and handaxes. They lived in huts or caves. Neanderthals took care of their injured and sick and commonly buried their dead, often placing food, weapons, and even flowers with the bodies. Such attention to the dead strongly sug- gests that they believed in a life after death. This is the first evidence of the symbolic thinking characteristic of modern humans. Fossils of H. neanderthalensis abruptly disappear from the fossil record about 34,000 years ago and are replaced by fossils of H. sapiens called the Cro-Magnons (named after the valley in France where their fossils were first discov- ered). We can only speculate why this sudden replacement occurred, but it was complete all over Europe in a short pe- riod. There is some evidence that the Cro-Magnons came from Africa—fossils of essentially modern aspect but as much as 100,000 years old have been found there. Cro- Magnons seem to have replaced the Neanderthals com- pletely in the Middle East by 40,000 years ago, and then spread across Europe, coexisting and possibly even inter- breeding with the Neanderthals for several thousand years. The Cro-Magnons had a complex social organization and are thought to have had full language capabilities. They lived by hunting. The world was cooler than it is now—the time of the last great ice age—and Europe was covered with grasslands inhabited by large herds of grazing animals. Pictures of them can be seen in elaborate and often beauti- ful cave paintings made by Cro-Magnons throughout Eu- rope (figure 23.15). Humans of modern appearance eventually spread across Siberia to North America, which they reached at least 13,000 years ago, after the ice had begun to retreat and a land bridge still connected Siberia and Alaska. By 10,000 years ago, about 5 million people inhabited the entire world (compared with more than 6 billion today). Homo sapiens Are Unique We humans are animals and the product of evolution. Our evolution has been marked by a progressive increase in brain size, distinguishing us from other animals in several ways. First, humans are able to make and use tools effectively—a capability that, more than any other factor, has been respon- sible for our dominant position in the animal kingdom. Sec- ond, although not the only animal capable of conceptual thought, we have refined and extended this ability until it has become the hallmark of our species. Lastly, we use symbolic language and can with words shape concepts out of experi- ence. Our language capability has allowed the accumulation of experience, which can be transmitted from one generation to another. Thus, we have what no other animal has ever had: extensive cultural evolution. Through culture, we have found ways to change and mold our environment, rather than changing evolutionarily in response to the demands of the environment. We control our biological future in a way never before possible—an exciting potential and frightening responsibility. Our species, Homo sapiens, is good at conceptual thought and tool use, and is the only animal that uses symbolic language. 490 Part VI Evolution FIGURE 23.15 Cro-Magnon art. Rhinoceroses are among the animals depicted in this remarkable cave painting found in 1995 near Vallon-Pont d’Arc, France. Human Races Human beings, like all other species, have differentiated in their characteristics as they have spread throughout the world. Local populations in one area often appear signifi- cantly different from those that live elsewhere. For exam- ple, northern Europeans often have blond hair, fair skin, and blue eyes, whereas Africans often have black hair, dark skin, and brown eyes. These traits may play a role in adapt- ing the particular populations to their environments. Blood groups may be associated with immunity to diseases more common in certain geographical areas, and dark skin shields the body from the damaging effects of ultraviolet radiation, which is much stronger in the tropics than in temperate regions. All human beings are capable of mating with one an- other and producing fertile offspring. The reasons that they do or do not choose to associate with one another are purely psychological and behavioral (cultural). The number of groups into which the human species might logically be divided has long been a point of contention. Some contem- porary anthropologists divide people into as many as 30 “races,” others as few as three: Caucasoid, Negroid, and Oriental. American Indians, Bushmen, and Aborigines are examples of particularly distinctive subunits that are some- times regarded as distinct groups. The problem with classifying people or other organisms into races in this fashion is that the characteristics used to define the races are usually not well correlated with one an- other, and so the determination of race is always somewhat arbitrary. Humans are visually oriented; consequently, we have relied on visual cues—primarily skin color—to define races. However, when other types of characters, such as blood groups, are examined, patterns of variation corre- spond very poorly with visually determined racial classes. Indeed, if one were to break the human species into sub- units based on overall genetic similarity, the groupings would be very different than those based on skin color or other visual features (figure 23.16). In human beings, it is simply not possible to delimit clearly defined races that reflect biologically differentiated and well-defined groupings. The reason is simple: different groups of people have constantly intermingled and inter- bred with one another during the entire course of history. This constant gene flow has prevented the human species from fragmenting in highly differentiated subspecies. Those characteristics that are differentiated among popula- tions, such as skin color, represent classic examples of the antagonism between gene flow and natural selection. As we saw in chapter 20, when selection is strong enough, as it is for dark coloration in tropical regions, populations can differentiate even in the presence of gene flow. However, even in cases such as this, gene flow will still ensure that populations are relatively homogeneous for genetic varia- tion at other loci. For this reason, relatively little of the variation in the human species represents differences between the de- scribed races. Indeed, one study calculated that only 8% of all genetic variation among humans could be accounted for as differences that exist among racial groups; in other words, the human racial categories do a very poor job in describing the vast majority of genetic variation that exists in humans. For this reason, most modern biologists reject human racial classifications as reflecting patterns of biolog- ical differentiation in the human species. This is a sound biological basis for dealing with each human being on his or her own merits and not as a member of a particular “race.” Human races do not reflect significant patterns of underlying biological differentiation. Chapter 23 How Humans Evolved 491 FIGURE 23.16 Patterns of genetic variation in human populations differ from patterns of skin color variation. (a) Genetic variation among Homo sapiens. Eight categories of humans were recognized based on overall similarity at many enzyme and blood group genetic loci. The code below the figure is arranged in order of similarity. (b) Similarity among Homo sapiensbased on skin color. The categories are arranged by amount of pigmentation in the skin. Skin pigmentation Very dark Dark Medium Light Very light Order of genetic similarity (a) (b) 492 Part VI Evolution Chapter 23 Summary Questions Media Resources 23.1 The evolutionary path to humans starts with the advent of primates. ? Prehensile (grasping) fingers and toes and binocular vision were distinct adaptations that allowed early primates to be successful in their particular environments. ? Mainly diurnal (day-active) anthropoids and mainly nocturnal (night-active) prosimians diverged about 40 million years ago. Anthropoids include monkeys, apes, and humans, and all exhibit complex social interactions and enlarged brains. ? The hominoids evolved from anthropoid ancestors about 25 million years ago. Hominoids consist of the apes (gibbons, orangutans, gorillas, and chimpanzees) and upright-walking hominids (human beings and their direct ancestors). 1. Which characteristics were selected for in the earliest primates to allow them to become successful in their environment? 2. How do monkeys differ from prosimians? 3. How are apes distinguished from monkeys? 4. What is the best explanation for why humans and chimpanzees are so similar genetically? ? Early hominids belonging to the genus Australopithecuswere ancestral to humans. They exhibited bipedalism (walking upright on two feet) and lived in Africa over 4 million years ago. 5. When did the first hominids appear? What were they called? What distinguished them from the apes? 23.2 The first hominids to evolve were australopithecines. ? Hominids with an enlarged brain and the ability to use tools belong to the genus Homo.Species of early Homoappeared in Africa about 2 million years ago and became extinct about 1.5 million years ago. ? Homo erectusappeared in Africa at least 1.5 million years ago and had a much larger brain than early species of Homo.Homo erectusalso walked erect and presumably was able to talk. Within a million years, Homo erectusmigrated from Africa to Europe and Asia. 6. Why is there some doubt in the scientific community that Homo habiliswas a true human? 7. How did Homo erectus differ from Homo habilis? 23.3 The genus Homo evolved in Africa. ? The modern species of Homoappeared about 600,000 years ago in Africa and about 350,000 years ago in Eurasia. ? The Neanderthals appeared in Europe about 130,000 years ago. They made diverse tools and showed evidence of symbolic thinking. ? Studies of mitochondrial DNA suggest (but do not yet prove) that all of today’s human races originated from Africa. ? Categorization of humans into races does not adequately reflect patterns of genetic differentiation among people in different parts of the world. 8. The greatest number of different mitochondrial DNA sequences in humans occurs in Africa. What does this tell us about human evolution? 9. How did Cro-Magnons differ from Neanderthals? Is there any evidence that they coexisted with Neanderthals? If so, where and when? 10. Are the commonly recognized human races equivalent to subspecies of other plant and animal species? 23.4 Modern humans evolved quite recently. www.mhhe.com www.biocourse.com ? Evolution of Primates ? On Science Article: Human Evolution ? Huminid History 493 Why do tropical songbirds lay fewer eggs? Sometimes odd generalizations in science lead to unex- pected places. Take, for example, a long obscure mono- graph published in 1944 by British ornithologist (bird ex- pert) Reginald Moreau in the journal Ibis on bird eggs. Moreau had worked in Africa for many years before mov- ing to a professorship in England in the early 1940s. He was not in England long before noting that the British songbirds seemed to lay more eggs than he was accustomed to seeing in nests in Africa. He set out to gather informa- tion on songbird clutch size (that is, the number of eggs in a nest) all over the world. Wading through a mountain of data (his Ibis paper is 51 pages long!), Moreau came to one of these odd generaliza- tions: songbirds in the tropics lay fewer eggs than their counterparts at higher latitudes (see above right). Tropical songbirds typically lay a clutch of 2 or 3 eggs, on average, while songbirds in temperate and subarctic regions gener- ally lay clutches of 4 to 6 eggs, and some species as many as 10. The trend is general, affecting all groups of songbirds in all regions of the world. What is a biologist to make of such a generalization? At first glance, we would expect natural selection to maximize evolutionary fitness—that is, songbirds the world over should have evolved to produce as many eggs as possible. Clearly, the birds living in the tropics have not read Dar- win, as they are producing only half as many eggs as they are capable of doing. A way out of this quandary was proposed by ornitholo- gist Alexander Skutch in 1949. He argued that birds pro- duced just enough offspring to offset deaths in the popula- tion. Any extra offspring would be wasteful of individuals, and so minimized by natural selection. An interesting idea, but it didn’t hold water. Bird populations are not smaller in the tropics, or related to the size of the populations there. A second idea, put forward a few years earlier in 1947 by a colleague of Moreau’s, David Lack, was more promising. Lack, one of the twentieth-century’s great bi- ologists, argued that few if any birds ever produce as many eggs as they might under ideal conditions, for the simple reason that conditions in nature are rarely ideal. Natural selection will indeed tend to maximize reproduc- tive rate (that is, the number of eggs laid in clutches) as Darwin predicted, but only to the greatest level possible within the limits of resources. There is nothing here that would have surprised Darwin. Birds lay fewer eggs in the tropics simply because parents can gather fewer resources to provide their young there—competition is just too fierce, resources too scanty. Lack went on to construct a general theory of clutch size in birds. He started with the sensible assumption that in a resource-limited environment birds can supply only so much food to their young. Thus, the more offspring they have, the less they can feed each nestling. As a result, Lack proposed that natural selection will favor a compromise be- tween offspring number and investment in each offspring, which maximizes the number of offspring which are fed enough to survive to maturity. The driving force behind Lack’s theory of optimal clutch size is his idea that broods with too many offspring would be undernourished, reducing the probability that the chicks would survive. In Lack’s own words: “The average clutch-size is ultimately determined by the av- erage maximum number of young which the parents can success- fully raise in the region and at the season in question, i.e. ... nat- ural selection eliminates a disproportionately large number of young in those clutches which are higher than the average, through the inability of the parents to get enough food for their young, so that some or all of the brood die before or soon after fledging (leaving the nest), with the result that few or no descen- dants are left with their parent’s propensity to lay a larger clutch.” Part VII Ecology and Behavior This Kentucky warbler is tending her nest of eggs. A similar species in the tropics would lay fewer eggs. Why? 494 Part VII Ecology and Behavior The Experiment Lack’s theory is attractive because of its simplicity and common sense—but is it right? Many studies have been conducted to examine this hypothesis. Typically, experi- menters would remove eggs from nests, and look to see if this improved the survivorship of the remaining off- spring. If Lack is right, then it should, as the remaining offspring will have access to a larger share of what the parents can provide. Usually, however, removal of eggs did not seem to make any difference. Parents just ad- justed down the amount of food they provided. The situ- ation was clearly more complicated than Lack’s simple theory envisioned. One can always argue with tests such as these, how- ever, as they involve direct interference with the nests, potentially having a major influence on how the birds be- have. It is hard to believe that a bird caring for a nest of six eggs would not notice when one turned up missing. A clear test of Lack’s theory would require avoiding all intervention. Just such a test was completed in 1987 in the woods near Oxford, England. Over many years, Oxford University re- searchers led by Professor Mark Boyce (now at the Univer- sity of Wyoming, Laramie) carefully monitored nests of a songbird, the greater tit, very common in the English countryside. They counted the number of eggs laid in each nest (the clutch size) and then watched to see how many of the offspring survived to fly away from the nest. Nothing was done to interfere with the birds. Over 22 years, they patiently examined 4489 nests. The Results The Oxford researchers found that the average clutch size was 8 eggs, but that nests with the greatest number of sur- viving offspring had not 8 but 12 eggs in them! Clearly, Lack’s theory is wrong. These birds are not producing as many offspring as natural selection to maximize fitness (that is, number of surviving offspring) would predict (see above left). Lack’s proposal had seemed eminently sensible. What was wrong? In 1966 the evolutionary theorist George Williams suggested the problem was that Lack’s theory ig- nores the cost of reproduction (see above). If a bird spends too much energy feeding one brood, then it may not sur- vive to raise another. Looking after a large clutch may ex- tract too high a price in terms of future reproductive suc- cess of the parent. The clutch size actually favored by natural selection is adjusted for the wear-and-tear on the parents, so that it is almost always smaller than the number which would produce the most offspring in that nest—just what the Oxford researchers observed. However, even William’s “cost-of-reproduction” is not enough to completely explain Boyce’s greater tit data. There were marked fluctuations in the weather over the years that the Oxford researchers gathered their data, and they observed that harsh years decreased survival of the young in large nests more than in small ones. This “bad- year” effect reduces the fitness of individuals laying larger clutches, and Boyce argues that it probably contributes at least as much as cost-of-reproduction in making it more advantageous, in the long term, for birds to lay clutches smaller than the Lack optimum. Testing Lack’s theory of optimum clutch size. In this study from woods near Oxford, England, researchers found that the most common clutch size was 8, even though clutches of 12 pro- duced the greatest number of surviving offspring. (After Boyce and Perrins, 1987.) Two theories of optimum clutch size. David Lack’s theory pre- dicts that optimum clutch size will be where reproductive success of the clutch is greatest. George Williams’s theory predicts that optimum clutch size will be where the net benefit is greatest—that is, where the difference between the cost of reproduction and the reproductive success of the clutch is greatest. 495 24 Population Ecology Concept Outline 24.1 Populations are individuals of the same species that live together. Population Ecology. The borders of populations are determined by areas in which individuals cannot survive and reproduce. Population ranges expand and contract through time as conditions change. Population Dispersion. The distribution of individuals in a population can be clumped, random, or even. Metapopulations. Sometimes, populations are arranged in networks connected by the exchange of individuals. 24.2 Population dynamics depend critically upon age distribution. Demography. The growth rate of a population is a sensitive function of its age structure; populations with many young individuals grow rapidly as these individuals enter reproductive age. 24.3 Life histories often reflect trade-offs between reproduction and survival. The Cost of Reproduction. Evolutionary success is a trade-off between investment in current reproduction and in growth that promotes future reproduction. 24.4 Population growth is limited by the environment. Biotic Potential. Populations grow if the birthrate exceeds the death rate until they reach the carrying capacity of their environment. The Influence of Population Density. Some of the factors that regulate a population’s growth depend upon the size of the population; others do not. Population Growth Rates and Life History Models. Some species have adaptations for rapid, exponential population growth, whereas other species exhibit slower population growth and have intense competition for resources. 24.5 The human population has grown explosively in the last three centuries. The Advent of Exponential Growth. Human populations have been growing exponentially since the 1700s and will continue to grow in developing countries because of the number of young people entering their reproductive years. E cology, the study of how organisms relate to one an- other and to their environments, is a complex and fascinating area of biology that has important implications for each of us. In our exploration of ecological principles, we will first consider the properties of populations, em- phasizing population dynamics (figure 24.1). In chapter 25, we will discuss communities and the interactions that occur in them. Chapter 26 moves on to focus on animals and how and why they behave as they do. Chapter 27 then deals with behavior in an environmental context, the ex- tent to which natural selection has molded behaviors adaptively. FIGURE 24.1 Life takes place in populations. This population of gannets is subject to the rigorous effects of reproductive strategy, competition, predation, and other limiting factors. Population Distributions No population, not even of humans, occurs in all habitats throughout the world. Most species, in fact, have relatively limited geographic ranges. The Devil’s Hole pupfish, for example, lives in a single hot water spring in southern Nevada, and the Socorro isopod is known from a single spring system in Socorro, New Mexico (figure 24.2). At the other extreme, some species are widely distributed. Popula- tions of some whales, for example, are found throughout all of the oceans of the northern or southern hemisphere. In chapter 29 we will discuss the variety of environmental challenges facing organisms. Suffice it to say for now that no population contains individuals adapted to live in all of the different environments on the earth. Polar bears are exqui- sitely adapted to survive the cold of the Arctic, but you won’t find them in the tropical rain forest. Certain bacteria can live in the near boiling waters of Yellowstone’s geysers, but they do not occur in cooler streams that are nearby. Each popula- tion has its own requirements—temperature, humidity, cer- tain types of food, and a host of other factors—that deter- mine where it can live and reproduce and where it can’t. In addition, in places that are otherwise suitable, the presence of predators, competitors, or parasites may prevent a popula- tion from occupying an area. 496 Part VII Ecology and Behavior Population Ecology Organisms live as members of populations, groups of indi- viduals of a species that live together. In this chapter, we will consider the properties of populations, focusing on ele- ments that influence whether a population will grow or shrink, and at what rate. The explosive growth of the world’s human population in the last few centuries provides a focus for our inquiry. A population consists of the individuals of a given species that occur together at one place and time. This flex- ible definition allows us to speak in similar terms of the world’s human population, the population of protozoa in the gut of an individual termite, or the population of deer that inhabit a forest. Sometimes the boundaries defining a boundary are sharp, such as the edge of an isolated moun- tain lake for trout, and sometimes they are more fuzzy, such as when individuals readily move back and forth be- tween areas, like deer in two forests separated by a corn- field. Three aspects of populations are particularly important: the range throughout which a population occurs, the dis- persion of individuals within that range, and the size a pop- ulation attains. 24.1 Populations are individuals of the same species that live together. Iriomote cat Northern white rhinoceros New Guinea tree kangaroo Iiwi Hawaiian bird Pupfish Catalina Island mahogany tree FIGURE 24.2 Species that occur in only one place. These species, and many others, are only found in a single population. All are endangered species, and should anything happen to their single habitat, the population—and the species—would go extinct. Range Expansions and Contractions Population ranges are not static, but, rather, change through time. These changes occur for two reasons. In some cases, the environment changes. For example, as the glaciers retreated at the end of the last ice age, approximately 10,000 years ago, many North Ameri- can plant and animal populations ex- panded northward. At the same time, as climates have warmed, species have experienced shifts in the elevation at which they are found on mountains (figure 24.3). In addition, populations can ex- pand their ranges when they are able to circumvent inhospitable habitat to colonize suitable, previously unoccu- pied areas. For example, the cattle egret is native to Africa. Some time in the late 1800s, these birds ap- peared in northern South America, having made the nearly 2000-mile transatlantic crossing, perhaps aided by strong winds. Since then, they have steadily expanded their range such that they now can be found throughout most of the United States (figure 24.4). Chapter 24 Population Ecology 497 Present Alpine tundra Spruce-fir forests Mixed conifer forest Woodlands Woodlands Grassland, chaparral, and desert scrub Grassland, chaparral, and desert scrub 15,000 years ago Alpine tundra Spruce-fir forests Mixed conifer forest Elevation (km) 0 km 2 km 3 km 1 km FIGURE 24.3 Altitudinal shifts in population ranges. During the glacial period 15,000 years ago, conditions were cooler than they are now. As the climate has warmed, tree species that require colder temperatures have shifted their distributional range upward in altitude so that they live in the climatic conditions to which they are adapted. Equator 1937 1943 19511958 1961 1960 19651964 1966 1970 1970 1956 Immigration from Africa FIGURE 24.4 Range expansion of the cattle egret. Although the cattle egret—so-named because it follows cattle and other hoofed animals, catching any insects or small vertebrates that they disturb—first arrived in South America in the late 1800s, the oldest preserved specimen dates from the 1930s. Since then, the range expansion of this species has been well documented, as it has moved westward and up into much of North America, as well as down the western side of the Andes to near the southern tip of South America. Population Dispersion Another key characteristic of population structure is the way in which individuals of a population are arranged. They may be randomly spaced, uniformly spaced, or clumped (figure 24.5). Randomly spaced Individuals are randomly spaced within populations when they do not interact strongly with one another or with nonuniform aspects of their microenvironment. Random distributions are not common in nature. Some species of trees, however, appear to exhibit random distributions in Amazonian rain forests. Uniformly spaced Individuals often are uniformly spaced within a population. This spacing may often, but not always, result from compe- tition for resources. The means by which it is accom- plished, however, varies. In animals, uniform spacing often results from behav- ioral interactions, which we will discuss in chapter 27. In many species, individuals of one or both sexes defend a ter- ritory from which other individuals are excluded. These territories serve to provide the owner with exclusive access to resources such as food, water, hiding refuges, or mates and tend to space individuals evenly across the habitat. Even in nonterritorial species, individuals often maintain a defended space into which other animals are not allowed to intrude. Among plants, uniform spacing also is a common result of competition for resources. In this case, however, the spacing results from direct competition for the resources. Closely spaced individual plants will contest for available sunlight, nutrients, or water. These contests can be direct, such as one plant casting a shadow over another, or indi- rect, such as two plants competing to see which is more efficient at extracting nutrients or water from a shared area. Only plants that are spaced an adequate distance from each other will be able to coexist, leading to uniform spacing. 498 Part VII Ecology and Behavior Clumped (a) Bacterial colonies UniformRandom ?? ? ?? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ?? ? ? ?? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ?? ?? ? ?? ? ? ? ? ? ? ?? ? ? ? ?? ?? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ?? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ?? ? ? ? ?? ? ? ? ? ? ? ? ?? ? ? ? ?? ? ? ? ? ? ? ? ? (b) Random distribution of Brosimum alicastrum (c) Uniform distribution of Coccoloba coronata (d) Clumped distribution of Chamguava schippii ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ?? ?? ?? ?? ? ? ? ?? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ?? ? ? ? ? ? FIGURE 24.5 Population dispersion. (a) Different arrangements of bacterial colonies. The different patterns of dispersion are exhibited by three different species of trees from the same locality in the Amazonian rain forest. (b) Brosimum alicastrum is randomly dispersed, (b) Coccoloba coronata is uniformly dispersed, and (d) Chamguava schippii exhibits a clumped distribution. Clumped Spacing Individuals clump into groups or clusters in response to un- even distribution of resources in their immediate environ- ments. Clumped distributions are common in nature be- cause individual animals, plants, and microorganisms tend to prefer microhabitats defined by soil type, moisture, or certain kinds of host trees. Social interactions also can lead to clumped distribu- tions. Many species live and move around in large groups, which go by a variety of names (examples include herds of antelope, flocks of birds, gaggles of geese, packs of wolves, prides of lions). Such groupings can provide many advan- tages, including increased awareness of and defense against predators, decreased energetic cost of moving through air and water, and access to the knowledge of all group members. At a broader scale, populations are often most densely populated in the interior of their range and less densely dis- tributed toward the edges. Such patterns usually result from the manner in which the environment changes in dif- ferent areas. Populations are often best adapted to the con- ditions in the interior of their distribution. As environmen- tal conditions change, individuals are less well adapted and thus densities decrease. Ultimately, the point is reached at which individuals cannot persist at all; this marks the edge of a population’s range. The Human Effect By altering the environment, we have allowed some species, such as coyotes, to expand their ranges, although, sadly, for most species the effect has been detrimental. Moreover, humans have served as an agent of dispersal for many species. Some of these transplants have been widely successful. For example, 100 starlings were introduced into New York City in 1896 in a misguided attempt to es- tablish every species of bird mentioned by Shakespeare. Their population steadily spread such that by 1980, they occurred throughout the United States. Similar stories could be told for countless numbers of plants and animals, and the list increases every year. Unfortunately, the suc- cess of these invaders often comes at the expense of native species. Dispersal Mechanisms Dispersal to new areas can occur in many ways. Lizards, for example, have colonized many distant islands, probably by individuals or their eggs floating or drifting on vegeta- tion. Seeds of many plants are designed to disperse in many ways (figure 24.6). Some seeds are aerodynamically designed to be blown long distances by the wind. Others have structures that stick to the fur or feathers of animals, so that they are carried long distances before falling to the ground. Still others are enclosed in fruits. These seeds can pass through the digestive systems of mammals or birds and then germinate at the spot upon which they are defe- cated. Finally, seeds of Arceuthobium are violently pro- pelled from the base of the fruit in an explosive discharge. Although the probability of long-distance dispersal events occurring and leading to successful establishment of new populations is slim, over millions of years, many such dis- persals have occurred. A population is a group of individuals of the same species living together at the same place and time. The range of a population is limited by ecologically inhospitable habitats, but through time, these range boundaries can change. Chapter 24 Population Ecology 499 Solanum dulcamara Juniperus chinensis Rubus sp. Windblown fruits Adherent fruits Fleshy fruits Asclepias syriaca Acer saccharum Terminalia calamansanai Ranunculus muricatusBidens frondosaMedicago polycarpa FIGURE 24.6 Some of the many adaptations of seeds to facilitate dispersal. Seeds have evolved a number of different means of moving long distances from their maternal plant. Metapopulations Species are often composed of a network of distinct popu- lations that interact with each other by exchanging individ- uals. Such networks are termed metapopulations and usu- ally occur in areas in which suitable habitat is patchily distributed and separated by intervening stretches of un- suitable habitat. To what degree populations within a metapopulation in- teract depends on the amount of dispersal and is often not symmetrical: populations increasing in size may tend to send out many dispersers, whereas populations at low levels will tend to receive more immigrants than they send off. In addition, relatively isolated populations will tend to receive relatively few arrivals. Not all suitable habitats within a metapopulation’s area may be occupied at any one time. For various reasons, some individual populations may go extinct, perhaps as a result of an epidemic disease, a catastrophic fire, or in- breeding depression. However, because of dispersal from other populations, such areas may eventually be recolo- nized. In some cases, the number of habitats occupied in a metapopulation may represent an equilibrium in which the rate of extinction of existing populations is balanced by the rate of colonization of empty habitats. A second type of metapopulation structure occurs in areas in which some habitats are suitable for long-term population maintenance, whereas others are not. In these situations, termed source-sink metapopulations, the populations in the better areas (the sources) continually send out dispersers that bolster the populations in the poorer habitats (the sinks). In the absence of such continual replenishment, sink populations would have a negative growth rate and would eventually become extinct. Metapopulations of butterflies have been studied partic- ularly intensively (figure 24.7). In one study, Ilkka Hanski and colleagues at the University of Helsinki sampled pop- ulations of the glanville fritillary butterfly at 1600 mead- ows in southwestern Finland. On average, every year, 200 populations became extinct, but 114 empty meadows were colonized. A variety of factors seemed to increase the like- lihood of a population’s extinction, including small popu- lation size, isolation from sources of immigrants, low re- source availability (as indicated by the number of flowers on a meadow), and lack of genetic variation present within the population. The researchers attribute the greater num- ber of extinctions than colonizations to a string of very dry summers. Because none of the populations is large enough to survive on its own, continued survival of the species in southwestern Finland would appear to require the contin- ued existence of a metapopulation network in which new populations are continually created and existing popula- tions are supplemented by emigrants. Continued bad weather thus may doom the species, at least in this part of its range. Metapopulations, where they occur, can have two im- portant implications for the range of a species. First, by continual colonization of empty patches, they prevent long-term extinction. If no such dispersal existed, then each population might eventually perish, leading to disap- pearance of the species from the entire area. Moreover, in source-sink metapopulations, the species as a whole occu- pies a larger area than it otherwise might occupy. For these reasons, the study of metapopulations has become very important in conservation biology as natural habitats become increasingly fragmented. The distribution of individuals within a population can be random, uniform, or clumped. Across broader areas, individuals may occur in populations that are loosely interconnected, termed metapopulations. 500 Part VII Ecology and Behavior 10 km Occupied habitat patch Unoccupied habitat patch Norway Sweden Finland ?land Islands FIGURE 24.7 Metapopulations of butterflies. The glanville fritillary butterfly occurs in metapopulations in southwestern Finland on the ?land Islands. None of the populations is large enough to survive for long on its own, but continual emigration of individuals from other populations allows some populations to survive. In addition, continual establishment of new populations tends to offset extinction of established populations, although in recent years, extinctions have outnumbered colonizations. One of the important features of any population is its size. Population size has a direct bearing on the ability of a given population to survive: for a variety of reasons dis- cussed in chapter 31, smaller populations are at a greater risk of disappearing than large populations. In addition, the interactions that occur between members of a popu- lation also depend critically on a population’s size and density. Demography Demography (from the Greek demos, “the people,” + graphos, “measurement”) is the statistical study of popula- tions. How the size of a population changes through time can be studied at two levels. At the most inclusive level, we can study the population as a whole to determine whether it is increasing, decreasing, or remaining constant. Popula- tions grow if births outnumber deaths and shrink if deaths outnumber births. Understanding these trends is often eas- ier if we break a population down into its constituent parts and analyze each separately. Factors Affecting Population Growth Rates The proportion of males and females in a population is its sex ratio. The number of births in a population is usually directly related to the number of females, but may not be as closely related to the number of males in species in which a single male can mate with several fe- males. In many species, males compete for the opportu- nity to mate with females (a situation we discuss in chap- ter 27); consequently, a few males get many matings, whereas many males do not mate at all. In such species, a female-biased sex ratio would not affect population growth rates; reduction in the number of males simply changes the identities of the reproductive males without reducing the number of births. Among monogamous species like many birds, by contrast, in which pairs form long-lasting reproductive relationships, a reduction in the number of males can directly reduce the number of births. Generation time, defined as the average interval be- tween the birth of an individual and the birth of its off- spring, can also affect population growth rates. Species differ greatly in generation time. Differences in body size can explain much of this variation—mice go through ap- proximately 100 generations during the course of one ele- phant generation—but not all of it (figure 24.8). Newts, for example, are smaller than mice, but have considerably longer generation times. Everything else equal, popula- tions with shorter generations can increase in size more quickly than populations with long generations. Con- versely, because generation time and life span are usually closely correlated, populations with short generation times may also diminish in size more rapidly if birthrates suddenly decrease. Chapter 24 Population Ecology 501 24.2 Population dynamics depend critically upon age distribution. ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? 1 H9262m 10 H9262m 100 H9262m 1 mm 1 cm 10 cm 1 m 10 m 100 m Generation time 1 hour 1 day 1 week 1 month 1 year 10 years 100 years B. aureus Pseudomonas E. coli Spirochaeta Euglena Tetrahymena Didinium Paramecium Stentor Daphnia Drosophila Housefly Clam Horsefly Bee Oyster Snail Chameleon Scallop Frog Mouse Newt Turtle Horseshoe crab Crab Rat Salamander Fox Beaver Snake Man Deer Elk Bear Elephant Rhino Dogwood Balsam Birch Kelp Whale Fir Sequoia Body size (le n g th) FIGURE 24.8 The relationship between body size and generation time. In general, larger animals have longer generation times, although there are exceptions. Age Structure In most species, the probability that an individual will re- produce or die varies through its life span. A group of indi- viduals of the same age is referred to as a cohort. Within a population, every cohort has a characteristic birthrate, or fecundity, defined as the number of offspring produced in a standard time (for example, per year), and a characteristic death rate, or mortality, the number of individuals that die in that period. The relative number of individuals in each cohort de- fines a population’s age structure. Because individuals of different ages have different fecundity and death rates, age structure has a critical impact on a population’s growth rate. Populations with a large proportion of young individuals, for example, tend to grow rapidly be- cause an increasing proportion of their individuals are re- productive. Populations in many underdeveloped coun- tries are an example, as we will discuss later in the chapter. Conversely, if a large proportion of a population is relatively old, populations may decline. This phenome- non now characterizes some wealthy countries in Europe and Japan. Life Tables and Population Change through Time Ecologists use life tables to assess how populations in na- ture are changing. Life tables can be constructed by follow- ing the fate of a cohort from birth until death, noting the number of offspring produced and individuals that die each year. A very nice example of a life table analysis is exhibited in a study of the meadow grass Poa annua. This study fol- lows the fate of 843 individuals through time, charting how many survive in each interval and how many offspring each survivor produces (table 24.1). In table 24.1, the first column indicates the age of the cohort (that is, the number of 3-month intervals from the start of the study). The second and third columns indicate the number of survivors and the proportion of the original cohort still alive at the beginning of that interval. The fourth column presents the mortality rate, the proportion of individuals that started that interval alive but died by the end of it. The fifth column indicates the average number of seeds produced by each surviving individual in that interval, and the last column presents the number of seeds produced relative to the size of the original cohort. 502 Part VII Ecology and Behavior Table 24.1 Life Table for a Cohort of the grass Poa annua Seeds Age Proportion of cohort produced (in 3- Number alive at surviving to beginning Mortality per surviving Fecundity month beginning of time of time interval rate during individual H11003 intervals) interval (survivorship) time interval (fecundity) survivorship 0 843 1.000 0.143 0.00 0.00 1 722 0.857 0.271 0.42 0.36 2 527 0.625 0.400 1.18 0.74 3 316 0.375 0.544 1.36 0.51 4 144 0.171 0.626 1.46 0.25 5 54 0.064 0.722 1.11 0.07 6 15 0.018 0.800 2.00 0.04 7 3 0.004 1.000 3.33 0.01 8 0 0.000 Total = 1.98 Modified from Ricklefs, 1997. Much can be learned from examination of life tables. In this particular case, we see that the probability of dying increases steadily with age, whereas the number of off- spring produced increases with age. By adding up the numbers in the last column, we get the total number of offspring produced per individual in the initial cohort. This number is almost 2, which means that for every orig- inal member of the cohort, on average two individuals have been produced. A figure of 1.0 would be the break- even number, the point at which the population was nei- ther growing nor shrinking. In this case, the population appears to be growing rapidly. In most cases, life table analysis is more complicated than this. First, except for organisms with short life spans, it is difficult to track the fate of a cohort from birth until death of the last individual. An alternative approach is to construct a cross-sectional study, examining the fate of all cohorts over a single year. In addition, many factors— such as offspring reproducing before all members of their parental generation’s cohort have died—complicate the interpretation of whether populations are growing or shrinking. Survivorship Curves One way to express some aspects of the age distribution characteristics of populations is through a survivorship curve. Survivorship is defined as the percentage of an orig- inal population that survives to a given age. Examples of different kinds of survivorship curves are shown in figure 24.9. In hydra, animals related to jellyfish, individuals are equally likely to die at any age, as indicated by the straight survivorship curve (type II). Oysters, like plants, produce vast numbers of offspring, only a few of which live to re- produce. However, once they become established and grow into reproductive individuals, their mortality rate is ex- tremely low (type III survivorship curve). Finally, even though human babies are susceptible to death at relatively high rates, mortality rates in humans, as in many animals and protists, rise steeply in the postreproductive years (type I survivorship curve). Examination of the data for Poa annua reveals that it approximates a type II survivorship curve (figure 24.10). The growth rate of a population is a sensitive function of its age structure. The age structure of a population and the manner in which mortality and birthrates vary among different age cohorts determine whether a population will increase or decrease in size. Chapter 24 Population Ecology 503 0 25 Survival per thousand 1000 100 Human (type I) Hydra (type II) Oyster (type III) 10 1 50 Percent of maximum life span 100 75 FIGURE 24.9 Survivorship curves. By convention, survival (the vertical axis) is plotted on a log scale. Humans have a type I life cycle, the hydra (an animal related to jellyfish) type II, and oysters type III. 3 2 3 4 5 10 20 30 40 50 100 200 300 400 500 1000 6 9 12 15 Age (months) Survival per thousand 18 21 24 27 FIGURE 24.10 Survivorship curve for a cohort of the meadow grass, Poa annua. Mortality increases at a constant rate through time. Natural selection favors traits that maximize the number of surviving offspring left in the next generation. Two factors affect this quantity: how long an individual lives and how many young it produces each year. Why doesn’t every organism reproduce immediately after its own birth, produce large families of large offspring, care for them intensively, and do this repeatedly throughout a long life, while outcompeting others, escaping predators, and capturing food with ease? The answer is that no one organism can do all of this—there are simply not enough resources available. Consequently, organisms allocate re- sources either to current reproduction or to increase their prospects of surviving and reproducing at later life stages. The Cost of Reproduction The complete life cycle of an organism constitutes its life history. All life histories involve significant trade-offs. Because resources are limited, a change that increases re- production may decrease survival and reduce future re- production. Thus, a Douglas fir tree that produces more cones increases its current reproductive success, but it also grows more slowly; because the number of cones produced is a function of how large a tree is, this dimin- ished growth will decrease the number of cones it can produce in the future. Similarly, birds that have more offspring each year have a higher probability of dying during that year or producing smaller clutches the fol- lowing year (figure 24.11). Conversely, individuals that delay reproduction may grow faster and larger, enhanc- ing future reproduction. In one elegant experiment, researchers changed the number of eggs in nests of a bird, the collared flycatcher (figure 24.12). Birds whose clutch size (the number of eggs produced in one breeding event) was decreased laid more eggs the next year, whereas those given more eggs produced fewer eggs the following year. Ecologists refer to the reduction in future reproductive potential result- ing from current reproductive efforts as the cost of reproduction. Natural selection will favor the life history that maxi- mizes lifetime reproductive success. When the cost of re- production is low, individuals should invest in producing as many offspring as possible because there is little cost. Low costs of reproduction may occur when resources are abun- dant, such that producing offspring does not impair sur- vival or the ability to produce many offspring in subsequent years. Costs of reproduction will also be low when overall mortality rates are high. In such cases, individuals may be unlikely to survive to the next breeding season anyway, so the incremental effect of increased reproductive efforts may not make a difference in future survival. Alternatively, when costs of reproduction are high, life- time reproductive success may be maximized by deferring or minimizing current reproduction to enhance growth and survival rates. This may occur when costs of reproduction significantly affect the ability of an individual to survive or decrease the number of offspring that can be produced in the future. 504 Part VII Ecology and Behavior 24.3 Life histories often reflect trade-offs between reproduction and survival. 1.00.50.2 Annual adult mortality rate Annual fecundity rate 0.10.05 5 2 1 0.5 0.2 0.1 FIGURE 24.11 Reproduction has a price. Increased fecundity in birds correlates with higher mortality in several populations of birds ranging from albatross (low) to sparrow (high). Birds that raise more offspring per year have a higher probability of dying during that year. +2+10 Change in clutch size Clutch size following year –1–2 7 6 5 FIGURE 24.12 Reproductive events per lifetime. Adding eggs to nests of collared flycatchers (which increases the reproductive efforts of the female rearing the young) decreases clutch size the following year; removing eggs from the nest increases the next year’s clutch size. This experiment demonstrates the tradeoff between current reproductive effort and future reproductive success. Investment per Offspring In terms of natural selection, the number of offspring pro- duced is not as important as how many of those offspring themselves survive to reproduce. A key reproductive trade-off concerns how many re- sources to invest in producing any single offspring. As- suming that the amount of energy to be invested in off- spring is limited, a trade-off must exist between the number of offspring produced and the size of each off- spring (figure 24.13). This trade-off has been experimen- tally demonstrated in the side-blotched lizard, Uta stans- buriana, which normally lays on average four and a half eggs at a time. When some of the eggs are removed sur- gically early in the reproductive cycle, the female lizard produces only 1 to 3 eggs, but supplies each of these eggs with greater amounts of yolk, producing eggs that are much larger than normal. In many species, the size of offspring critically affects their survival prospects—larger offspring have a greater chance of survival. Producing many offspring with little chance of survival might not be the best strategy, but pro- ducing only a single, extraordinarily robust offspring also would not maximize the number of surviving offspring. Rather, an intermediate situation, in which several fairly large offspring are produced, should maximize the number of surviving offspring. This example is fundamentally the same as the trade-off between clutch size and parental in- vestment discussed above; in this case, the parental invest- ment is simply how many resources can be invested in each offspring before they are born. Reproductive Events per Lifetime The trade-off between age and fecundity plays a key role in many life histories. Annual plants and most insects focus all of their reproductive resources on a single large event and then die. This life history adaptation is called semelparity (from the Latin semel, “once,” H11001 parito, “to beget”). Organisms that produce offspring several times over many seasons exhibit a life history adaptation called iteroparity (from the Latin itero, “to repeat”). Species that reproduce yearly must avoid overtaxing themselves in any one reproductive episode so that they will be able to survive and reproduce in the future. Semelparity, or “big bang” reproduction, is usually found in short-lived species in which the probability of staying alive between broods is low, such as plants growing in harsh climates. Semelparity is also favored when fecundity entails large reproductive cost, as when Pacific salmon migrate upriver to their spawning grounds. In these species, rather than investing some resources in an unlikely bid to survive until the next breeding season, individuals place all their resources into reproduction. Age at First Reproduction Among mammals and many other animals, longer-lived species reproduce later (figure 24.14). Birds, for example, gain experience as juveniles before expending the high costs of reproduction. In long-lived animals, the relative advantage of juvenile experience outweighs the energy in- vestment in survival and growth. In shorter-lived animals, on the other hand, quick reproduction is more critical than juvenile training, and reproduction tends to occur earlier. Life history adaptations involve many trade-offs between reproductive cost and investment in survival. Different kinds of animals and plants employ quite different approaches. Chapter 24 Population Ecology 505 ? ? ? ? ? ? ? ? ? ? ? ? ? 024 68101214 17.5 18.0 18.5 19.0 19.5 Clutch size Nes t lin g size (weig h t i n g r a ms) FIGURE 24.13 The relationship between clutch size and offspring size. In great tits, the size of nestlings is inversely related to the number of eggs laid. The more mouths they have to feed, the less the parents can provide to any one nestling. Vole –0.8–1.2 Mouse Warthog –0.8 –1.2 Pig Lynx Impala Beaver Hippo Sheep Otter Cottontail rabbit Red squirrel African elephant Pika Chipmunk Kob –0.4 0.0 0.4 0.8 –0.4 Relative life expectancy Relative age at first reproduction 0.0 0.4 0.8 FIGURE 24.14 Age at first reproduction. Among mammals, compensating for the effects of size, age at first reproduction increases with life expectancy at birth. Each dot represents a species. Values are relative to the species symbolized H18554. (After Begon et al., 1996.) Biotic Potential Populations often remain at a relatively constant size, re- gardless of how many offspring they produce. As you saw in chapter 1, Darwin based his theory of natural selection partly on this seeming contradiction. Natural selection oc- curs because of checks on reproduction, with some individ- uals reproducing less often than others. To understand populations, we must consider how they grow and what factors in nature limit population growth. The Exponential Growth Model The actual rate of population increase, r, is defined as the difference between the birth rate and the death rate cor- rected for any movement of individuals in or out of the population, whether net emigration (movement out of the area) or net immigration (movement into the area). Thus, r = (b – d) + (i – e) Movements of individuals can have a major impact on population growth rates. For example, the increase in human population in the United States during the closing decades of the twentieth century is mostly due to immi- grants. Less than half of the increase came from the repro- duction of the people already living there. The simplest model of population growth assumes a population growing without limits at its maximal rate. This rate, called the biotic potential, is the rate at which a pop- ulation of a given species will increase when no limits are placed on its rate of growth. In mathematical terms, this is defined by the following formula: dN = r i N dt where N is the number of individuals in the population, dN/dt is the rate of change in its numbers over time, and r i is the intrinsic rate of natural increase for that population— its innate capacity for growth. The innate capacity for growth of any population is ex- ponential (red line in figure 24.15). Even when the rate of increase remains constant, the actual increase in the num- ber of individuals accelerates rapidly as the size of the population grows. The result of unchecked exponential growth is a population explosion. A single pair of house- flies, laying 120 eggs per generation, could produce more than 5 trillion descendants in a year. In 10 years, their de- scendants would form a swarm more than 2 meters thick over the entire surface of the earth! In practice, such pat- terns of unrestrained growth prevail only for short peri- ods, usually when an organism reaches a new habitat with abundant resources (figure 24.16). Natural examples in- clude dandelions reaching the fields, lawns, and meadows 506 Part VII Ecology and Behavior 24.4 Population growth is limited by the environment. 1250 1000 750 = 1.0 N dN dt 500 250 0 0510 Number of generations (t) Population size ( N ) 15 = 1.0 N Carrying capacity dN dt 1000 – N 1000 FIGURE 24.15 Two models of population growth. The red line illustrates the exponential growth model for a population with an r of 1.0. The blue line illustrates the logistic growth model in a population with r = 1.0 and K = 1000 individuals. At first, logistic growth accelerates exponentially, then, as resources become limiting, the death rate increases and growth slows. Growth ceases when the death rate equals the birthrate. The carrying capacity (K) ultimately depends on the resources available in the environment. FIGURE 24.16 An example of a rapidly increasing population. European purple loosestrife, Lythrum salicaria, became naturalized over thousands of square miles of marshes and other wetlands in North America. It was introduced sometime before 1860 and has had a negative impact on many native plants and animals. of North America from Europe for the first time; algae colonizing a newly formed pond; or the first terrestrial immigrants arriving on an island recently thrust up from the sea. Carrying Capacity No matter how rapidly populations grow, they eventually reach a limit imposed by shortages of important environ- mental factors, such as space, light, water, or nutrients. A population ultimately may stabilize at a certain size, called the carrying capacity of the particular place where it lives. The carrying capacity, symbolized by K, is the maximum number of individuals that a population can support. The Logistic Growth Model As a population approaches its carrying capacity, its rate of growth slows greatly, because fewer resources remain for each new individual to use. The growth curve of such a population, which is always limited by one or more factors in the environment, can be approximated by the following logistic growth equation: dN = rN ( K-N ) dt K In this logistic model of population growth, the growth rate of the population (dN/dt) equals its rate of increase (r multiplied by N, the number of individuals present at any one time), adjusted for the amount of resources available. The adjustment is made by multiplying rN by the fraction of K still unused (K minus N, divided by K). As N in- creases (the population grows in size), the fraction by which r is multiplied (the remaining resources) becomes smaller and smaller, and the rate of increase of the popu- lation declines. In mathematical terms, as N approaches K, the rate of population growth (dN/dt) begins to slow, reaching 0 when N = K (blue line in figure 24.18). Graphically, if you plot N versus t (time) you obtain an S-shaped sigmoid growth curve characteristic of many biological populations. The curve is called “sigmoid” because its shape has a double curve like the letter S. As the size of a population stabilizes at the carrying capacity, its rate of growth slows down, eventually coming to a halt (figure 24.17a). In many cases, real populations display trends corre- sponding to a logistic growth curve. This is true not only in the laboratory, but also in natural populations (figure 24.17b). In some cases, however, the fit is not perfect (fig- ure 24.17c) and, as we shall see shortly, many populations exhibit other patterns. The size at which a population stabilizes in a particular place is defined as the carrying capacity of that place for that species. Populations often grow to the carrying capacity of their environment. Chapter 24 Population Ecology 507 0 5 10 15 20 25 Time (days) 500 400 300 200 100 0 Number o f p a ramecia ( p e r c m 3 ) ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? (a) (c) 10 8 6 4 2 0 Time (years) Number of breeding male fur seals (thousands) 1915 1925 1935 1945 ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? (b) 500 400 300 200 100 0 20010 30 5040 60 Time (days) Numb er of cladocera n s (pe r 20 0 m l) FIGURE 24.17 Most natural populations exhibit logistic growth. (a) Paramecium grown in a laboratory environment. (b) A fur seal (Callorhinus ursinus) population on St. Paul Island, Alaska. (c) Laboratory populations of two populations of the cladoceran Bosmina longirsotris. Note that the populations first exceeded the carrying capacity, before decreasing to a size which was then maintained. The Influence of Population Density The reason that population growth rates are affected by population size is that many important processes are density-dependent. When populations approach their carrying capacity, competition for resources can be severe, leading both to a decreased birthrate and an increased risk of mortality (figure 24.18). In addition, predators often focus their attention on particularly common prey, which also results in increasing rates of mortality as populations increase. High population densities can also lead to an ac- cumulation of toxic wastes, a situation to which humans are becoming increasingly accustomed. Behavioral changes may also affect population growth rates. Some species of rodents, for example, become antiso- cial, fighting more, breeding less, and generally acting stressed-out. These behavioral changes result from hor- monal actions, but their ultimate cause is not yet clear; most likely, they have evolved as adaptive responses to situ- ations in which resources are scarce. In addition, in crowded populations, the population growth rate may de- crease because of an increased rate of emigration of indi- viduals attempting to find better conditions elsewhere (fig- ure 24.19). However, not all density-dependent factors are nega- tively related to population size. In some cases, growth rates increase with population size. This phenomenon is re- ferred to as the Allee effect (after Warder Allee, who first described it). The Allee effect can take several forms. Most obviously, in populations that are too sparsely distributed, individuals may have difficulty finding mates. Moreover, some species may rely on large groups to deter predators or to provide the necessary stimulation for breeding activities. 508 Part VII Ecology and Behavior 0.4 0.5 0.7 0.6 0.8 0.9 40 80 Number of adults Juvenile mortality 12010060200 140 160 ? ? ? ? ? ? ? ? ? ? ? ? ? 2.0 1.0 3.0 4.0 5.0 20 40 Number of breeding females Number of surviving young per female 605030100 70 80 ? ? ? ? ? ? ? ? ? ? ? (a) (b) FIGURE 24.18 Density dependence in the song sparrow (Melospiza melodia) on Mandarte Island. Reproductive success decreases (a) and mortality rates increase (b) as population size increases. FIGURE 24.19 Density-dependent effects. Migratory locusts, Locusta migratoria, are a legendary plague of large areas of Africa and Eurasia. At high population densities, the locusts have different hormonal and physical characteristics and take off as a swarm. The most serious infestation of locusts in 30 years occurred in North Africa in 1988. Density-Independent Effects Growth rates in populations sometimes do not correspond to the logistic growth equation. In many cases, such patterns result because growth is under the control of density-independent effects. In other words, the rate of growth of a population at any instant is limited by something other than the size of the population. A variety of factors may affect popula- tions in a density-independent manner. Most of these are aspects of the external environment. Extremely cold winters, droughts, storms, volcanic eruptions— individuals often will be affected by these activities regardless of the size of the population. Populations that occur in areas in which such events occur rela- tively frequently will display erratic pop- ulation growth patterns in which the populations increase rapidly when condi- tions are benign, but suffer extreme reductions whenever the environment turns hostile. Population Cycles Some populations exhibit another type of pattern incon- sistent with simple logistic equations: they exhibit cyclic patterns of increase and decrease. Ecologists have studied cycles in hare populations since the 1920s. They have found that the North American snowshoe hare (Lepus americanus) follows a “10-year cycle” (in reality, it varies from 8 to 11 years). Its numbers fall tenfold to 30-fold in a typical cycle, and 100-fold changes can occur. Two fac- tors appear to be generating the cycle: food plants and predators. Food plants. The preferred foods of snowshoe hares are willow and birch twigs. As hare density increases, the quantity of these twigs decreases, forcing the hares to feed on high-fiber (low-quality) food. Lower birthrates, low juvenile survivorship, and low growth rates follow. The hares also spend more time searching for food, ex- posing them more to predation. The result is a precipi- tous decline in willow and birch twig abundance, and a corresponding fall in hare abundance. It takes two to three years for the quantity of mature twigs to recover. Predators. A key predator of the snowshoe hare is the Canada lynx (Lynx canadensis). The Canada lynx shows a “10-year” cycle of abundance that seems remarkably en- trained to the hare abundance cycle (figure 24.20). As hare numbers increase, lynx numbers do, too, rising in response to the increased availability of lynx food. When hare numbers fall, so do lynx numbers, their food supply depleted. Which factor is responsible for the predator-prey oscil- lations? Do increasing numbers of hares lead to overhar- vesting of plants (a hare-plant cycle) or do increasing num- bers of lynx lead to overharvesting of hares (a hare-lynx cycle)? Field experiments carried out by C. Krebs and coworkers in 1992 provide an answer. Krebs set up experi- mental plots in Canada’s Yukon-containing hare popula- tions. If food is added (no food effect) and predators ex- cluded (no predator effect) from an experimental area, hare numbers increase tenfold and stay there—the cycle is lost. However, the cycle is retained if either of the factors is al- lowed to operate alone: exclude predators but don’t add food (food effect alone), or add food in presence of preda- tors (predator effect alone). Thus, both factors can affect the cycle, which, in practice, seems to be generated by the interaction between the two factors. Population cycles traditionally have been considered to occur rarely. However, a recent review of nearly 700 long- term (25 years or more) studies of trends within popula- tions found that cycles were not uncommon; nearly 30% of the studies—including birds, mammals, fish, and crus- taceans—provided evidence of some cyclic pattern in popu- lation size through time, although most of these cycles are nowhere near as dramatic in amplitude as the snowshoe hare and lynx cycles. Density-dependent effects are caused by factors that come into play particularly when the population size is larger; density-independent effects are controlled by factors that operate regardless of population size. Chapter 24 Population Ecology 509 1845 1855 1865 1875 1885 1895 1905 1915 1925 1935 40 0 80 120 160 Year Number of pelts (in thousands) Snowshoe hare Lynx FIGURE 24.20 Linked population cycles of the snowshoe hare and the northern lynx. These data are based on records of fur returns from trappers in the Hudson Bay region of Canada. The lynx populations carefully track the snowshoe hares, but lag behind them slightly. Population Growth Rates and Life History Models As we have seen, some species usually have stable popula- tion sizes maintained near the carrying capacity, whereas the populations of other species fluctuate markedly and are often far below carrying capacity. As we saw in our discus- sion of life histories, the selective factors affecting such species will differ markedly. Populations near their carrying capacity may face stiff competition for limited resources. By contrast, resources are abundant in populations far below carrying capacity. We have already seen the consequences of such differ- ences. When resources are limited, the cost of reproduc- tion often will be very high. Consequently, selection will favor individuals that can compete effectively and utilize re- sources efficiently. Such adaptations often come at the cost of lowered reproductive rates. Such populations are termed K-selected because they are adapted to thrive when the population is near its carrying capacity (K). Table 24.2 lists some of the typical features of K-selected populations. Ex- amples of K-selected species include coconut palms, whooping cranes, whales, and humans. By contrast, in populations far below the carrying ca- pacity, resources may be abundant. Costs of reproduction will be low, and selection will favor those individuals that can produce the maximum number of offspring. Selec- tion here favors individuals with the highest reproductive rates; such populations are termed r-selected. Examples of organisms displaying r-selected life history adaptations include dandelions, aphids, mice, and cockroaches (figure 24.21). Most natural populations show life history adaptations that exist along a continuum ranging from completely r- selected traits to completely K-selected traits. Although these tendencies hold true as generalities, few populations are purely r- or K-selected and show all of the traits listed in table 24.2. These attributes should be treated as general- ities, with the recognition that many exceptions do exist. Some life history adaptations favor near-exponential growth, others the more competitive logistic growth. Most natural populations exhibit a combination of the two. 510 Part VII Ecology and Behavior Table 24.2 r-Selected and K-Selected Life History Adaptations r-Selected K-Selected Adaptation Populations Populations Age at first Early Late reproduction Life span Short Long Maturation time Short Long Mortality rate Often high Usually low Number of offspring Many Few produced per reproductive episode Number of Usually one Often several reproductions per lifetime Parental care None Often extensive Size of offspring Small Large or eggs Source: Data from E. R. Pianka, Evolutionary Ecology, 4th edition, 1987, Harper & Row, New York. FIGURE 24.21 The consequences of exponential growth. All organisms have the potential to produce populations larger than those that actually occur in nature. The German cockroach (Blatella germanica), a major household pest, produces 80 young every six months. If every cockroach that hatched survived for three generations, kitchens might look like this theoretical culinary nightmare concocted by the Smithsonian Museum of Natural History. The Advent of Exponential Growth Humans exhibit many K-selected life history traits, in- cluding small brood size, late reproduction, and a high degree of parental care. These life history traits evolved during the early history of hominids, when the limited resources available from the environment controlled pop- ulation size. Throughout most of human history, our populations have been regulated by food availability, dis- ease, and predators. Although unusual disturbances, in- cluding floods, plagues, and droughts no doubt affected the pattern of human population growth, the overall size of the human population grew only slowly during our early history. Two thousand years ago, perhaps 130 mil- lion people populated the earth. It took a thousand years for that number to double, and it was 1650 before it had doubled again, to about 500 million. For over 16 cen- turies, the human population was characterized by very slow growth. In this respect, human populations resem- bled many other species with predominantly K-selected life history adaptations. Starting in the early 1700s, changes in technology have given humans more control over their food supply, en- abled them to develop superior weapons to ward off predators, and led to the development of cures for many diseases. At the same time, improvements in shelter and storage capabilities have made humans less vulnerable to climatic uncertainties. These changes allowed humans to expand the carrying capacity of the habitats in which they lived, and thus to escape the confines of logistic growth and reenter the exponential phase of the sigmoidal growth curve. Responding to the lack of environmental constraints, the human population has grown explosively over the last 300 years. While the birthrate has remained unchanged at about 30 per 1000 per year over this period, the death rate has fallen dramatically, from 20 per 1000 per year to its present level of 13 per 1000 per year. The difference be- tween birth and death rates meant that the population grew as much as 2% per year, although the rate has now declined to 1.4% per year. A 1.4% annual growth rate may not seem large, but it has produced a current human population of 6 billion peo- ple (figure 24.22)! At this growth rate, 77 million people are added to the world population annually, and the human population will double in 39 years. As we will discuss in chapter 30, both the current human population level and the projected growth rate have potential consequences for our future that are extremely grave. Chapter 24 Population Ecology 511 24.5 The human population has grown explosively in the last three centuries. 4000 B.C. 2 1 3 4 5 6 3000 B.C. 2000 B.C. 1000 B.C. Year Industrial Revolution Significant advances in medicine through science and technology Bubonic plague "Black Death" Billions of people 0 1000 2000 FIGURE 24.22 History of human population size. Temporary increases in death rate, even severe ones like the Black Death of the 1400s, have little lasting impact. Explosive growth began with the Industrial Revolution in the 1700s, which produced a significant long-term lowering of the death rate. The current population is 6 billion, and at the current rate will double in 39 years. Population Pyramids While the human population as a whole continues to grow rapidly at the close of the twentieth century, this growth is not occurring uniformly over the planet. Some countries, like Mexico, are growing rapidly, their birthrate greatly ex- ceeding their death rate (figure 24.23). Other countries are growing much more slowly. The rate at which a population can be expected to grow in the future can be assessed graphically by means of a population pyramid—a bar graph displaying the numbers of people in each age cate- gory. Males are conventionally shown to the left of the ver- tical age axis, females to the right. A human population pyramid thus displays the age composition of a population by sex. In most human population pyramids, the number of older females is disproportionately large compared to the number of older males, because females in most regions have a longer life expectancy than males. Viewing such a pyramid, one can predict demographic trends in births and deaths. In general, rectangular “pyramids” are characteristic of countries whose popula- tions are stable, their numbers neither growing nor shrinking. A triangular pyramid is characteristic of a country that will exhibit rapid future growth, as most of its population has not yet entered the child-bearing years. Inverted triangles are characteristic of populations that are shrinking. Examples of population pyramids for the United States and Kenya in 1990 are shown in figure 24.24. In the nearly rectangular population pyramid for the United States, the cohort (group of individuals) 55 to 59 years old represents people born during the Depression and is smaller in size than the cohorts in the preceding and following years. The cohorts 25 to 44 years old represent the “baby boom.” The rectangular shape of the population pyramid indicates that the population of the United States is not expanding rapidly. The very triangular pyramid of Kenya, by contrast, predicts explosive future growth. The population of Kenya is predicted to double in less than 20 years. 512 Part VII Ecology and Behavior 1895– 1899 1920– 1924 1945– 1949 Time Death rate Me xico Number per 1000 population 0 10 20 30 40 50 Birthrate 1985– 1990 1970– 1975 FIGURE 24.23 Why the population of Mexico is growing. The death rate (red line) in Mexico fell steadily throughout the last century, while the birthrate (blue line) remained fairly steady until 1970. The difference between birth and death rates has fueled a high growth rate. Efforts begun in 1970 to reduce the birthrate have been quite successful, although the growth rate remains rapid. 75 + 70–74 65–69 60–64 55–59 50–54 45–49 40–44 35–39 30–34 25–29 20–24 15–19 10–14 5–9 0–4 Percent of population Age Kenya 024246810 6 8 10 United States 02424 Male Female FIGURE 24.24 Population pyramids from 1990. Population pyramids are graphed according to a population’s age distribution. Kenya’s pyramid has a broad base because of the great number of individuals below child-bearing age. When all of the young people begin to bear children, the population will experience rapid growth. The U.S. pyramid demonstrates a larger number of individuals in the “baby boom” cohort—the pyramid bulges because of an increase in births between 1945 and 1964. An Uncertain Future The earth’s rapidly growing human population constitutes perhaps the greatest challenge to the future of the bio- sphere, the world’s interacting community of living things. Humanity is adding 77 million people a year to the earth's population—a million every five days, 150 every minute! In more rapidly growing countries, the resulting population increase is staggering (table 24.3). India, for example, had a population of 853 million in 1996; by 2020 its population will exceed 1.4 billion! A key element in the world’s population growth is its uneven distribution among countries. Of the billion people added to the world’s population in the 1990s, 90% live in developing countries (figure 24.25). This is leading to a major reduction in the fraction of the world’s population that lives in industrialized countries. In 1950, fully one- third of the world’s population lived in industrialized coun- tries; by 1996 that proportion had fallen to one-quarter; in 2020 the proportion will have fallen to one-sixth. Thus the world’s population growth will be centered in the parts of the world least equipped to deal with the pressures of rapid growth. Rapid population growth in developing countries has the harsh consequence of increasing the gap between rich and poor. Today 23% of the world’s population lives in the industrialized world with a per capita income of $17,900, while 77% of the world’s population lives in de- veloping countries with a per capita income of only $810. The disproportionate wealth of the industrialized quarter of the world’s population is evidenced by the fact that 85% of the world’s capital wealth is in the industrial world, only 15% in developing countries. Eighty percent of all the energy used today is consumed by the industrial world, only 20% by developing countries. Perhaps most worrisome for the future, fully 94% of all scientists and engineers reside in the industrialized world, only 6% in developing countries. Thus the problems created by the future’s explosive population growth will be faced by countries with little of the world’s scientific or technolog- ical expertise. No one knows whether the world can sustain today’s population of 6 billion people, much less the far greater populations expected in the future. As chapter 30 out- lines, the world ecosystem is already under considerable stress. We cannot reasonably expect to continue to ex- pand its carrying capacity indefinitely, and indeed we al- ready seem to be stretching the limits. It seems unavoid- able that to restrain the world’s future population growth, birth and death rates must be equalized. If we are to avoid catastrophic increases in the death rate, the birthrates must fall dramatically. Faced with this grim di- chotomy, significant efforts are underway worldwide to lower birthrates. The human population has been growing rapidly for 300 years, since technological innovations dramatically reduced the death rate. Chapter 24 Population Ecology 513 Table 24.3 A Comparison of 1996 Population Data in Developed and Developing Countries United States Brazil Ethiopia (highly developed )(moderately developed )(poorly developed ) Fertility rate 2.0 2.8 6.8 Doubling time at current rate (yr) 114 41 23 Infant mortality rate (per 1000 births) 7.5 58 120 Life expectancy at birth (yrs) 76 66 50 Per capita GNP (U.S. $; 1994) $25,860 $3,370 $130 1 2 3 Time W orld population in billions 19501900 1990 2000 Developing countries World total 2050 2100 4 5 6 7 8 9 10 11 0 Developed countries FIGURE 24.25 Most of the worldwide increase in population since 1950 has occurred in developing countries. The age structures of developing countries indicate that this trend will increase in the near future. The stabilizing of the world’s population at about 10 billion (shown here) is an optimistic World Bank/United Nations prediction that assumes significant worldwide reductions in growth rate. If the world’s population continues to increase at its 1996 rate, there will be over 30 billion humans by 2100! 514 Part VII Ecology and Behavior Chapter 24 Summary Questions Media Resources 24.1 Populations are individuals of the same species that live together. ? Populations are the same species in one place; communities are populations of different species that live together in a particular place. A community and the nonliving components of its environment combine to form an ecosystem. ? Populations may be dispersed in a clumped, uniform, or random manner. 1. What are the three types of dispersion in a population? Which type is most frequently seen in nature? Why? 2. What are some causes of clumped distributions? ? The growth rate of a population depends on its age structure, and to a lesser degree, sex ratio. ? Survivorship curves describe the characteristics of mortality in different kinds of populations. 3. What is survivorship? Describe the three types of survivorship curves and give examples of each. 4. What is demography? How does a life table work? 24.2 Population dynamics depend critically upon age distribution. ? Organisms balance investment in current reproduction with investment in growth and future reproduction. 5. Why do some birds lay fewer than the optimal number of eggs as predicted by David Lack? 24.3 Life histories often reflect trade-offs between reproduction and survival. ? Population size will change if birth and death rates differ, or if there is net migration into or out of the population. The intrinsic rate of increase of a population is defined as its biotic potential. ? Many populations exhibit a sigmoid growth curve, with a relatively slow start in growth, a rapid increase, and then a leveling off when the carrying capacity of the environment is reached. ? Large broods and rapid rates of population growth characterize r-strategists. K-strategists are limited in population size by the carrying capacity of their environments; they tend to have fewer offspring and slower rates of population growth. ? Density-independent factors have the same impact on a population no matter what its density. 6. Define the biotic potential of a population. What is the definition for the actual rate of population increase? What other two factors affect it? 7. What is an exponential capacity for growth? When does this type of growth naturally occur? Give an example. 8. What is carrying capacity? Is this a static or dynamic measure? Why? 9. What is the difference between r- and K-selected populations? 24.4 Population growth is limited by the environment. ? Exponential growth of the world’s human population is placing severe strains on the global environment. 10. How do population pyramids predict whether a population is likely to grow or shrink? 24.5 The human population has grown explosively in the last three centuries. www.mhhe.com/raven6e www.biocourse.com ? Introduction to Populations ? Population Characteristics ? On Science Article: Snakes in Ireland ? On Science Article: Deer Hunting ? On Science Article: Science for the Future ? Human Population ? Stages of Population Growth ? Population Growth ? Size Regulation ? Scientists on Science: Coral Reefs Threatened ? Student Research: Prairie Habitat Fragmentation ? On Science Article: Tropical Songbirds Lay Fewer Eggs ? On Science Article: Was Malthus Mistaken? 515 25 Community Ecology Concept Outline 25.1 Interactions among competing species shape ecological niches. The Realized Niche. Interspecific interactions often limit the portion of their niche that they can actually use. Gause and the Principle of Competitive Exclusion. No two species can occupy the same niche indefinitely without competition driving one to extinction. Resource Partitioning. Species that live together partition the available resources, reducing competition. Detecting Interspecific Competition. Experiments are often the best way to detect competition, but they have their limitations. 25.2 Predators and their prey coevolve. Predation and Prey Populations. Predators can limit the size of populations and sometimes even eliminate a species from a community. Plant Defenses against Herbivores. Plants use chemicals to defend themselves against animals trying to eat them. Animal Defenses against Predators. Animals defend themselves with camouflage, chemicals, and stings. Mimicry. Sometimes a species copies the appearance of another protected one. 25.3 Evolution sometimes fosters cooperation. Coevolution and Symbiosis. Organisms have evolved many adjustments and accommodations to living together. Commensalism. Some organisms use others, neither hurting or helping their benefactors. Mutualism. Often species interact in ways that benefit both. Parasitism. Sometimes one organism serves as the food supply of another much smaller one. Interactions among Ecological Processes. Multiple processes may occur simultaneously within a community. 25.4 Ecological succession may increase species richness. Succession. Communities change through time. The Role of Disturbance. Disturbances can disrupt successional change. In some cases, moderate amounts of disturbance increase species diversity. A ll the organisms that live together in a place are called a community. The myriad species that inhabit a tropi- cal rain forest are a community. Indeed, every inhabited place on earth supports its own particular array of organ- isms. Over time, the different species have made many complex adjustments to community living (figure 25.1), evolving together and forging relationships that give the community its character and stability. Both competition and cooperation have played key roles; in this chapter, we will look at these and other factors in community ecology. FIGURE 25.1 Communities involve interactions between disparate groups. This clownfish is one of the few species that can nestle safely among the stinging tentacles of the sea anemone—a classic example of a symbiotic relationship. Processes other than competition can also restrict the realized niche of a species. For example, a plant, the St. John’s-wort, was introduced and became widespread in open rangeland habitats in California until a specialized beetle was introduced to control it. Populations of the plant quickly decreased and it is now only found in shady sites where the beetle cannot thrive. In this case, the presence of a predator limits the realized niche of a plant. In some cases, the absence of another species leads to a smaller realized niche. For example, many North American plants depend on the American honeybee for pollination. The honeybee’s population is currently declining for a vari- ety of reasons. Conservationists are concerned that if the honeybee disappears from some habitats, the niche of these plant species will decrease or even disappear entirely. In this case, then, the absence—rather than the presence—of another species will be cause of a relatively small realized niche. A niche may be defined as the way in which an organism utilizes its environment. Interspecific interactions may cause a species’ realized niche to be smaller than its fundamental niche. If resources are limiting, two species normally cannot occupy the same niche indefinitely. 516 Part VII Ecology and Behavior The Realized Niche Each organism in an ecosystem confronts the challenge of survival in a different way. The niche an organism occupies is the sum total of all the ways it utilizes the resources of its environment. A niche may be described in terms of space utilization, food consumption, temperature range, appro- priate conditions for mating, requirements for moisture, and other factors. Niche is not synonymous with habitat, the place where an organism lives. Habitat is a place, niche a pattern of living. Sometimes species are not able to occupy their entire niche because of the presence or absence of other species. Species can interact with each other in a number of ways, and these interactions can either have positive or negative effects. One type of interaction is interspecific competi- tion, which occurs when two species attempt to utilize the same resource when there is not enough of the resource to satisfy both. Fighting over resources is referred to as inter- ference competition; consuming shared resources is called exploitative competition. The entire niche that a species is capable of using, based on its physiological requirements and resource needs, is called the fundamental niche. The actual niche the species occupies is called its realized niche. Because of interspecific interactions, the realized niche of a species may be considerably smaller than its fundamental niche. In a classic study, J. H. Connell of the University of California, Santa Barbara investigated competitive inter- actions between two species of barnacles that grow to- gether on rocks along the coast of Scotland. Of the two species Connell studied, Chthamalus stellatus lives in shal- lower water, where tidal action often exposed it to air, and Semibalanus balanoides (called Balanus balanoides prior to 1995) lives lower down, where it is rarely exposed to the atmosphere (figure 25.2). In the deeper zone, Semi- balanus could always outcompete Chthamalus by crowding it off the rocks, undercutting it, and replacing it even where it had begun to grow, an example of interference competition. When Connell removed Semibalanus from the area, however, Chthamalus was easily able to occupy the deeper zone, indicating that no physiological or other general obstacles prevented it from becoming established there. In contrast, Semibalanus could not survive in the shallow-water habitats where Chthamalus normally oc- curs; it evidently does not have the special adaptations that allow Chthamalus to occupy this zone. Thus, the fun- damental niche of the barnacle Chthamalus included both shallow and deeper zones, but its realized niche was much narrower because Chthamalus was outcompeted by Semibalanus in parts of its fundamental niche. By con- trast, the realized and fundamental niches of Semibalanus appear to be identical. 25.1 Interactions among competing species shape ecological niches. Fundamental niches Realized niches Chthamalus Semibalanus FIGURE 25.2 Competition among two species of barnacles limits niche use. Chthamalus can live in both deep and shallow zones (its fundamental niche), but Semibalanus forces Chthamalus out of the part of its fundamental niche that overlaps the realized niche of Semibalanus. Gause and the Principle of Competitive Exclusion In classic experiments carried out in 1934 and 1935, Russ- ian ecologist G. F. Gause studied competition among three species of Paramecium, a tiny protist. All three species grew well alone in culture tubes, preying on bacteria and yeasts that fed on oatmeal suspended in the culture fluid (figure 25.3a). However, when Gause grew P. aurelia together with P. caudatum in the same culture tube, the numbers of P. caudatum always declined to extinction, leaving P. aurelia the only survivor (figure 25.3b). Why? Gause found P. au- relia was able to grow six times faster than its competitor P. caudatum because it was able to better utilize the limited available resources, an example of exploitative competition. From experiments such as this, Gause formulated what is now called the principle of competitive exclusion. This principle states that if two species are competing for a limited resource, the species that uses the resource more ef- ficiently will eventually eliminate the other locally—no two species with the same niche can coexist when resources are limiting. Niche Overlap In a revealing experiment, Gause challenged Paramecium caudatum—the defeated species in his earlier experiments— with a third species, P. bursaria. Because he expected these two species to also compete for the limited bacterial food supply, Gause thought one would win out, as had happened in his previous experiments. But that’s not what happened. Instead, both species survived in the culture tubes; the paramecia found a way to divide the food resources. How did they do it? In the upper part of the culture tubes, where the oxygen concentration and bacterial density were high, P. caudatum dominated because it was better able to feed on bacteria. However, in the lower part of the tubes, the lower oxygen concentration favored the growth of a different po- tential food, yeast, and P. bursaria was better able to eat this food. The fundamental niche of each species was the whole culture tube, but the realized niche of each species was only a portion of the tube. Because the niches of the two species did not overlap too much, both species were able to sur- vive. However, competition did have a negative effect on the participants (figure 25.3c). When grown without a com- petitor, both species reached densities three times greater than when they were grown with a competitor. Competitive Exclusion Gause’s principle of competitive exclusion can be restated to say that no two species can occupy the same niche indefinitely when resources are limiting. Certainly species can and do co- exist while competing for some of the same resources. Nev- ertheless, Gause’s theory predicts that when two species coexist on a long-term basis, either resources must not be limited or their niches will always differ in one or more fea- tures; otherwise, one species will outcompete the other and the extinction of the second species will inevitably result, a process referred to as competitive exclusion. If resources are limiting, no two species can occupy the same niche indefinitely without competition driving one to extinction. Chapter 25 Community Ecology 517 ? ? ? ? ? ? ? ? ? ? ? ? ? ??? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? 200 150 100 50 0 00 0 4 8 12 16 20 24 20161284 Days Days(b) (c) P. caudatum P. aurelia P. caudatum P. bursaria Population density (measured by volume) 50 75 25 FIGURE 25.3 Competitive exclusion among three species of Paramecium. In the microscopic world, Paramecium is a ferocious predator. Paramecia eat by ingesting their prey; their cell membranes surround bacterial or yeast cells, forming a food vacuole containing the prey cell. (a) In his experiments, Gause found that three species of Paramecium grew well alone in culture tubes. (b) But Paramecium caudatum would decline to extinction when grown with P. aurelia because they shared the same realized niche, and P. aurelia outcompeted P. caudatum for food resources. (c) However, P. caudatum and P. bursaria were able to coexist because the two have different realized niches and thus avoided competition. 0 50 100 150 200 50 100 150 200 50 100 150 200 Days Population density (measured by volume) 40 812162024 40 812162024 40 812162024 0 Days 0 Days P. aurelia P. caudatum P. bursaria ? ? ? ? ? ? ? ? ? ?? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ?? ? ?? ? ? (a) Resource Partitioning Gause’s exclusion principle has a very important conse- quence: persistent competition between two species is rare in natural communities. Either one species drives the other to extinction, or natural selection reduces the competition between them. When the late Princeton ecologist Robert MacArthur studied five species of warblers, small insect- eating forest songbirds, he found that they all appeared to be competing for the same resources. However, when he studied them more carefully, he found that each species ac- tually fed in a different part of spruce trees and so ate dif- ferent subsets of insects. One species fed on insects near the tips of branches, a second within the dense foliage, a third on the lower branches, a fourth high on the trees and a fifth at the very apex of the trees. Thus, each species of warbler had evolved so as to utilize a different portion of the spruce tree resource. They subdivided the niche, parti- tioning the available resource so as to avoid direct competi- tion with one another. Resource partitioning is often seen in similar species that occupy the same geographical area. Such sympatric species often avoid competition by living in different por- tions of the habitat or by utilizing different food or other resources (figure 25.4). This pattern of resource partition- ing is thought to result from the process of natural selec- tion causing initially similar species to diverge in resource use in order to reduce competitive pressures. Evidence for the role of evolution comes from compari- son of species whose ranges are only partially overlapping. Where the two species co-occur, they tend to exhibit greater differences in morphology (the form and structure of an organism) and resource use than do their allopatric populations. Called character displacement, the differ- ences evident between sympatric species are thought to have been favored by natural selection as a mechanism to facilitate habitat partitioning and thus reduce competition. Thus, the two Darwin’s finches in figure 25.5 have bills of similar size where the finches are allopatric, each living on an island where the other does not occur. On islands where they are sympatric, the two species have evolved beaks of different sizes, one adapted to larger seeds, the other to smaller ones. Sympatric species partition available resources, reducing competition between them. 518 Part VII Ecology and Behavior 50 25 0 50 25 0 50 25 0 7 9 11 13 15 Finch beak depth (mm) Los Hermanos Islets Daphne Major Island San Cristobal and Santa Maria Islands G. fuliginosa Allopatric G. fortis Allopatric G. fuliginosa and G. fortis Sympatric H11541 Individuals in each size class (%) FIGURE 25.5 Character displacement in Darwin’s finches. These two species of finches (genus Geospiza) have bills of similar size when allopatric, but different size when sympatric. FIGURE 25.4 Resource partitioning among sympatric lizard species. Species of Anolis lizards on Caribbean islands partition their tree habitats in a variety of ways. Some species of anoles occupy the canopy of trees (a), others use twigs on the periphery (b), and still others are found at the base of the trunk (c). In addition, some use grassy areas in the open (d). When two species occupy the same part of the tree, they either utilize different-sized insects as food or partition the thermal microhabitat; for example, one might only be found in the shade, whereas the other would only bask in the sun. Most interestingly, the same pattern of resource partitioning has evolved independently on different Caribbean islands. (c) (d) (a) (b) Detecting Interspecific Competition It is not simple to determine when two species are compet- ing. The fact that two species use the same resources need not imply competition if that resource is not in limited sup- ply. If the population sizes of two species are negatively correlated, such that where one species has a large popula- tion, the other species has a small population and vice versa, the two species need not be competing for the same limiting resource. Instead, the two species might be inde- pendently responding to the same feature of the environ- ment—perhaps one species thrives best in warm conditions and the other in cool conditions. Experimental Studies of Competition Some of the best evidence for the existence of competi- tion comes from experimental field studies. By setting up experiments in which two species either occur alone or together, scientists can determine whether the presence of one species has a negative effect on a population of a second species. For example, a variety of seed-eating ro- dents occur in the Chihuahuan Desert of the southwest- ern part of North America. In 1988, researchers set up a series of 50 meter H11003 50 meter enclosures to investigate the effect of kangaroo rats on other, smaller seed-eating rodents. Kangaroo rats were removed from half of the enclosures, but not from the other enclosures. The walls of all of the enclosures had holes in them that allowed ro- dents to come and go, but in the kangaroo rat removal plots, the holes were too small to allow the kangaroo rats to enter. Over the course of the next three years, the re- searchers monitored the number of the other, smaller seed-eating rodents present in the plots. As figure 25.6 il- lustrates, the number of other rodents was substantially higher in the absence of kangaroo rats, indicating that kangaroo rats compete with the other rodents and limit their population sizes. A great number of similar experiments have indicated that interspecific competition occurs between many species of plants and animals. Effects of competition can be seen in aspects of population biology other than population size, such as behavior and individual growth rates. For example, two species of Anolis lizards occur on the island of St. Maarten. When one of the species, A. gingivinus, is placed in 12 m H11003 12 m enclosures without the other species, indi- vidual lizards grow faster and perch lower than lizards of the same species do when placed in enclosures in which A. pogus is also present. Caution Is Necessary Although experimental studies can be a powerful means of understanding the interactions that occur between coexist- ing species, they have their limitations. First, care is necessary in interpreting the results of field experiments. Negative effects of one species on another do not automatically indicate the existence of competition. For example, many similar-sized fish have a negative effect on each other, but it results not from competition, but from the fact that adults of each species will prey on juveniles of the other species. In addition, the presence of one species may attract predators, which then also prey on the second species. In this case, the second species may have a lower population size in the presence of the first species due to the presence of predators, even if they are not competing at all. Thus, experimental studies are most effective when they are combined with detailed examination of the ecolog- ical mechanism causing the negative effect of one species on another species. In addition, experimental studies are not always feasible. For example, the coyote has increased its population in the United States in recent years simultaneously with the de- cline of the grey wolf. Is this trend an indication that the species compete? Because of the size of the animals and the large geographic areas occupied by each individual, manip- ulative experiments involving fenced areas with only one or both species—with each experimental treatment replicated several times for statistical analysis—are not practical. Sim- ilarly, studies of slow-growing trees might require many centuries to detect competition between adult trees. In such cases, detailed studies of the ecological requirements of the species are our best bet to understanding interspe- cific interactions. Experimental studies can provide strong tests of the hypothesis that interspecific competition occurs, but such studies have limitations. Detailed ecological studies are important regardless of whether experiments are conducted. Chapter 25 Community Ecology 519 10 15 5 0 199019891988 ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? Kangaroo rats removed Kangaroo rats present Numbe r of captu r es of othe r r o d ents FIGURE 25.6 Detecting interspecific competition. This experiment tests the effect of removal of kangaroo rats on the population size of other rodents. Immediately after kangaroo rats were removed, the number of rodents increased relative to the enclosures that still had kangaroo rats. Notice that population sizes (as estimated by number of captures) increased and decreased in synchrony in the two treatments, probably reflecting changes in the weather. Predation is the consuming of one organism by another. In this sense, predation includes everything from a leopard capturing and eating an antelope, to a deer grazing on spring grass. When experimental populations are set up under simple laboratory conditions, the predator often ex- terminates its prey and then becomes extinct itself, having nothing left to eat (figure 25.7). However, if refuges are provided for the prey, its population will drop to low levels but not to extinction. Low prey population levels will then provide inadequate food for the predators, causing the predator population to decrease. When this occurs, the prey population can recover. Predation and Prey Populations In nature, predators can often have large effects on prey populations. Some of the most dramatic examples involve situations in which humans have either added or elimi- nated predators from an area. For example, the elimina- tion of large carnivores from much of the eastern United States has led to population explosions of white-tailed deer, which strip the habitat of all edible plant life. Simi- larly, when sea otters were hunted to near extinction on the western coast of the United States, sea urchin popula- tions exploded. Conversely, the introduction of rats, dogs, and cats to many islands around the world has led to the decimation of native faunas. Populations of Galápagos tortoises on several islands are endangered, for example, by intro- duced rats, dogs, and cats, which eat eggs and young tor- toises. Similarly, several species of birds and reptiles have been eradicated by rat predation from New Zealand and now only occur on a few offshore islands that the rats have not reached. In addition, on Stephens Island, near New Zealand, every individual of the now extinct Stephen Island wren was killed by a single lighthouse keeper’s cat! A classic example of the role predation can play in a community involves the introduction of prickly pear cac- tus to Australia in the nineteenth century. In the absence of predators, the cactus spread rapidly, by 1925 occupy- ing 12 million hectares of rangeland in an impenetrable morass of spines that made cattle ranching difficult. To control the cactus, a predator from its natural habitat in Argentina, the moth Cactoblastis cactorum, was introduced beginning in 1926. By 1940, cactus populations had been decimated, and it now generally occurs in small populations. Predation and Evolution Predation provides strong selective pressures on prey popu- lations. Any feature that would decrease the probability of capture should be strongly favored. In the next three pages, we discuss a number of defense mechanisms in plants and animals. In turn, the evolution of such features will cause natural selection to favor counteradaptations in predator populations. In this way, a coevolutionary arms race may ensue in which predators and prey are constantly evolving better defenses and better means of circumventing these defenses. One example comes from the fossil record of molluscs and gastropods and their predators. During the Mesozoic period (approximately 65 to 225 million years ago), new forms of predatory fish and crustaceans evolved that were able to crush or tear open shells. As a result, a variety of de- fensive measures evolved in molluscs and gastropods, in- cluding thicker shells, spines, and shells too smooth for predators to be able to grasp. In turn, these adaptations may have pressured predators to evolve ever more effective predatory adaptations and tactics. Predation can have substantial effects on prey populations. As a result prey species often evolve defensive adaptations. 520 Part VII Ecology and Behavior 25.2 Predators and their prey coevolve. 0 1 2 3 4 5 40 80 120 Number of individuals Time (days) Paramecium Didinium FIGURE 25.7 Predator-prey in the microscopic world. When the predatory Didinium is added to a Paramecium population, the numbers of Didinium initially rise, while the numbers of Paramecium steadily fall. When the Paramecium population is depleted, however, the Didinium individuals also die. Plant Defenses against Herbivores Plants have evolved many mecha- nisms to defend themselves from her- bivores. The most obvious are mor- phological defenses: thorns, spines, and prickles play an important role in discouraging browsers, and plant hairs, especially those that have a glandular, sticky tip, deter insect her- bivores. Some plants, such as grasses, deposit silica in their leaves, both strengthening and protecting them- selves. If enough silica is present in their cells, these plants are simply too tough to eat. Chemical Defenses Significant as these morphological adaptations are, the chemical defenses that occur so widely in plants are even more crucial. Best known and perhaps most important in the defenses of plants against herbivores are secondary chemical compounds. These are distinguished from pri- mary compounds, which are regular components of the major metabolic pathways, such as respiration. Many plants, and apparently many algae as well, contain very structurally diverse secondary compounds that are either toxic to most herbivores or disturb their metabolism greatly, preventing, for example, the normal development of larval insects. Consequently, most herbivores tend to avoid the plants that possess these compounds. The mustard family (Brassicaceae) is characterized by a group of chemicals known as mustard oils. These are the substances that give the pungent aromas and tastes to such plants as mustard, cabbage, watercress, radish, and horseradish. The same tastes we enjoy signal the presence of chemicals that are toxic to many groups of insects. Sim- ilarly, plants of the milkweed family (Asclepiadaceae) and the related dogbane family (Apocynaceae) produce a milky sap that deters herbivores from eating them. In ad- dition, these plants usually contain cardiac glycosides, molecules named for their drastic effect on heart function in vertebrates. The Evolutionary Response of Herbivores Certain groups of herbivores are associated with each fam- ily or group of plants protected by a particular kind of sec- ondary compound. These herbivores are able to feed on these plants without harm, often as their exclusive food source. For example, cabbage butterfly caterpillars (sub- family Pierinae) feed almost exclusively on plants of the mustard and caper families, as well as on a few other small families of plants that also contain mustard oils (figure 25.8). Similarly, caterpillars of monarch butterflies and their relatives (subfamily Danainae) feed on plants of the milkweed and dogbane families. How do these animals manage to avoid the chemical defenses of the plants, and what are the evolutionary precursors and ecological conse- quences of such patterns of specialization? We can offer a potential explanation for the evolution of these particular patterns. Once the ability to manufac- ture mustard oils evolved in the ancestors of the caper and mustard families, the plants were protected for a time against most or all herbivores that were feeding on other plants in their area. At some point, certain groups of in- sects—for example, the cabbage butterflies—evolved the ability to break down mustard oils and thus feed on these plants without harming themselves. Having developed this ability, the butterflies were able to use a new resource without competing with other herbivores for it. Often, in groups of insects such as cabbage butterflies, sense organs have evolved that are able to detect the secondary com- pounds that their food plants produce. Clearly, the rela- tionship that has formed between cabbage butterflies and the plants of the mustard and caper families is an example of coevolution. The members of many groups of plants are protected from most herbivores by their secondary compounds. Once the members of a particular herbivore group evolve the ability to feed on them, these herbivores gain access to a new resource, which they can exploit without competition from other herbivores. Chapter 25 Community Ecology 521 (a) (b) FIGURE 25.8 Insect herbivores are well suited to their hosts. (a) The green caterpillars of the cabbage butterfly, Pieris rapae, are camouflaged on the leaves of cabbage and other plants on which they feed. Although mustard oils protect these plants against most herbivores, the cabbage butterfly caterpillars are able to break down the mustard oil compounds. (b) An adult cabbage butterfly. Animal Defenses against Predators Some animals that feed on plants rich in secondary com- pounds receive an extra benefit. When the caterpillars of monarch butterflies feed on plants of the milkweed family, they do not break down the cardiac glycosides that protect these plants from herbivores. Instead, the caterpillars con- centrate and store the cardiac glycosides in fat bodies; they then pass them through the chrysalis stage to the adult and even to the eggs of the next generation. The incorporation of cardiac glycosides thus protects all stages of the monarch life cycle from predators. A bird that eats a monarch but- terfly quickly regurgitates it (figure 25.9) and in the future avoids the conspicuous orange-and-black pattern that char- acterizes the adult monarch. Some birds, however, appear to have acquired the ability to tolerate the protective chem- icals. These birds eat the monarchs. Defensive Coloration Many insects that feed on milkweed plants are brightly col- ored; they advertise their poisonous nature using an eco- logical strategy known as warning coloration, or apose- matic coloration. Showy coloration is characteristic of animals that use poisons and stings to repel predators, while organisms that lack specific chemical defenses are sel- dom brightly colored. In fact, many have cryptic col- oration—color that blends with the surroundings and thus hides the individual from predators (figure 25.10). Camou- flaged animals usually do not live together in groups be- cause a predator that discovers one individual gains a valu- able clue to the presence of others. Chemical Defenses Animals also manufacture and use a startling array of sub- stances to perform a variety of defensive functions. Bees, wasps, predatory bugs, scorpions, spiders, and many other arthropods use chemicals to defend themselves and to kill their prey. In addition, various chemical defenses have evolved among marine animals and the vertebrates, includ- ing venomous snakes, lizards, fishes, and some birds. The poison-dart frogs of the family Dendrobatidae produce toxic alkaloids in the mucus that covers their brightly col- ored skin (figure 25.11). Some of these toxins are so power- ful that a few micrograms will kill a person if injected into the bloodstream. More than 200 different alkaloids have been isolated from these frogs, and some are playing im- portant roles in neuromuscular research. There is an inten- sive investigation of marine animals, algae, and flowering plants for new drugs to fight cancer and other diseases, or as sources of antibiotics. Animals defend themselves against predators with warning coloration, camouflage, and chemical defenses such as poisons and stings. 522 Part VII Ecology and Behavior FIGURE 25.9 A blue jay learns that monarch butterflies taste bad. (a) This cage-reared jay had never seen a monarch butterfly before it tried eating one. (b) The same jay regurgitated the butterfly a few minutes later. This bird will probably avoid trying to capture all orange-and-black insects in the future. (a) (b) FIGURE 25.10 Cryptic coloration. An inchworm caterpillar (Necophora quernaria) (hanging from the upper twig) closely resembles a twig. FIGURE 25.11 Vertebrate chemical defenses. Frogs of the family Dendrobatidae, abundant in the forests of Latin America, are extremely poisonous to vertebrates. Dendrobatids advertise their toxicity with aposematic coloration, as shown here. Mimicry During the course of their evolution, many species have come to resemble distasteful ones that exhibit aposematic coloration. The mimic gains an advantage by looking like the distasteful model. Two types of mimicry have been identified: Batesian and Müllerian mimicry. Batesian Mimicry Batesian mimicry is named for Henry Bates, the British naturalist who first brought this type of mimicry to gen- eral attention in 1857. In his journeys to the Amazon re- gion of South America, Bates discovered many instances of palatable insects that resembled brightly colored, dis- tasteful species. He reasoned that the mimics would be avoided by predators, who would be fooled by the dis- guise into thinking the mimic actually is the distasteful model. Many of the best-known examples of Batesian mimicry occur among butterflies and moths. Obviously, predators in systems of this kind must use visual cues to hunt for their prey; otherwise, similar color patterns would not matter to potential predators. There is also increasing evidence indi- cating that Batesian mimicry can also involve nonvisual cues, such as olfaction, although such examples are less ob- vious to humans. The kinds of butterflies that provide the models in Bate- sian mimicry are, not surprisingly, members of groups whose caterpillars feed on only one or a few closely related plant families. The plant families on which they feed are strongly protected by toxic chemicals. The model butter- flies incorporate the poisonous molecules from these plants into their bodies. The mimic butterflies, in contrast, belong to groups in which the feeding habits of the caterpillars are not so restricted. As caterpillars, these butterflies feed on a number of different plant families unprotected by toxic chemicals. One often-studied mimic among North American but- terflies is the viceroy, Limenitis archippus (figure 25.12a). This butterfly, which resembles the poisonous monarch, ranges from central Canada through much of the United States and into Mexico. The caterpillars feed on willows and cottonwoods, and neither caterpillars nor adults were thought to be distasteful to birds, although recent findings may dispute this. Interestingly, the Batesian mimicry seen in the adult viceroy butterfly does not extend to the cater- pillars: viceroy caterpillars are camouflaged on leaves, re- sembling bird droppings, while the monarch’s distasteful caterpillars are very conspicuous. Müllerian Mimicry Another kind of mimicry, Müllerian mimicry, was named for German biologist Fritz Müller, who first described it in 1878. In Müllerian mimicry, several unrelated but pro- tected animal species come to resemble one another (figure 25.12b). If animals that resemble one another are all poiso- nous or dangerous, they gain an advantage because a preda- tor will learn more quickly to avoid them. In some cases, predator populations even evolve an innate avoidance of species; such evolution may occur more quickly when mul- tiple dangerous prey look alike. In both Batesian and Müllerian mimicry, mimic and model must not only look alike but also act alike if preda- tors are to be deceived. For example, the members of sev- eral families of insects that closely resemble wasps behave surprisingly like the wasps they mimic, flying often and ac- tively from place to place. In Batesian mimicry, unprotected species resemble others that are distasteful. Both species exhibit aposematic coloration. In Müllerian mimicry, two or more unrelated but protected species resemble one another, thus achieving a kind of group defense. Chapter 25 Community Ecology 523 (a) Batesian mimicry: Monarch (Danaus) is poisonous; viceroy (Limenitis) is palatable mimic (b) Müllerian mimicry: two pairs of mimics; all are distasteful Heliconius erato Heliconius melpomene Danaus plexippus Limenitis archippus Heliconius sapho Heliconius cydno FIGURE 25.12 Mimicry. (a) Batesian mimicry. Monarch butterflies (Danaus plexippus) are protected from birds and other predators by the cardiac glycosides they incorporate from the milkweeds and dogbanes they feed on as larvae. Adult monarch butterflies advertise their poisonous nature with warning coloration. Viceroy butterflies (Limenitis archippus) are Batesian mimics of the poisonous monarch. (b) Pairs of Müllerian mimics. Heliconius erato and H. melpomene are sympatric, and H. sapho and H. cydno are sympatric. All of these butterflies are distasteful. They have evolved similar coloration patterns in sympatry to minimize predation; predators need only learn one pattern to avoid. Coevolution and Symbiosis The plants, animals, protists, fungi, and bacteria that live together in communities have changed and adjusted to one another continually over a period of millions of years. For example, many features of flowering plants have evolved in relation to the dispersal of the plant’s ga- metes by animals (figure 25.13). These animals, in turn, have evolved a number of special traits that enable them to obtain food or other resources efficiently from the plants they visit, often from their flowers. While doing so, the animals pick up pollen, which they may deposit on the next plant they visit, or seeds, which may be left else- where in the environment, sometimes a great distance from the parental plant. Such interactions, which involve the long-term, mutual evolutionary adjustment of the characteristics of the mem- bers of biological communities, are examples of coevolu- tion, a phenomenon we have already seen in predator-prey interactions. Symbiosis Is Widespread Another type of coevolution involves symbiotic relation- ships in which two or more kinds of organisms live to- gether in often elaborate and more-or-less permanent re- lationships. All symbiotic relationships carry the potential for coevolution between the organisms involved, and in many instances the results of this coevolution are fascinat- ing. Examples of symbiosis include lichens, which are asso- ciations of certain fungi with green algae or cyanobacte- ria. Lichens are discussed in more detail in chapter 36. Another important example are mycorrhizae, the associa- tion between fungi and the roots of most kinds of plants. The fungi expedite the plant’s absorption of certain nutri- ents, and the plants in turn provide the fungi with carbo- hydrates. Similarly, root nodules that occur in legumes and certain other kinds of plants contain bacteria that fix atmospheric nitrogen and make it available to their host plants. In the tropics, leafcutter ants are often so abundant that they can remove a quarter or more of the total leaf surface of the plants in a given area. They do not eat these leaves directly; rather, they take them to under- ground nests, where they chew them up and inoculate them with the spores of particular fungi. These fungi are cultivated by the ants and brought from one specially prepared bed to another, where they grow and repro- duce. In turn, the fungi constitute the primary food of the ants and their larvae. The relationship between leaf- cutter ants and these fungi is an excellent example of symbiosis. Kinds of Symbiosis The major kinds of symbiotic relationships include (1) commensalism, in which one species benefits while the other neither benefits nor is harmed; (2) mutualism, in which both participating species benefit; and (3) para- sitism, in which one species benefits but the other is harmed. Parasitism can also be viewed as a form of preda- tion, although the organism that is preyed upon does not necessarily die. Coevolution is a term that describes the long-term evolutionary adjustments of species to one another. In symbiosis two or more species interact closely, with at least one species benefitting. 524 Part VII Ecology and Behavior 25.3 Evolution sometimes fosters cooperation. FIGURE 25.13 Pollination by bat. Many flowers have coevolved with other species to facilitate pollen transfer. Insects are widely known as pollinators, but they’re not the only ones. Notice the cargo of pollen on the bat’s snout. Commensalism Commensalism is a symbiotic rela- tionship that benefits one species and neither hurts nor helps the other. In nature, individuals of one species are often physically attached to members of another. For example, epiphytes are plants that grow on the branches of other plants. In general, the host plant is unharmed, while the epiphyte that grows on it benefits. Similarly, various marine animals, such as barnacles, grow on other, often actively moving sea animals like whales and thus are carried pas- sively from place to place. These “passengers” presumably gain more protection from predation than they would if they were fixed in one place, and they also reach new sources of food. The increased water circulation that such animals receive as their host moves around may be of great importance, particularly if the pas- sengers are filter feeders. The ga- metes of the passenger are also more widely dispersed than would be the case otherwise. Examples of Commensalism The best-known examples of commensalism involve the re- lationships between certain small tropical fishes and sea anemones, marine animals that have stinging tentacles (see chapter 44). These fish have evolved the ability to live among the tentacles of sea anemones, even though these tentacles would quickly paralyze other fishes that touched them (figure 25.14). The anemone fishes feed on the detri- tus left from the meals of the host anemone, remaining un- injured under remarkable circumstances. On land, an analogous relationship exists between birds called oxpeckers and grazing animals such as cattle or rhi- noceros. The birds spend most of their time clinging to the animals, picking off parasites and other insects, carrying out their entire life cycles in close association with the host animals. When Is Commensalism Commensalism? In each of these instances, it is difficult to be certain whether the second partner receives a benefit or not; there is no clear-cut boundary between commensalism and mutualism. For instance, it may be advantageous to the sea anemone to have particles of food removed from its tentacles; it may then be better able to catch other prey. Similarly, while often thought of as commensalism, the association of grazing mammals and gleaning birds is actually an example of mutualism. The mammal benefits by having parasites and other insects removed from its body, but the birds also benefit by gaining a dependable source of food. On the other hand, commensalism can easily transform itself into parasitism. For example, oxpeckers are also known to pick not only parasites, but also scabs off their grazing hosts. Once the scab is picked, the birds drink the blood that flows from the wound. Occasionally, the cumu- lative effect of persistent attacks can greatly weaken the herbivore, particularly when conditions are not favorable, such as during droughts. Commensalism is the benign use of one organism by another. Chapter 25 Community Ecology 525 FIGURE 25.14 Commensalism in the sea. Clownfishes, such as this Amphiprion perideraion in Guam, often form symbiotic associations with sea anemones, gaining protection by remaining among their tentacles and gleaning scraps from their food. Different species of anemones secrete different chemical mediators; these attract particular species of fishes and may be toxic to the fish species that occur symbiotically with other species of anemones in the same habitat. There are 26 species of clownfishes, all found only in association with sea anemones; 10 species of anemones are involved in such associations, so that some of the anemone species are host to more than one species of clownfish. Mutualism Mutualism is a symbiotic relationship among organisms in which both species benefit. Examples of mutualism are of fundamental importance in determining the structure of bi- ological communities. Some of the most spectacular exam- ples of mutualism occur among flowering plants and their animal visitors, including insects, birds, and bats. As we will see in chapter 37, during the course of their evolution, the characteristics of flowers have evolved in large part in rela- tion to the characteristics of the animals that visit them for food and, in doing so, spread their pollen from individual to individual. At the same time, characteristics of the ani- mals have changed, increasing their specialization for ob- taining food or other substances from particular kinds of flowers. Another example of mutualism involves ants and aphids. Aphids, also called greenflies, are small insects that suck fluids from the phloem of living plants with their piercing mouthparts. They extract a certain amount of the sucrose and other nutrients from this fluid, but they excrete much of it in an altered form through their anus. Certain ants have taken advantage of this—in effect, domesticating the aphids. The ants carry the aphids to new plants, where they come into contact with new sources of food, and then con- sume as food the “honeydew” that the aphids excrete. Ants and Acacias A particularly striking example of mutualism involves ants and certain Latin American species of the plant genus Aca- cia. In these species, certain leaf parts, called stipules, are modified as paired, hollow thorns. The thorns are inhab- ited by stinging ants of the genus Pseudomyrmex, which do not nest anywhere else (figure 25.15). Like all thorns that occur on plants, the acacia horns serve to deter herbivores. At the tip of the leaflets of these acacias are unique, pro- tein-rich bodies called Beltian bodies, named after the nineteenth-century British naturalist Thomas Belt. Beltian bodies do not occur in species of Acacia that are not inhab- ited by ants, and their role is clear: they serve as a primary food for the ants. In addition, the plants secrete nectar from glands near the bases of their leaves. The ants con- sume this nectar as well, feeding it and the Beltian bodies to their larvae. Obviously, this association is beneficial to the ants, and one can readily see why they inhabit acacias of this group. The ants and their larvae are protected within the swollen thorns, and the trees provide a balanced diet, including the sugar-rich nectar and the protein-rich Beltian bodies. What, if anything, do the ants do for the plants? Whenever any herbivore lands on the branches or leaves of an acacia inhabited by ants, the ants, which continually patrol the acacia’s branches, immediately attack and devour the herbivore. The ants that live in the acacias also help their hosts to compete with other plants. The ants cut away any branches of other plants that touch the acacia in which they are living. They create, in effect, a tunnel of light through which the acacia can grow, even in the lush decid- uous forests of lowland Central America. In fact, when an ant colony is experimentally removed from a tree, the aca- cia is unable to compete successfully in this habitat. Finally, the ants bring organic material into their nests. The parts they do not consume, together with their excretions, pro- vide the acacias with an abundant source of nitrogen. As with commensalism, however, things are not always as they seem. Ant-acacia mutualisms also occur in Africa. In Kenya, several species of acacia ants occur, but only one species occurs on any tree. One species, Crematogaster ni- griceps, is competitively inferior to two of the other species. To prevent invasion by other ant species, C. nigriceps prunes the branches of the acacia, preventing it from com- ing into contact with branches of other trees, which would serve as a bridge for invaders. Although this behavior is beneficial to the ant, it is detrimental to the tree, as it de- stroys the tissue from which flowers are produced, essen- tially sterilizing the tree. In this case, what has initially evolved as a mutualistic interaction has instead become a parasitic one. Mutualism involves cooperation between species, to the mutual benefit of both. 526 Part VII Ecology and Behavior FIGURE 25.15 Mutualism: ants and acacias. Ants of the genus Pseudomyrmex live within the hollow thorns of certain species of acacia trees in Latin America. The nectaries at the bases of the leaves and the Beltian bodies at the ends of the leaflets provide food for the ants. The ants, in turn, supply the acacias with organic nutrients and protect the acacia from herbivores. Parasitism Parasitism may be regarded as a special form of symbiosis in which the predator, or parasite, is much smaller than the prey and remains closely associated with it. Parasitism is harmful to the prey organism and beneficial to the parasite. The concept of parasitism seems obvious, but individual in- stances are often surprisingly difficult to distinguish from predation and from other kinds of symbiosis. External Parasites Parasites that feed on the exterior surface of an organism are external parasites, or ectoparasites. Many instances of external parasitism are known (figure 25.16). Lice, which live on the bodies of vertebrates—mainly birds and mam- mals—are normally considered parasites. Mosquitoes are not considered parasites, even though they draw food from birds and mammals in a similar manner to lice, because their interaction with their host is so brief. Parasitoids are insects that lay eggs on living hosts. This behavior is common among wasps, whose larvae feed on the body of the unfortunate host, often killing it. Internal Parasites Vertebrates are parasitized internally by endoparasites, members of many different phyla of animals and protists. Invertebrates also have many kinds of parasites that live within their bodies. Bacteria and viruses are not usually considered parasites, even though they fit our definition precisely. Internal parasitism is generally marked by much more extreme specialization than external parasitism, as shown by the many protist and invertebrate parasites that infect humans. The more closely the life of the parasite is linked with that of its host, the more its morphology and behavior are likely to have been modified during the course of its evolution. The same is true of symbiotic relationships of all sorts. Conditions within the body of an organism are dif- ferent from those encountered outside and are apt to be much more constant. Consequently, the structure of an in- ternal parasite is often simplified, and unnecessary arma- ments and structures are lost as it evolves. Brood Parasitism Not all parasites consume the body of their host. In brood parasitism, birds like cowbirds and European cuckoos lay their eggs in the nests of other species. The host parents raise the brood parasite as if it were one of their own clutch, in many cases investing more in feeding the im- poster than in feeding their own offspring (figure 25.17). The brood parasite reduces the reproductive success of the foster parent hosts, so it is not surprising that in some cases natural selection has fostered the hosts’ ability to detect parasite eggs and reject them. What is more surprising is that in many other species, the ability to detect parasite eggs has not evolved. In parasitism, one organism serves as a host to another organism, usually to the host’s disadvantage. Chapter 25 Community Ecology 527 FIGURE 25.16 An external parasite. The flowering plant dodder (Cuscuta) is a parasite and has lost its chlorophyll and its leaves in the course of its evolution. Because it is heterotrophic, unable to manufacture its own food, dodder obtains its food from the host plants it grows on. FIGURE 25.17 Brood parasitism. This bird is feeding a cuckoo chick in its nest. The cuckoo chick is larger than the adult bird, but the bird does not recognize that the cuckoo is not its own offspring. Cuckoo mothers sneak into the nests of other birds and lay an egg, entrusting the care of their offspring to an unwitting bird of another species. Interactions among Ecological Processes We have seen the different ways in which species within a community can interact with each other. In nature, how- ever, more than one type of interaction usually occurs at the same time. In many cases, the outcome of one type of interaction is modified or even reversed when another type of interaction is also occurring. Predation Reduces Competition When resources are limiting, a superior competitor can eliminate other species from a community. However, predators can prevent or greatly reduce competitive ex- clusion by reducing the numbers of individuals of compet- ing species. A given predator may often feed on two, three, or more kinds of plants or animals in a given com- munity. The predator’s choice depends partly on the rela- tive abundance of the prey options. In other words, a predator may feed on species A when it is abundant and then switch to species B when A is rare. Similarly, a given prey species may be a primary source of food for increas- ing numbers of species as it becomes more abundant. In this way, superior competitors may be prevented from outcompeting other species. Such patterns are often characteristic of biological communities in marine intertidal habitats. For example, in preying selectively on bivalves, sea stars prevent bi- valves from monopolizing such habitats, opening up space for many other organisms (figure 25.18). When sea stars are removed from a habitat, species diversity falls precipitously, the seafloor community coming to be dom- inated by a few species of bivalves. Because predation tends to reduce competition in natural communities, it is usually a mistake to attempt to eliminate a major preda- tor such as wolves or mountain lions from a community. The result is to decrease rather than increase the biologi- cal diversity of the community, the opposite of what is intended. Parasitism May Counter Competition Parasites may effect sympatric species differently and thus influence the outcome of interspecific interactions. In a classic experiment, Thomas Park of the University of Chicago investigated interactions between two flour bee- tles, Tribolium castaneum and T. confusum with a parasite, Adelina. In the absence of the parasite, T. castaneum is dom- inant and T. confusum normally goes extinct. When the par- asite is present, however, the outcome is reversed and T. castaneum perishes. Similar effects of parasites in natural systems have been observed in many species. For example, in the Anolis lizards of St. Maarten mentioned previously, the competitively inferior species is resistant to malaria, whereas the other species is highly susceptible. Only in areas in which the malaria parasite occurs are the two species capable of coexisting. Indirect Effects In some cases, species may not directly interact, yet the presence of one species may effect a second species by way of interactions with a third species. Such effects are termed indirect effects. For example, in the Chihuahuan Desert, rodents and ants both eat seeds. Thus, one might expect them to compete with each other. However, when all ro- dents were completely removed from large enclosures (un- like the experiment discussed above, there were no holes in 528 Part VII Ecology and Behavior FIGURE 25.18 Predation reduces competition. (a) In a controlled experiment in a coastal ecosystem, an investigator removed a key predator (Pisaster). (b) In response, fiercely competitive mussels exploded in growth, effectively crowding out seven other indigenous species. (a) (b) the enclosure walls, so once removed, rodents couldn’t get back in), ant populations first increased, but then declined (figure 25.19). The initial increase was the expected result of removing a competitor; why did it reverse? The answer reveals the intricacies of natural ecosystems (figure 25.20). Rodents prefer large seeds, whereas ants prefer smaller seeds. Further, in this system plants with large seeds are competitively superior to plants with small seeds. Thus, the removal of rodents leads to an increase in the number of plants with large seeds, which reduces the number of small seeds available to ants, which thus leads to a decline in ant populations. Thus, the effect of rodents on ants is compli- cated: a direct negative effect of resource competition and an indirect, positive effect mediated by plant competition. Keystone Species Species that have particularly strong effects on the compo- sition of communities are termed keystone species. Predators, such as the starfish, can often serve as keystone species by preventing one species from outcompeting oth- ers, thus maintaining high levels of species richness in a community. There are, however, a wide variety of other types of key- stone species. Some species manipulate the environment in ways that create new habitats for other species. Beavers, for example, change running streams into small impound- ments, changing the flow of water and flooding areas (fig- ure 25.21). Similarly, alligators excavate deep holes at the bottoms of lakes. In times of drought, these holes are the only areas in which water remains, thus allowing aquatic species that otherwise would perish to persist until the drought ends and the lake refills. Many different processes are likely to be occurring simultaneously within communities. Only by understanding how these processes interact will we be able to understand how communities function. Chapter 25 Community Ecology 529 ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? 60 40 20 Sampling periods Numb e r of ant c olo n ie s Oct 74 May 75 Sep 75 May 76 Aug 76 Jul 77 Rodents removed Rodents not removed FIGURE 25.19 Change in ant population size after the removal of rodents. Ants initially increased in population size relative to ants in the enclosures from which rodents weren’t removed, but then these ant populations declined. Rodents Large seeds Small seeds Ants – – – + + FIGURE 25.20 Rodent-ant interactions. Rodents and ants both eat seeds, so the presence of rodents has a negative effect on ants and vice versa. However, the presence of rodents has a negative effect on large seeds. In turn, the number of plants with large seeds has a negative effect on plants that produce small seeds. Hence, the presence of rodents should increase the number of small seeds. In turn, the number of small seeds has a positive effect on ant populations. Thus, indirectly, the presence of rodents has a positive effect on ant population size. FIGURE 25.21 Example of a keystone species. Beavers, by constructing dams and transforming flowing streams into ponds, create new habitats for many plant and animal species. Even when the climate of an area remains stable year after year, ecosystems have a tendency to change from simple to complex in a process known as succession. This process is familiar to anyone who has seen a vacant lot or cleared woods slowly become occupied by an increasing number of plants, or a pond become dry land as it is filled with vegeta- tion encroaching from the sides. Succession If a wooded area is cleared and left alone, plants will slowly reclaim the area. Eventually, traces of the clearing will disappear and the area will again be woods. This kind of succession, which occurs in areas where an existing community has been disturbed, is called secondary succession. In contrast, primary succession occurs on bare, lifeless substrate, such as rocks, or in open water, where organisms gradually move into an area and change its nature. Primary succession occurs in lakes left behind after the retreat of glaciers, on volcanic islands that rise above the sea, and on land exposed by retreating glaciers (figure 25.22). Primary succession on glacial moraines provides an example (figure 25.23). On bare, mineral-poor soil, lichens grow first, forming small pockets of soil. Acidic secretions from the lichens help to break down the substrate and add to the ac- cumulation of soil. Mosses then colonize these pockets of soil, eventually building up enough nutrients in the soil for alder shrubs to take hold. Over a hundred years, the alders build up the soil nitrogen levels until spruce are able to thrive, eventually crowding out the alder and forming a dense spruce forest. In a similar example, an oligotrophic lake—one poor in nutrients—may gradually, by the accumulation of organic matter, become eutrophic—rich in nutrients. As this oc- curs, the composition of communities will change, first in- creasing in species richness and then declining. Primary succession in different habitats often eventually arrives at the same kinds of vegetation—vegetation charac- teristic of the region as a whole. This relationship led American ecologist F. E. Clements, at about the turn of the century, to propose the concept of a final climax commu- nity. With an increasing realization that (1) the climate keeps changing, (2) the process of succession is often very slow, and (3) the nature of a region’s vegetation is being de- termined to an increasing extent by human activities, ecol- ogists do not consider the concept of “climax community” to be as useful as they once did. Why Succession Happens Succession happens because species alter the habitat and the resources available in it in ways that favor other species. Three dynamic concepts are of critical importance in the process: tolerance, inhibition, and facilitation. 1. Tolerance. Early successional stages are character- ized by weedy r-selected species that are tolerant of the harsh, abiotic conditions in barren areas. 2. Facilitation. The weedy early successional stages in- troduce local changes in the habitat that favor other, less weedy species. Thus, the mosses in the Glacier Bay succession convert nitrogen to a form that allows alders to invade. The alders in turn lower soil pH as their fallen leaves decompose, and spruce and hem- lock, which require acidic soil, are able to invade. 3. Inhibition. Sometimes the changes in the habitat caused by one species, while favoring other species, inhibit the growth of the species that caused them. Alders, for example, do not grow as well in acidic soil as the spruce and hemlock that replace them. Over the course of succession, the number of species typically increases as the environment becomes more hos- pitable. In some cases, however, as ecosystems mature, more K-selected species replace r-selected ones, and supe- rior competitors force out other species, leading ultimately to a decline in species richness. Communities evolve to have greater total biomass and species richness in a process called succession. 530 Part VII Ecology and Behavior 25.4 Ecological succession may increase species richness. Pioneer mosses Invading alders Alder thickets Spruce forest Year 1 Year 100 Year 200 50 100 150 200 250 300 Nitrogen concentration (g/m 2 of surface) b c Nitrogen in mineral soil Nitrogen in forest floor FIGURE 25.22 Plant succession produces progressive changes in the soil. Initially, the glacial moraine at Glacier Bay, Alaska, portrayed in figure 25.23, had little soil nitrogen, but nitrogen-fixing alders led to a buildup of nitrogen in the soil, encouraging the subsequent growth of the conifer forest. Letters in the graph correspond to photographs in parts b and c of figure 25.23. The Role of Disturbance Disturbances often interrupt the succession of plant com- munities. Depending on the magnitude of the disturbance, communities may revert to earlier stages of succession or even, in extreme cases, begin at the earliest stages of pri- mary succession. Disturbances severe enough to disrupt succession include calamities such as forest fires, drought, and floods. Animals may also cause severe disruptions. Gypsy moths can devastate a forest by consuming its trees. Unregulated deer populations may grow explosively, the deer overgrazing and so destroying the forest they live in, in the same way too many cattle overgraze a pasture by eat- ing all available grass down to the ground. Intermediate Disturbance Hypothesis In some cases, disturbance may act to increase the species richness of an area. According to the intermediate disturbance hypothesis, communities experiencing moderate amounts of disturbance will have higher levels of species richness than communities experiencing either little or great amounts of disturbance. Two factors could account for this pattern. First, in communities in which moderate amounts of disturbance occur, patches of habitat will exist at different successional stages. Thus, within the area as a whole, species diversity will be greatest because the full range of species—those character- istic of all stages of succession—will be present. For example, a pattern of intermittent episodic disturbance that produces gaps in the rain forest (like when a tree falls) allows invasion of the gap by other species (figure 25.24). Eventually, the species inhabiting the gap will go through a successional se- quence, one tree replacing another, until a canopy tree species comes again to occupy the gap. But if there are lots of gaps of different ages in the forest, many different species will coexist, some in young gaps, others in older ones. Second, moderate levels of disturbance may prevent communities from reaching the final stages of succession, in which a few dominant competitors eliminate most of the other species. On the other hand, too much disturbance might leave the community continually in the earliest stages of succession, when species richness is relatively low. Ecologists are increasingly realizing that disturbance is the norm, rather than the exception, in many communities. As a result, the idea that communities inexorably move along a successional trajectory culminating in the develop- ment of a climax community is no longer widely accepted. Rather, predicting the state of a community in the future may be difficult because the unpredictable occurrence of disturbances will often counter successional changes. Un- derstanding the role that disturbances play in structuring communities is currently an important area of investigation in ecology. Succession is often disrupted by natural or human causes. In some cases, intermediate levels of disturbance may maximize the species richness of a community. Chapter 25 Community Ecology 531 (a) (b) (c) FIGURE 25.23 Primary succession at Alaska’s Glacier Bay. (a) The sides of the glacier have been retreating at a rate of some 8 meters a year, leaving behind exposed soil from which nitrogen and other minerals have been leached out. The first invaders of these exposed sites are pioneer moss species with nitrogen-fixing mutualistic microbes. Within 20 years, young alder shrubs take hold. (b) Rapidly fixing nitrogen, they soon form dense thickets. As soil nitrogen levels rise, (c) spruce crowd out the mature alders, forming a forest. FIGURE 25.24 Intermediate disturbance. A single fallen tree creates a small light gap in the tropical rain forest of Panama. Such gaps play a key role in maintaining the high species diversity of the rain forest. 532 Part VII Ecology and Behavior Chapter 25 Summary Questions Media Resources 25.1 Interactions among competing species shape ecological niches. ? Each species plays a specific role in its ecosystem; this role is called its niche. ? An organism’s fundamental niche is the total niche that the organism would occupy in the absence of competition. Its realized niche is the actual niche it occupies in nature. ? Two species cannot occupy the same niche for long if resources are limiting; one will outcompete the other, driving it to extinction. ? Species can coexist by partitioning resources to mini- mize competition. 1. What is the difference between interspecific competition and intraspecific competition? What is Gause’s principle of competitive exclusion? 2. Is the term niche synonymous with the term habitat? Why or why not? How does an organism’s fundamental niche differ from its realized niche? ? Plants are often protected from herbivores by chemicals they manufacture. ? Warning, or aposematic, coloration is characteristic of organisms that are poisonous, sting, or are otherwise harmful. In contrast, cryptic coloration, or camouflage, is characteristic of nonpoisonous organisms. ? Predator-prey relationships are of crucial importance in limiting population sizes in nature. 3. What morphological defenses do plants use to defend themselves against herbivores? 4. Consider aposematic coloration, cryptic coloration, and Batesian mimicry. Which would be associated with an adult viceroy butterfly? Which would be associated with a larval monarch butterfly? Which would be associated with a larval viceroy butterfly? 25.2 Predators and their prey coevolve. ? Coevolution occurs when different kinds of organisms evolve adjustments to one another over long periods of time. ? Many organisms have coevolved to a point of dependence. In mutualism the relationship is mutually beneficial; in commensalism, only one organism benefits while the other is unharmed; and in parasitism one organism serves as a host to another, usually to the host’s disadvantage. 5. Why is eliminating predators a bad idea for species richness? 6. How can predation and competition interact in regulating species diversity of a community? 25.3 Evolution sometimes fosters cooperation. ? Primary succession takes place in barren areas, like rocks or open water. Secondary succession takes place in areas where the original communities of organisms have been disturbed. ? Succession occurs because of tolerance, facilitation, and inhibition. ? Disturbance can disrupt successional changes. In some cases, disturbance can increase species richness of a community. 7. Why have scientists altered the concept of a final, climax vegetation in a given ecosystem? What types of organisms are often associated with early stages of succession? What is the role of disturbance in succession? 25.4 Ecological succession may increase species richness. www.mhhe.com/raven6e www.biocourse.com ? Introduction to Communities ? Community Organization ? On Science Article: Killer Bees ? Student Research: Hermit Crab—Sea Anemone Associations ? Succession ? Book Review: Guns, Germs, and Steel by Diamond 533 26 Animal Behavior Concept Outline 26.1 Ethology focuses on the natural history of behavior. Approaches to the Study of Behavior. Field biologists focus on evolutionary aspects of behavior. Behavioral Genetics. At least some behaviors are genetically determined. 26.2 Comparative psychology focuses on how learning influences behavior. Learning. Association plays a major role in learning. The Development of Behavior. Parent-offspring interactions play a key role in the development of behavior. The Physiology of Behavior. Hormones influence many behaviors, particularly reproductive ones. Behavioral Rhythms. Many behaviors are governed by innate biological clocks. 26.3 Communication is a key element of many animal behaviors. Courtship. Animals use many kinds of signals to court one another. Communication in Social Groups. Bees and other social animals communicate in complex ways. 26.4 Migratory behavior presents many puzzles. Orientation and Migration. Animals use many cues from the environment to navigate during migrations. 26.5 To what degree animals “think” is a subject of lively dispute. Animal Cognition. It is not clear to what degree animals “think.” O rganisms interact with their environment in many ways. To understand these interactions, we need to appreciate both the internal factors that shape the way an animal behaves, as well as aspects of the external environ- ment that affect individuals and organisms. In this chapter, we explore the mechanisms that determine an animal’s be- havior (figure 26.1), as well as the ways in which behavior develops in an individual. In the next chapter, we will con- sider the field of behavioral ecology, which investigates how natural selection has molded behavior through evolu- tionary time. FIGURE 26.1 Rearing offspring involves complex behaviors. Living in groups called prides makes lions better mothers. Females share the responsibilities of nursing and protecting the pride’s young, increasing the probability that the youngsters will survive into adulthood. other males and to attract a female to reproduce; this is the ultimate, or evolutionary, explanation for the male’s vocalization. The study of behavior has had a long history of contro- versy. One source of controversy has been the question of whether behavior is determined more by an individual’s genes or its learning and experience. In other words, is be- havior the result of nature (instinct) or nurture (experi- ence)? In the past, this question has been considered an “ei- ther/or” proposition, but we now know that instinct and experience both play significant roles, often interacting in complex ways to produce the final behavior. The scientific study of instinct and learning, as well as their interrelation- ship, has led to the growth of several scientific disciplines, including ethology, behavioral genetics, behavioral neuro- science, and comparative psychology. Ethology Ethology is the study of the natural history of behavior. Early ethologists (figure 26.2) were trained in zoology and evolutionary biology, fields that emphasize the study of an- imal behavior under natural conditions. As a result of this training, they believed that behavior is largely instinctive, or innate—the product of natural selection. Because behav- ior is often stereotyped (appearing in the same way in dif- ferent individuals of a species), they argued that it must be based on preset paths in the nervous system. In their view, these paths are structured from genetic blueprints and cause animals to show a relatively complete behavior the first time it is produced. The early ethologists based their opinions on behav- iors such as egg retrieval by geese. Geese incubate their eggs in a nest. If a goose notices that an egg has been knocked out of the nest, it will extend its neck toward the egg, get up, and roll the egg back into the nest with a side-to-side motion of its neck while the egg is tucked beneath its bill. Even if the egg is removed during re- trieval, the goose completes the behavior, as if driven by a program released by the initial sight of the egg outside the nest. According to ethologists, egg retrieval behavior is triggered by a sign stimulus (also called a key stimu- lus), the appearance of an egg out of the nest; a compo- nent of the goose’s nervous system, the innate releasing mechanism, provides the neural instructions for the motor program, or fixed action pattern (figure 26.3). More generally, the sign stimulus is a “signal” in the en- vironment that triggers a behavior. The innate releasing mechanism is the sensory mechanism that detects the sig- nal, and the fixed action pattern is the stereotyped act. 534 Part VII Ecology and Behavior Approaches to the Study of Behavior During the past two decades, the study of animal behavior has emerged as an important and diverse science that bridges several disciplines within biology. Evolution, ecol- ogy, physiology, genetics, and psychology all have natural and logical linkages with the study of behavior, each disci- pline adding a different perspective and addressing differ- ent questions. Research in animal behavior has made major contribu- tions to our understanding of nervous system organization, child development, and human communication, as well as the process of speciation, community organization, and the mechanism of natural selection itself. The study of the be- havior of nonhuman animals has led to the identification of general principles of behavior, which have been applied, often controversially, to humans. This has changed the way we think about the origins of human behavior and the way we perceive ourselves. Behavior can be defined as the way an organism re- sponds to stimuli in its environment. These stimuli might be as simple as the odor of food. In this sense, a bacterial cell “behaves” by moving toward higher concentrations of sugar. This behavior is very simple and well-suited to the life of bacteria, allowing these organisms to live and repro- duce. As animals evolved, they occupied different environ- ments and faced diverse problems that affected their sur- vival and reproduction. Their nervous systems and behavior concomitantly became more complex. Nervous systems perceive and process information concerning envi- ronmental stimuli and trigger adaptive motor responses, which we see as patterns of behavior. When we observe animal behavior, we can explain it in two different ways. First, we might ask how it all works, that is, how the animal’s senses, nerve networks, or inter- nal state provide a physiological basis for the behavior. In this way, we would be asking a question of proximate causation. To analyze the proximate cause of behavior, we might measure hormone levels or record the impulse activity of neurons in the animal. We could also ask why the behavior evolved, that is, what is its adaptive value? This is a question concerning ultimate causation. To study the ultimate cause of a behavior, we would attempt to determine how it influenced the animal’s survival or re- productive success. Thus, a male songbird may sing dur- ing the breeding season because it has a level of the steroid sex hormone, testosterone, which binds to hor- mone receptors in the brain and triggers the production of song; this would be the proximate cause of the male bird’s song. But the male sings to defend a territory from 26.1 Ethology focuses on the natural history of behavior. Similarly, a frog unfolds its long, sticky tongue at the sight of a moving insect, and a male stickleback fish will attack another male showing a bright red underside. Such responses certainly appear to be programmed and in- stinctive, but what evidence supports the ethological view that behavior has an underlying neural basis? Behavior as a Response to Stimuli in the Environment In the example of egg retrieval behavior in geese, a goose must first perceive that an egg is outside of the nest. To re- spond to this stimulus, it must convert one form of energy which is an input to its visual system—the energy of pho- tons of light—into a form of energy its nervous system can understand and use to respond—the electrical energy of a nerve impulse. Animals need to respond to other stimuli in the environment as well. For an animal to orient from a food source back to its nest, it might rely on the position of the sun. To find a mate, an animal might use a particular chemical scent. The electromagnetic energy of light and the chemical energy of an odor must be converted to the electrical energy of a nerve impulse. This is done through transduction, the conversion of energy in the environment to an action potential, and the first step in the processing of stimuli perceived by the senses. For example, rhodopsin is responsible for the transduction of visual stimuli. Rhodopsin is made of cis-retinal and the protein opsin. Light is absorbed by the visual pigment cis-retinal causing it to change its shape to trans-retinal (see chapter 55). This in turn changes the shape of the companion protein opsin, and induces the first step in a cascade of molecular events that finally triggers a nerve impulse. Sound, odor, and tastes are transduced to nerve impulses by similar processes. Ethologists study behavior from an evolutionary perspective, focusing on the neural basis of behaviors. Chapter 26 Animal Behavior 535 FIGURE 26.2 The founding fathers of ethology: Karl von Frisch, Konrad Lorenz, and Niko Tinbergen pioneered the study of behavioral science. In 1973, they received the Nobel Prize in Physiology or Medicine for their path-making contributions. Von Frisch led the study of honeybee communication and sensory biology. Lorenz focused on social development (imprinting) and the natural history of aggression. Tinbergen examined the functional significance of behavior and was the first behavioral ecologist. FIGURE 26.3 Lizard prey capture. The complex series of movements of the tongue this chameleon uses to capture an insect represents a fixed action pattern. Behavioral Genetics In a famous experiment carried out in the 1940s, Robert Tryon studied the ability of rats to find their way through a maze with many blind alleys and only one exit, where a reward of food awaited. Some rats quickly learned to zip right through the maze to the food, making few incorrect turns, while other rats took much longer to learn the cor- rect path (figure 26.4). Tryon bred the fast learners with one another to establish a “maze-bright” colony, and he similarly bred the slow learners with one another to estab- lish a “maze-dull” colony. He then tested the offspring in each colony to see how quickly they learned the maze. The offspring of maze-bright rats learned even more quickly than their parents had, while the offspring of maze-dull parents were even poorer at maze learning. After repeating this procedure over several generations, Tryon was able to produce two behaviorally distinct types of rat with very different maze-learning abilities. Clearly the ability to learn the maze was to some degree heredi- tary, governed by genes passed from parent to offspring. Furthermore, those genes were specific to this behavior, as the two groups of rats did not differ in their ability to perform other behavioral tasks, such as running a com- pletely different kind of maze. Tryon’s research demon- strates how a study can reveal that behavior has a herita- ble component. Further support for the genetic basis of behavior has come from studies of hybrids. William Dilger of Cornell University has examined two species of lovebird (genus Agapornis), which differ in the way they carry twigs, paper, and other materials used to build a nest. A. personata holds nest material in its beak, while A. roseicollis carries material tucked under its flank feathers (figure 26.5). When Dilger crossed the two species to produce hybrids, he found that the hybrids carry nest material in a way that seems inter- mediate between that of the parents: they repeatedly shift material between the bill and the flank feathers. Other studies conducted on courtship songs in crickets and tree frogs also demonstrate the intermediate nature of hybrid behavior. The role of genetics can also be seen in humans by comparing the behavior of identical twins. Identical twins are, as their name implies, genetically identical. How- ever, most sets of identical twins are raised in the same environment, so it is not possible to determine whether similarities in behavior result from their genetic similar- ity or from experiences shared as they grew up (the clas- sic nature versus nurture debate). However, in some cases, twins have been separated at birth. A recent study of 50 such sets of twins revealed many similarities in per- sonality, temperament, and even leisure-time activities, even though the twins were often raised in very different environments. These similarities indicate that genetics plays a role in determining behavior even in humans, al- though the relative importance of genetics versus envi- ronment is still hotly debated. 536 Part VII Ecology and Behavior Parental generation First generation Second generation Fifth generation Seventh generation Total number of errors in negotiating the maze (fourteen trials) 9 39 64 114 214 Quicker rats Slower rats FIGURE 26.4 The genetics of learning. Tryon selected rats for their ability to learn to run a maze and demonstrated that this ability is influenced by genes. He tested a large group of rats, selected those that ran the maze in the shortest time, and let them breed with one another. He then tested their progeny and again selected those with the quickest maze-running times for breeding. After seven generations, he had succeeded in halving the average time an inexperienced rat required to negotiate the maze. Parallel “artificial selection” for slow running time more than doubled the average running time. FIGURE 26.5 Genetics of lovebird behavior. Lovebirds inherit the tendency to carry nest material, such as these paper strips, under their flank feathers. Single Gene Effects on Behavior The maze-learning, hybrid, and identical twins studies just described suggest genes play a role in behavior, but recent research has provided much greater detail on the genetic basis of behavior. In the fruit fly Drosophila, and in mice, many mutations have been associated with particular be- havioral abnormalities. In fruit flies, for example, individuals that possess alter- native alleles for a single gene differ greatly in their feeding behavior as larvae; larvae with one allele move around a great deal as they eat, whereas individuals with the alterna- tive allele move hardly at all. A wide variety of mutations at other genes are now known in Drosophila which affect al- most every aspect of courtship behavior. The ways in which genetic differences affect behavior have been worked out for several mouse genes. For example, some mice with one mutation have trouble remembering in- formation that they learned two days earlier about where ob- jects are located. This difference appears to result because the mutant mice do not produce the enzyme α-calcium- calmodulin-dependent kinase II, which plays an important role in the functioning of a part of the brain, the hippocam- pus, that is important for spatial learning. Modern molecular biology techniques allow the role of genetics in behavior to be investigated with ever greater precision. For example, male mice genetically engineered (as “knock-outs”) to lack the ability to synthesize nitric oxide, a brain neurotransmitter, show increased aggressive behavior. A particularly fascinating breakthrough occurred in 1996, when scientists using the knock-out technique dis- covered a new gene, fosB, that seems to determine whether or not female mice will nurture their young. Females with both fosB alleles knocked out will initially investigate their newborn babies, but then ignore them, in stark contrast to the caring and protective maternal behavior provided by normal females (figure 26.6). The cause of this inattentiveness appears to result from a chain reaction. When mothers of new babies initially in- spect them, information from their auditory, olfactory, and tactile senses are transmitted to the hypothalamus, where fosB alleles are activated, producing a particular protein, which in turn activates other enzymes and genes that affect the neural circuitry within the hypothalamus. These modi- fications within the brain cause the female to react mater- nally toward her offspring. In contrast, in mothers lacking the fosB alleles, this reaction is stopped midway. No protein is activated, the brain’s neural circuitry is not rewired, and maternal behavior does not result. As these genetic techniques are becoming used more widely, the next few years should see similar dramatic ad- vances in our knowledge of how genes affect behavior in many varieties of humans. The genetic basis of behavior is supported by artificial selection experiments, hybridization studies, and studies on the behavior of mutants. Research has also identified specific genes that control behavior. Chapter 26 Animal Behavior 537 14 12 10 8 6 4 2 0 1.0 0.8 0.6 0.4 0.2 (c) (d) fosB alleles present fosB alleles absent Minutes crouchin g over o f fspr i n g Proporti o n of pups r e triev e d (a) (b) FIGURE 26.6 Genetically caused defect in maternal care. (a) In mice, normal mothers take very good care of their offspring, retrieving them if they move away and crouching over them. (b) Mothers with the mutant fosB allele perform neither of these behaviors, leaving their pups exposed. (c) Amount of time female mice were observed crouching in a nursing posture over offspring. (d) Proportion of pups retrieved when they were experimentally moved. Learning While ethologists were attempting to explain behavior as an instinctive process, comparative psychologists focused heavily on learning as the major element that shapes behav- ior. These behavioral scientists, working primarily on rats in laboratory settings, identified the ways in which animals learn. Learning is any modification of behavior that results from experience rather than maturation. The simplest type of learning, nonassociative learn- ing, does not require an animal to form an association between two stimuli or between a stimulus and a re- sponse. One form of nonassociative learning is habitua- tion, which can be defined as a decrease in response to a repeated stimulus that has no positive or negative conse- quences (that is, no reinforcement). In many cases, the stimulus evokes a strong response when it is first encoun- tered, but the magnitude of the response gradually de- clines with repeated exposure. For example, young birds see many types of objects moving overhead. At first, they may respond by crouching down and remaining still. Some of the objects, like falling leaves or members of their own species flying by, are seen very frequently and have no positive or negative consequence to the nestlings. Over time, the young birds may habituate to such stimuli and stop responding. Thus, habituation can be thought of as learning not to respond to a stimulus. Being able to ignore unimportant stimuli is critical to an animal confronting a barrage of stimuli in a complex en- vironment. Another form of nonassociative learning is sensitization, characterized by an increased responsive- ness to a stimulus. Sensitization is essentially the opposite of habituation. A change in behavior that involves an association be- tween two stimuli or between a stimulus and a response is termed associative learning (figure 26.7). The behavior is modified, or conditioned, through the association. This form of learning is more complex than habituation or sensitization. The two major types of associative learn- ing are called classical conditioning and operant con- ditioning; they differ in the way the associations are established. Classical Conditioning In classical conditioning, the paired presentation of two different kinds of stimuli causes the animal to form an asso- ciation between the stimuli. Classical conditioning is also called Pavlovian conditioning, after Russian psychologist Ivan Pavlov, who first described it. Pavlov presented meat powder, an unconditioned stimulus, to a dog and noted that the dog responded by salivating, an unconditioned response. If an unrelated stimulus, such as the ringing of a bell, was 538 Part VII Ecology and Behavior 26.2 Comparative psychology focuses on how learning influences behavior. FIGURE 26.7 Learning what is edible. Associative learning is involved in predator-prey interactions. (a) A naive toad is offered a bumblebee as food. (b) The toad is stung, and (c) subsequently avoids feeding on bumblebees or any other insects having their black-and-yellow coloration. The toad has associated the appearance of the insect with pain, and modifies its behavior. (a) (b) (c) presented at the same time as the meat powder, over re- peated trials the dog would salivate in response to the sound of the bell alone. The dog had learned to associate the unrelated sound stimulus with the meat powder stimu- lus. Its response to the sound stimulus was, therefore, con- ditioned, and the sound of the bell is referred to as a condi- tioned stimulus. Operant Conditioning In operant conditioning, an animal learns to associate its behavioral response with a reward or punishment. Ameri- can psychologist B. F. Skinner studied operant condition- ing in rats by placing them in an apparatus that came to be called a “Skinner box.” As the rat explored the box, it would occasionally press a lever by accident, causing a pel- let of food to appear. At first, the rat would ignore the lever, eat the food pellet, and continue to move about. Soon, however, it learned to associate pressing the lever (the behavioral response) with obtaining food (the reward). When it was hungry, it would spend all its time pressing the lever. This sort of trial-and-error learning is of major importance to most vertebrates. Comparative psychologists used to believe that any two stimuli could be linked in classical conditioning and that animals could be conditioned to perform any learnable behavior in response to any stimulus by operant condi- tioning. As you will see below, this view has changed. Today, it is thought that instinct guides learning by deter- mining what type of information can be learned through conditioning. Instinct It is now clear that some animals have innate predisposi- tions toward forming certain associations. For example, if a rat is offered a food pellet at the same time it is exposed to X rays (which later produces nausea), the rat will remember the taste of the food pellet but not its size. Conversely, if a rat is given a food pellet at the same time an electric shock is delivered (which immediately causes pain), the rat will re- member the size of the pellet but not its taste. Similarly, pi- geons can learn to associate food with colors but not with sounds; on the other hand, they can associate danger with sounds but not with colors. These examples of learning preparedness demon- strate that what an animal can learn is biologically influ- enced—that is, learning is possible only within the bound- aries set by instinct. Innate programs have evolved because they underscore adaptive responses. Rats, which forage at night and have a highly developed sense of smell, are better able to identify dangerous food by its odor than by its size or color. The seed a pigeon eats may have a distinctive color that the pigeon can see, but it makes no sound the pigeon can hear. The study of learn- ing has expanded to include its ecological significance, so that we are now able to consider the “evolution of learn- ing.” An animal’s ecology, of course, is key to understand- ing what an animal is capable of learning. Some species of birds, like Clark’s nutcracker, feed on seeds. Birds store seeds in caches they bury when seeds are abundant so they will have food during the winter. Thousands of seed caches may be buried and then later recovered. One would expect the birds to have an extraordinary spatial memory, and this is indeed what has been found (figure 26.8). Clark’s nutcracker, and other seed-hoarding birds, have an unusually large hippocampus, the center for memory storage in the brain (see chapter 54). Habituation and sensitization are simple forms of learning in which there is no association between stimuli and responses. In contrast, associative learning (classical and operant conditioning) involves the formation of an association between two stimuli or between a stimulus and a response. Chapter 26 Animal Behavior 539 FIGURE 26.8 The Clark’s nutcracker has an extraordinary memory. A Clark’s nutcracker can remember the locations of up to 2000 seed caches months after hiding them. After conducting experiments, scientists have concluded that the birds use features of the landscape and other surrounding objects as spatial references to memorize the locations of the caches. The Development of Behavior Behavioral biologists now recognize that behavior has both genetic and learned components, and the schools of ethology and psychology are less polarized than they once were. Thus far in this chapter we have discussed the influence of genes and learning separately. As we will see, these factors interact during development to shape behavior. Parent-Offspring Interactions As an animal matures, it may form so- cial attachments to other individuals or form preferences that will influence behavior later in life. This process, called imprinting, is sometimes con- sidered a type of learning. In filial im- printing, social attachments form be- tween parents and offspring. For example, young birds of some species begin to follow their mother within a few hours after hatching, and their fol- lowing response results in a bond be- tween mother and young. However, the young birds’ initial experience de- termines how this imprint is estab- lished. The German ethologist Kon- rad Lorenz showed that birds will follow the first object they see after hatching and direct their social behavior to- ward that object. Lorenz raised geese from eggs, and when he offered himself as a model for imprinting, the goslings treated him as if he were their parent, following him duti- fully (figure 26.9). Black boxes, flashing lights, and water- ing cans can also be effective imprinting objects (figure 26.10). Imprinting occurs during a sensitive phase, or a critical period (roughly 13 to 16 hours after hatching in geese), when the success of imprinting is highest. Several studies demonstrate that the social interactions that occur between parents and offspring during the critical period are key to the normal development of behavior. The psychologist Harry Harlow gave orphaned rhesus monkey infants the opportunity to form social attachments with two surrogate “mothers,” one made of soft cloth covering a wire frame and the other made only of wire. The infants chose to spend time with the cloth mother, even if only the wire mother provided food, indicating that texture and tac- tile contact, rather than providing food, may be among the key qualities in a mother that promote infant social attach- ment. If infants are deprived of normal social contact, their development is abnormal. Greater degrees of deprivation lead to greater abnormalities in social behavior during childhood and adulthood. Studies on orphaned human in- fants suggest that a constant “mother figure” is required for normal growth and psychological development. Recent research has revealed a biological need for the stimulation that occurs during parent-offspring interactions early in life. Female rats lick their pups after birth, and this stimulation inhibits the release of an endorphin (see chap- ter 56) that can block normal growth. Pups that receive normal tactile stimulation also have more brain receptors for glucocorticoid hormones, longer-lived brain neurons, and a greater tolerance for stress. Premature human infants who are massaged gain weight rapidly. These studies indi- cate that the need for normal social interaction is based in the brain and that touch and other aspects of contact be- tween parents and offspring are important for physical as well as behavioral development. Sexual imprinting is a process in which an individual learns to direct its sexual behavior at members of its own species. Cross-fostering studies, in which individuals of one species are raised by parents of another species, reveal that this form of imprinting also occurs early in life. In most species of birds, these studies have shown that the fos- tered bird will attempt to mate with members of its foster species when it is sexually mature. 540 Part VII Ecology and Behavior (a) (b) FIGURE 26.9 An unlikely parent. The eager goslings following Konrad Lorenz think he is their mother. He is the first object they saw when they hatched, and they have used him as a model for imprinting. FIGURE 26.10 How imprinting is studied. Ducklings will imprint on the first object they see, even (a) a black box or (b) a white sphere. Interaction between Instinct and Learning The work of Peter Marler and his colleagues on the ac- quisition of courtship song by white-crowned sparrows provides an excellent example of the interaction between instinct and learning in the development of behavior. Courtship songs are sung by mature males and are species-specific. By rearing male birds in soundproof in- cubators provided with speakers and microphones, Marler could control what a bird heard as it matured and record the song it produced as an adult. He found that white- crowned sparrows that heard no song at all during devel- opment, or that heard only the song of a different species, the song sparrow, sang a poorly developed song as adults (figure 26.11). But birds that heard the song of their own species, or that heard the songs of both the white-crowned sparrow and the song sparrow, sang a fully developed, white-crowned sparrow song as adults. These results sug- gest that these birds have a genetic template, or instinc- tive program, that guides them to learn the appropriate song. During a critical period in development, the tem- plate will accept the correct song as a model. Thus, song acquisition depends on learning, but only the song of the correct species can be learned. The genetic template for learning is selective. However, learning plays a prominent role as well. If a young white-crowned sparrow is surgi- cally deafened after it hears its species’ song during the critical period, it will also sing a poorly developed song as an adult. Therefore, the bird must “practice” listening to himself sing, matching what he hears to the model his template has accepted. Although this explanation of song development stood unchallenged for many years, recent research has shown that white-crowned sparrow males can learn another species’ song under certain conditions. If a live male strawberry finch is placed in a cage next to a young male sparrow, the young sparrow will learn to sing the straw- berry finch’s song! This finding indicates that social stimuli may be more effective than a tape-recorded song in overriding the innate program that guides song devel- opment. Furthermore, the males of some bird species have no opportunity to hear the song of their own species. In such cases, it appears that the males instinc- tively “know” their own species’ song. For example, cuck- oos are brood parasites; females lay their eggs in the nest of another species of bird, and the young that hatch are reared by the foster parents (figure 26.12). When the cuckoos become adults, they sing the song of their own species rather than that of their foster parents. Because male brood parasites would most likely hear the song of their host species during development, it is adaptive for them to ignore such “incorrect” stimuli. They hear no adult males of their own species singing, so no correct song models are available. In these species, natural selec- tion has programmed the male with a genetically guided song. Interactions that occur during sensitive phases of imprinting are critical to normal behavioral development. Physical contact plays an important role in the development of psychological well-being and growth. Chapter 26 Animal Behavior 541 5 4 3 2 1 6 4 2 Frequen cy (k H z ) (a) (b) 0.5 1.0 1.5 2.0 Time (s) FIGURE 26.11 Song development in birds. (a) The sonograms of songs produced by male white-crowned sparrows that had been exposed to their own species’ song during development are different from (b) those of male sparrows that heard no song during rearing. This difference indicates that the genetic program itself is insufficient to produce a normal song. FIGURE 26.12 Brood parasite. Cuckoos lay their eggs in the nests of other species of birds. Because the young cuckoos (large bird to the right) are raised by a different species (like this meadow pipit, smaller bird to the left), they have no opportunity to learn the cuckoo song; the cuckoo song they later sing is innate. The Physiology of Behavior The early ethologists’ emphasis on in- stinct sometimes overlooked the internal factors that control behavior. If asked why a male bird defends a territory and sings only during the breeding season, they would answer that a bird sings when it is in the right motivational state or mood and has the appropriate drive. But what do these phrases mean in terms of physiological control mechanisms? Part of our understanding of the physiological control of behavior has come from the study of reproductive behavior. Animals show reproductive behaviors such as courtship only during the breeding season. Research on lizards, birds, rats, and other animals has revealed that hormones play an im- portant role in these behaviors. Changes in day length trigger the secretion of gonadotropin-releasing hormone by the hypothalamus, which stimulates the re- lease of the gonadotropins, follicle- stimulating hormone (FSH) and luteinizing hormone, by the anterior pi- tuitary gland. These hormones cause the development of reproductive tissues to ready the animal for breeding. The gonadotropins, in turn, stimulate the se- cretion of the steroid sex hormones, es- trogens and progesterone in females and testosterone in males. The sex hor- mones act on the brain to trigger behav- iors associated with reproduction. For example, birdsong and territorial behav- ior depend upon the level of testos- terone in the male, and the receptivity of females to male courtship depends upon estrogen levels. Hormones have both organizational and activational effects. In the example of birdsong given above, estrogen in the male causes the development of the song system, which is composed of neural tissue in the forebrain and its connections to the spinal cord and the syrinx (a structure like our larynx that allows the bird to sing). Early in a male’s development, the gonads produce estrogen, which stimulates neuron growth in the brain. In the mature male, the testes produce testosterone, which activates song. Thus, the development of the neural sys- tems that are responsible for behavior is first organized, then activated by hormones. Research on the physiology of repro- ductive behavior shows that there are important interactions among hor- mones, behavior, and stimuli in both the physical and social environments of an individual. Daniel Lehrman’s work on reproduction in ring doves provides an excellent example of how these factors interact (figure 26.13). Male courtship behavior is controlled by testosterone and related steroid hormones. The male’s behavior causes the release of FSH in the female, and FSH promotes the growth of the ovarian follicles (see chapter 59). The developing follicles re- lease estrogens, which affect other re- productive tissues. Nest construction follows after one or two days. The pres- ence of the nest then triggers the secre- tion of progesterone in the female, initi- ating incubation behavior after the egg is laid. Feeding occurs once the eggs hatch, and this behavior is also hormon- ally controlled. The research of Lehrman and his colleagues paved the way for many addi- tional investigations in behavioral en- docrinology, the study of the hormonal regulation of behavior. For example, male Anolis lizards begin courtship after a seasonal rise in temperature, and the male’s courtship is needed to stimulate the growth of ovarian follicles in the fe- male. These and other studies demon- strate the interactive effects of the phys- ical environment (for example, temperature and day length) and the so- cial environment (such as the presence of a nest and the courtship display of a mate) on the hormonal condition of an animal. Hormones are, therefore, a proximate cause of behavior. To control reproductive behavior, they must be re- leased when the conditions are most fa- vorable for the growth of young. Other behaviors, such as territoriality and dominance behavior, also have hormonal correlates. Hormones may interact with neuro- transmitters to alter behavior. Estrogen affects the neuro- transmitter serotonin in female mice, and may be in part responsible for the “mood swings” experienced by some human females during the menstrual cycle. Hormones have important influences on reproductive and social behavior. 542 Part VII Ecology and Behavior (1) (2) (3) (4) (5) FIGURE 26.13 Hormonal control of reproductive behavior. Reproduction in the ring dove involves a sequence of behaviors regulated by hormones: (1) courtship and copulation; (2) nest building; (3) egg laying; (4) incubation; and (5) feeding crop milk to the young after they hatch. Behavioral Rhythms Many animals exhibit behaviors that vary at regular inter- vals of time. Geese migrate south in the fall, birds sing in the early morning, bats fly at night rather than during the day, and most humans sleep at night and are active in the daytime. Some behaviors are timed to occur in concert with lunar or tidal cycles (figure 26.14). Why do regular re- peating patterns of behavior occur, and what determines when they occur? The study of questions like these has re- vealed that rhythmic animal behaviors are based on both endogenous (internal) rhythms and exogenous (external) timers. Most studies of behavioral rhythms have focused on be- haviors that appear to be keyed to a daily cycle, such as sleeping. Rhythms with a period of about 24 hours are called circadian (“about a day”) rhythms. Many of these behaviors have a strong endogenous component, as if they were driven by a biological clock. Such behaviors are said to be free-running, continuing on a regular cycle even in the absence of any cues from the environment. Almost all fruit fly pupae hatch in the early morning, for example, even if they are kept in total darkness throughout their week-long development. They keep track of time with an internal clock whose pattern is determined by a single gene, called the per (for period) gene. Different mutations of the per gene shorten or lengthen the daily rhythm. The per gene produces a protein in a regular 24-hour cycle in the brain, serving as the fly’s pacemaker of activity. The protein prob- ably affects the expression of other genes that ultimately regulate activity. As the per protein accumulates, it seems to turn off the gene. In mice, the clock gene is responsible for regulating the animal’s daily rhythm. Most biological clocks do not exactly match the rhythms of the environment. Therefore, the behavioral rhythm of an individual deprived of external cues gradually drifts out of phase with the environment. Exposure to an environ- mental cue resets the biological clock and keeps the behav- ior properly synchronized with the environment. Light is the most common cue for resetting circadian rhythms. The most obvious circadian rhythm in humans is the sleep-activity cycle. In controlled experiments, humans have lived for months in underground apartments, where all light is artificial and there are no external cues whatso- ever indicating day length. Left to set their own schedules, most of these people adopt daily activity patterns (one phase of activity plus one phase of sleep) of about 25 hours, although there is considerable variation. Some individuals exhibit 50-hour clocks, active for as long as 36 hours during each period! Under normal circumstances, the day-night cycle resets an individual’s free-running clock every day to a cycle period of 24 hours. What constitutes an animal’s biological clock? In some insects, the clock is thought to be located in the optic lobes of the brain, and timekeeping appears to be based on hor- mones. In mammals, including humans, the biological clock lies in a specific region of the hypothalamus called the suprachiasmatic nucleus (SCN). The SCN is a self- sustaining oscillator, which means it undergoes sponta- neous, cyclical changes in activity. This oscillatory activity helps the SCN to act as a pacemaker for circadian rhythms, but in order for the rhythms to be entrained to external light-dark cycles, the SCN must be influenced by light. In fact, there are both direct and indirect neural projections from the retina to the SCN. The SCN controls circadian rhythms by regulating the secretion of the hormone melatonin by the pineal gland. During the daytime, the SCN suppresses melatonin secre- tion. Consequently, more melatonin is secreted over a 24- hour period during short days than during long days. Vari- ations in melatonin secretion thus serve as an indicator of seasonal changes in day length, and these variations partici- pate in timing the seasonal reproductive behavior of many mammals. Disturbances in melatonin secretion may be par- tially responsible for the “jet-lag” people experience when air travel suddenly throws their internal clocks out of regis- ter with the day-night cycle. Many important behavioral rhythms have cycle periods longer than 24 hours. For example, circannual behaviors such as breeding, hibernation, and migration occur on a yearly cycle. These behaviors seem to be largely timed by hormonal and other physiological changes keyed to ex- ogenous factors such as day length. The degree to which endogenous biological clocks underlie circannual rhythms is not known, as it is very difficult to perform constant- environment experiments of several years’ duration. The mechanism of the biological clock remains one of the most tantalizing puzzles in biology today. Endogenous circadian rhythms have free-running cycle periods of approximately 24 hours; they are entrained to a more exact 24-hour cycle period by environmental cues. Chapter 26 Animal Behavior 543 FIGURE 26.14 Tidal rhythm. Oysters open their shells for feeding when the tide is in and close them when the tide is out. Much of the research in animal behavior is devoted to ana- lyzing the nature of communication signals, determining how they are perceived, and identifying the ecological roles they play and their evolutionary origins. Courtship During courtship, animals produce signals to communicate with potential mates and with other members of their own sex. A stimulus-response chain sometimes occurs, in which the behavior of one individual in turn releases a be- havior by another individual (figure 26.15). Courtship Signaling A male stickleback fish will defend the nest it builds on the bottom of a pond or stream by attacking conspecific males (that is, males of the same species) that approach the nest. Niko Tinbergen studied the social releasers responsible for this behavior by making simple clay models. He found that a model’s shape and degree of resemblance to a fish were 544 Part VII Ecology and Behavior 26.3 Communication is a key element of many animal behaviors. Female gives head-up display to male 1 Male swims zigzag to female and then leads her to nest Male shows female entrance to nest 2 3 4 5 Female enters nest and spawns while male stimulates tail Male enters nest and fertilizes eggs unimportant; any model with a red underside (like the un- derside of a male stickleback) could release the attack be- havior. Tinbergen also used a series of clay models to demonstrate that a male stickleback recognizes a female by her abdomen, swollen with eggs. Courtship signals are often species-specific, limiting com- munication to members of the same species and thus play- ing a key role in reproductive isolation. The flashes of fire- flies (which are actually beetles) are such species-specific signals. Females recognize conspecific males by their flash pattern (figure 26.16), and males recognize conspecific fe- males by their flash response. This series of reciprocal re- sponses provides a continuous “check” on the species iden- tity of potential mates. Visual courtship displays sometimes have more than one component. The male Anolis lizard extends and retracts his fleshy and often colorful dewlap while perched on a branch in his territory (figure 26.17). The display thus involves both color and movement (the extension of the dewlap as well as a series of lizard “push-ups”). To which component of the display does the female respond? Experiments in which the dewlap color is altered with ink show that color is unimportant for some species; that is, a female can be courted successfully by a male with an atypically colored dewlap. FIGURE 26.15 A stimulus-response chain. Stickleback courtship involves a sequence of behaviors leading to the fertilization of eggs. Pheromones Chemical signals also mediate interactions between males and females. Pheromones, chemical messengers used for communication between individuals of the same species, serve as sex attractants among other functions in many ani- mals. Even the human egg produces a chemical attractant to communicate with sperm! Female silk moths (Bombyx mori) produce a sex pheromone called bombykol in a gland associated with the reproductive system. Neurophysiologi- cal studies show that the male’s antennae contain numerous sensory receptors specific for bombykol. These receptors are extraordinarily sensitive, enabling the male to respond behaviorally to concentrations of bombykol as low as one molecule in 10 17 molecules of oxygen in the air! Many insects, amphibians, and birds produce species- specific acoustic signals to attract mates. Bullfrog males call to females by inflating and discharging air from their vocal sacs, located beneath the lower jaw. The female can distin- guish a conspecific male’s call from the call of other frogs that may be in the same habitat and mating at the same time. Male birds produce songs, complex sounds composed of notes and phrases, to advertise their presence and to at- tract females. In many bird species, variations in the males’ songs identify particular males in a population. In these species, the song is individually specific as well as species- specific. Level of Specificity Why should different signals have different levels of speci- ficity? The level of specificity relates to the function of the signal. Many courtship signals are species-specific to help animals avoid making errors in mating that would produce inviable hybrids or otherwise waste reproductive effort. A male bird’s song is individually specific because it allows his presence (as opposed to simply the presence of an unidentifiable member of the species) to be recognized by neighboring birds. When territories are being estab- lished, males may sing and aggressively confront neighbor- ing conspecifics to defend their space. Aggression carries the risk of injury, and it is energetically costly to sing. After territorial borders have been established, intrusions by neighbors are few because the outcome of the contests have already been determined. Each male then “knows” his neighbor by the song he sings, and also “knows” that male does not constitute a threat because they have already settled their territorial contests. So, all birds in the popula- tion can lower their energy costs by identifying their neighbors through their individualistic songs. In a similar way, mammals mark their territories with pheromones that signal individual identity, which may be encoded as a blend of a number of chemicals. Other signals, such as the mobbing and alarm calls of birds, are anonymous, convey- ing no information about the identity of the sender. These signals may permit communication about the presence of a predator common to several bird species. Courtship behaviors are keyed to species-specific visual, chemical, and acoustic signals. Chapter 26 Animal Behavior 545 1 2 3 4 5 6 7 8 9 FIGURE 26.16 Firefly fireworks. The bioluminescent displays of these lampyrid beetles are species-specific and serve as behavioral mechanisms of reproductive isolation. Each number represents the flash pattern of a male of a different species. FIGURE 26.17 Dewlap display of a male Anolis lizard. Under hormonal stimulation, males extend their fleshy, colored dewlaps to court females. This behavior also stimulates hormone release and egg- laying in the female. Communication in Social Groups Many insects, fish, birds, and mam- mals live in social groups in which in- formation is communicated between group members. For example, some individuals in mammalian societies serve as “guards.” When a predator appears, the guards give an alarm call, and group members respond by seek- ing shelter. Social insects, such as ants and honeybees, produce alarm pheromones that trigger attack be- havior. Ants also deposit trail pheromones between the nest and a food source to induce cooperation during foraging (figure 26.18). Honey- bees have an extremely complex dance language that directs nestmates to rich nectar sources. The Dance Language of the Honeybee The European honeybee, Apis mellifera, lives in hives consisting of 30,000 to 40,000 individuals whose behaviors are integrated into a complex colony. Worker bees may forage for miles from the hive, collecting nectar and pollen from a variety of plants and switching between plant species and popula- tions on the basis of how energeti- cally rewarding their food is. The food sources used by bees tend to occur in patches, and each patch of- fers much more food than a single bee can transport to the hive. A colony is able to exploit the resources of a patch because of the behavior of scout bees, which locate patches and communicate their location to hivemates through a dance language. Over many years, Nobel laureate Karl von Frisch was able to unravel the details of this communica- tion system. After a successful scout bee returns to the hive, she per- forms a remarkable behavior pattern called a waggle dance on a vertical comb (figure 26.19). The path of the bee dur- ing the dance resembles a figure-eight. On the straight part of the path, the bee vibrates or waggles her abdomen while producing bursts of sound. She may stop periodically to give her hivemates a sample of the nectar she has carried back to the hive in her crop. As she dances, she is followed closely by other bees, which soon appear as foragers at the new food source. Von Frisch and his colleagues claimed that the other bees use information in the waggle dance to locate the food source. According to their explanation, the scout bee indi- cates the direction of the food source by representing the angle between the food source and the hive in reference to the sun as the angle between the straight part of the dance and vertical in the hive. The distance to the food source is indicated by the tempo, or degree of vigor, of the dance. Adrian Wenner, a scientist at the University of Califor- nia, did not believe that the dance language communicated anything about the location of food, and he challenged von Frisch’s explanation. Wenner maintained that flower odor was the most important cue allowing recruited bees to ar- rive at a new food source. A heated controversy ensued as 546 Part VII Ecology and Behavior (a) (b) FIGURE 26.18 The chemical control of fire ant foraging. Trial pheromones, produced in an accessory gland near the fire ant’s sting, organize cooperative foraging. The trails taken by the first ants to travel to a food source (a) are soon followed by most of the other ants (b). (a) (b) FIGURE 26.19 The waggle dance of honeybees. (a) A scout bee dances on a comb in the hive. (b) The angle between the food source and the nest is represented by a dancing bee as the angle between the straight part of the dance and vertical. The food is 20° to the right of the sun, and the straight part of the bee’s dance on the hive is 20° to the right of vertical. the two groups of researchers published articles supporting their positions. The “dance language controversy” was resolved (in the minds of most scientists) in the mid-1970s by the creative research of James L. Gould. Gould devised an experiment in which hive members were tricked into misinterpreting the directions given by the scout bee’s dance. As a result, Gould was able to manipulate where the hive members would go if they were using visual signals. If odor were the cue they were using, hive members would have appeared at the food source, but instead they appeared exactly where Gould predicted. This confirmed von Frisch’s ideas. Recently, researchers have extended the study of the honeybee dance language by building robot bees whose dances can be completely controlled. Their dances are pro- grammed by a computer and perfectly reproduce the nat- ural honeybee dance; the robots even stop to give food samples! The use of robot bees has allowed scientists to de- termine precisely which cues direct hivemates to food sources. Primate Language Some primates have a “vocabulary” that allows individuals to communicate the identity of specific predators. The vo- calizations of African vervet monkeys, for example, distin- guish eagles, leopards, and snakes (figure 26.20). Chim- panzees and gorillas can learn to recognize a large number of symbols and use them to communicate abstract con- cepts. The complexity of human language would at first ap- pear to defy biological explanation, but closer examination suggests that the differences are in fact superficial—all lan- guages share many basic structural similarities. All of the roughly 3000 languages draw from the same set of 40 con- sonant sounds (English uses two dozen of them), and any human can learn them. Researchers believe these similari- ties reflect the way our brains handle abstract information, a genetically determined characteristic of all humans. Language develops at an early age in humans. Human infants are capable of recognizing the 40 consonant sounds characteristic of speech, including those not present in the particular language they will learn, while they ignore other sounds. In contrast, individuals who have not heard certain consonant sounds as infants can only rarely distinguish or produce them as adults. That is why English speakers have difficulty mastering the throaty French “r,” French speak- ers typically replace the English “th” with “z,” and native Japanese often substitute “l” for the unfamiliar English “r.” Children go through a “babbling” phase, in which they learn by trial and error how to make the sounds of lan- guage. Even deaf children go through a babbling phase using sign language. Next, children quickly and easily learn a vocabulary of thousands of words. Like babbling, this phase of rapid learning seems to be genetically pro- grammed. It is followed by a stage in which children form simple sentences which, though they may be grammatically incorrect, can convey information. Learning the rules of grammar constitutes the final step in language acquisition. While language is the primary channel of human com- munication, odor and other nonverbal signals (such as “body language”) may also convey information. However, it is difficult to determine the relative importance of these other communication channels in humans. The study of animal communication involves analysis of the specificity of signals, their information content, and the methods used to produce and receive them. Chapter 26 Animal Behavior 547 0 1 0.5 seconds Eagle 2 3 4 5 6 7 8 0.5 seconds Leopard 0 1Frequency (kilocycles per second) Frequency (kilocycles per second) 2 3 4 5 6 7 8 (a) (b) FIGURE 26.20 Primate semantics. (a) Predators, like this leopard, attack and feed on vervet monkeys. (b) The monkeys give different alarm calls when eagles, leopards, and snakes are sighted by troupe members. Each distinctive call elicits a different and adaptive escape behavior. Orientation and Migration Animals may travel to and from a nest to feed or move reg- ularly from one place to another. To do so, they must ori- ent themselves by tracking stimuli in the environment. Movement toward or away from some stimulus is called taxis. The attraction of flying insects to outdoor lights is an example of positive phototaxis. Insects that avoid light, such as the common cockroach, exhibit negative phototaxis. Other stimuli may be used as orienting cues. For example, trout orient themselves in a stream so as to face against the cur- rent. However, not all responses involve a specific orienta- tion. Some animals just become more active when stimulus intensity increases, a responses called kineses. Long-range, two-way movements are known as migra- tions. In many animals, migrations occur circannually. Ducks and geese migrate along flyways from Canada across the United States each fall and return each spring. Monarch butterflies migrate each fall from central and eastern North America to several small, geographically iso- lated areas of coniferous forest in the mountains of central Mexico (figure 26.21). Each August, the butterflies begin a flight southward to their overwintering sites. At the end of winter, the monarchs begin the return flight to their sum- mer breeding ranges. What is amazing about the migration of the monarch, however, is that two to five generations may be produced as the butterflies fly north. The butter- flies that migrate in the autumn to the precisely located overwintering grounds in Mexico have never been there before. When colonies of bobolinks became established in the western United States, far from their normal range in the Midwest and East, they did not migrate directly to their winter range in South America. Instead, they migrated east to their ancestral range and then south along the original flyway (figure 26.22). Rather than changing the original migration pattern, they simply added a new pattern. How Migrating Animals Navigate Biologists have studied migration with great interest, and we now have a good understanding of how these feats of navigation are achieved. It is important to understand the distinction between orientation (the ability to follow a bearing) and navigation (the ability to set or adjust a bear- ing, and then follow it). The former is analogous to using a compass, while the latter is like using a compass in con- junction with a map. Experiments on starlings indicate that inexperienced birds migrate by orientation, while older birds that have migrated previously use true navigation (figure 26.23). Birds and other animals navigate by looking at the sun and the stars. The indigo bunting, which flies during the day and uses the sun as a guide, compensates for the movement of the sun in the sky as the day progresses by reference to the north star, which does not move in the sky. Buntings also use the positions of the constellations and the position of the pole star in the night sky, cues they learn as young birds. Starlings and certain other birds compensate for the sun’s apparent movement in the 548 Part VII Ecology and Behavior 26.4 Migratory behavior presents many puzzles. San Francisco New York Los Angeles Mexico City Summer breeding ranges Overwintering aggregation areas (a) (b) (c) FIGURE 26.21 Migration of monarch butterflies. (a) Monarchs from western North America overwinter in areas of mild climate along the Pacific Coast. Those from the eastern United States and southeastern Canada migrate to Mexico, a journey of over 3000 kilometers that takes from two to five generations to complete. (b) Monarch butterflies arriving at the remote fir forests of the overwintering grounds and (c) forming aggregations on the tree trunks. sky by using an internal clock. If such birds are shown an experimental sun in a fixed position while in captivity, they will change their orientation to it at a constant rate of about 15° per hour. Many migrating birds also have the ability to detect the earth’s magnetic field and to orient themselves with respect to it. In a closed indoor cage, they will attempt to move in the correct geographical direction, even though there are no visible external cues. However, the placement of a pow- erful magnet near the cage can alter the direction in which the birds attempt to move. Magnetite, a magnetized iron ore, has been found in the heads of some birds, but the sen- sory receptors birds employ to detect magnetic fields have not been identified. It appears that the first migration of a bird is innately guided by both celestial cues (the birds fly mainly at night) and the earth’s magnetic field. These cues give the same information about the general direction of the mi- gration, but the information about direction provided by the stars seems to dominate over the magnetic informa- tion when the two cues are experimentally manipulated to give conflicting directions. Recent studies, however, indi- cate that celestial cues tell northern hemisphere birds to move south when they begin their migration, while mag- netic cues give them the direction for the specific migra- tory path (perhaps a southeast turn the bird must make midroute). In short, these new data suggest that celestial and magnetic cues interact during development to fine- tune the bird’s navigation. We know relatively little about how other migrating animals navigate. For instance, green sea turtles migrate from Brazil halfway across the Atlantic Ocean to Ascen- sion Island, where the females lay their eggs. How do they find this tiny island in the middle of the ocean, which they haven’t seen for perhaps 30 years? How do the young that hatch on the island know how to find their way to Brazil? Recent studies suggest that wave ac- tion is an important cue. Many animals migrate in predictable ways, navigating by looking at the sun and stars, and in some cases by detecting magnetic fields. Chapter 26 Animal Behavior 549 FIGURE 26.22 Birds on the move. (a) The summer range of bobolinks recently extended to the far West from their more established range in the Midwest. When they migrate to South America in the winter, bobolinks that nested in the West do not fly directly to the winter range; instead, they fly to the Midwest first and then use the ancestral flyway. (b) The golden plover has an even longer migration route that is circular. These birds fly from Arctic breeding grounds to wintering areas in southeastern South America, a distance of some 13,000 kilometers. Wintering range Breeding range Holland Switzerland Spain Bobolink Golden plover Summer nesting range Winter range Summer nesting range Winter range (a) (b) FIGURE 26.23 Migratory behavior of starlings. The navigational abilities of inexperienced birds differ from those of adults who have made the migratory journey before. Starlings were captured in Holland, halfway along their full migratory route from Baltic breeding grounds to wintering grounds in the British Isles; these birds were transported to Switzerland and released. Experienced older birds compensated for the displacement and flew toward the normal wintering grounds (blue arrow). Inexperienced young birds kept flying in the same direction, on a course that took them toward Spain (red arrow). These observations imply that inexperienced birds fly by orientation, while experienced birds learn true navigation. Animal Cognition It is likely each of us could tell an anecdotal story about the behavior of a pet cat or dog that would seem to suggest that the animal had a degree of reasoning ability or was capable of thinking. For many decades, however, students of animal behavior flatly rejected the notion that nonhuman animals can think. In fact, behaviorist Lloyd Morgan stated that one should never assume a behavior represents conscious thought if there is any other explanation that precludes the assumption of consciousness. The prevailing approach was to treat animals as though they responded to the environ- ment through reflexlike behaviors. In recent years, serious attention has been given to the topic of animal awareness. The central question is whether animals show cognitive behavior—that is, do they process information and respond in a manner that suggests thinking (figure 26.24)? What kinds of behavior would demonstrate cognition? Some birds in urban areas remove the foil caps from nonhomogenized milk bottles to get at the cream beneath, and this behavior is known to have spread within a population to other birds. Japanese macaques learned to wash potatoes and float grain to sep- arate it from sand. A chimpanzee pulls the leaves off of a tree branch and uses the stick to probe the entrance to a termite nest and gather termites. As we saw earlier, vervet monkeys have a vocabulary that identifies specific preda- tors. Only a few experiments have tested the thinking ability of nonhuman animals. Some of these studies suggest that animals may give false information (that is, they “lie”). Currently, researchers are trying to determine if some pri- mates deceive others to manipulate the behavior of the other members of their troop. There are many anecdotal accounts that appear to support the idea that deception oc- curs in some nonhuman primate species such as baboons and chimpanzees, but it has been difficult to devise field- based experiments to test this idea. Much of this type of re- search on animal cognition is in its infancy, but it is sure to grow and to raise controversy. In any case, there is nothing to be gained by a dogmatic denial of the possibility of animal consciousness. 550 Part VII Ecology and Behavior 26.5 To what degree animals “think” is a subject of lively dispute. (a) (b) FIGURE 26.24 Animal thinking? (a) This chimpanzee is stripping the leaves from a twig, which it will then use to probe a termite nest. This behavior strongly suggests that the chimpanzee is consciously planning ahead, with full knowledge of what it intends to do. (b) This sea otter is using a rock as an “anvil,” against which it bashes a clam to break it open. A sea otter will often keep a favorite rock for a long time, as though it has a clear idea of what it is going to use the rock for. Behaviors such as these suggest that animals have cognitive abilities. In any case, some examples, particularly those involving problem-solving, are hard to explain in any way other than as a result of some sort of mental process. For example, in a series of classic experiments conducted in the 1920s, a chimpanzee was left in a room with a banana hanging from the ceiling out of reach. Also in the room were several boxes, each lying on the floor. After unsuccessful attempts to jump up and grab the bananas, the chimpanzee suddenly looks at the boxes and immediately proceeds to move them underneath the banana, stack one on top of another, and climb up to claim its prize (figure 26.25). Perhaps it is not so surprising to find obvious intelli- gence in animals as closely related to us as chimpanzees. But recent studies have found that other animals also show evidence of cognition. Ravens have always been con- sidered among the most intelligent of birds. Bernd Hein- rich of the University of Vermont recently conducted an experiment using a group of hand-reared crows that lived in an outdoor aviary. Heinrich placed a piece of meat on the end of a string and hung it from a branch in the aviary. The birds liked to eat meat, but had never seen string before and were unable to get at the meat. After several hours, during which time the birds periodically looked at the meat but did nothing else, one bird flew to the branch, reached down, grabbed the string, pulled it up, and placed it under his foot. He then reached down and grabbed another piece of the string, repeating this ac- tion over and over, each time bringing the meat closer (figure 26.26). Eventually, the meat was within reach and was grasped. The raven, presented with a completely novel problem, had devised a solution. Eventually, three of the other five ravens also figured out how to get to the meat. Heinrich has conducted other similarly creative ex- periments that can leave little doubt that ravens have ad- vanced cognitive abilities. Research on the cognitive behavior of animals is in its infancy, but some examples are compelling. Chapter 26 Animal Behavior 551 FIGURE 26.26 Problem solving by a raven. Confronted with a problem it had never previously confronted, the raven figures out how to get the meat at the end of the string by repeatedly pulling up a bit of string and stepping on it. FIGURE 26.25 Problem solving by a chimpanzee. Unable to get the bananas by jumping, the chimpanzee devises a solution. 552 Part VII Ecology and Behavior Chapter 26 Summary Questions Media Resources 26.1 Ethology focuses on the natural history of behavior. ? Behavior is an adaptive response to stimuli in the environment. An animal’s sensory systems detect and process information about these stimuli. 1. How does a hybrid lovebird’s method of carrying nest materials compare with that of its parents? What does this comparison suggest about whether the behavior is instinctive or learned? ? Behavior is both instinctive (influenced by genes) and learned through experience. Genes are thought to limit the extent to which behavior can be modified and the types of associations that can be made. ? The simplest forms of learning involve habituation and sensitization. More complex associative learning, such as classical and operant conditioning, may be due to the strengthening or weakening of existing synapses as well as the formation of entirely new synapses. ? An animal’s internal state influences when and how a behavior will occur. Hormones can change an ani- mal’s behavior and perception of stimuli in a way that facilitates reproduction. 2. How does associative learning differ from nonassociative learning? How does classical conditioning differ from operant conditioning? 3. What is filial imprinting? What is sexual imprinting? Why do some young animals imprint on objects like a moving box? 4. How does Marler’s work on song development in white- crowned sparrows indicate that behavior is shaped by learning? How does it indicate that behavior is shaped by instinct? 26.2 Comparative psychology focuses on how learning influences behavior. ? Animals communicate by producing visual, acoustic, and chemical signals. These signals are involved in mating, finding food, defense against predators, and other social situations. 5. How do communication signals participate in reproductive isolation? Give one example of a signal that is species-specific. Why are some signals individually specific? 26.3 Communication is a key element of many animal behaviors. ? Animals use cues such as the position of the sun and stars to orient during daily activities and to navigate during long-range migrations. 6. What is the definition of taxis? What are kineses? What cues do migrating birds use to orient and navigate during their migrations? 26.4 Migratory behavior presents many puzzles. ? Many anecdotal accounts point to animal cognition, but research is in its infancy. 7. What evidence would you accept that an animal is “thinking”? 26.5 To what degree animals “think” is a subject of lively dispute. www.mhhe.comraven6e www.biocourse.com ? On Science Article: Polyandry in Hawks 553 27 Behavioral Ecology Concept Outline 27.1 Evolutionary forces shape behavior. Behavioral Ecology. Behavior is shaped by natural selection. Foraging Behavior. Natural selection favors the most efficient foraging behavior. Territorial Behavior. Animals defend territory to increase reproductive advantage and foraging efficiency. 27.2 Reproductive behavior involves many choices influenced by natural selection. Parental Investment and Mate Choice. The degree of parental investment strongly influences other reproductive behaviors. Reproductive Competition and Sexual Selection. Mate choice affects reproductive success, and so is a target of natural selection. Mating Systems. Mating systems are reproductive solutions to particular ecological challenges. 27.3 There is considerable controversy about the evolution of social behavior. Factors Favoring Altruism and Group Living. Many explanations have been put forward to explain the evolution of altruism. Examples of Kin Selection. One explanation for altruism is that individuals can increase the extent to which their genes are passed on to the next generation by aiding their relatives. Group Living and the Evolution of Social Systems. Insect societies exhibit extreme cooperation and altruism, perhaps as a result of close genetic relationship of society members. 27.4 Vertebrates exhibit a broad range of social behaviors. Vertebrate Societies. Many vertebrate societies exhibit altruism. Human Sociobiology. Human behavior, like that of other vertebrates, is influenced by natural selection. A nimal behavior can be investigated in a variety of ways. An investigator can ask, how did the behavior develop? What is the physiology behind the behavior? Or what is the function of the behavior (figure 27.1), and does it confer an advantage to the animal? The field of behav- ioral ecology deals with the last two questions. Specifically, behavioral ecologists study the ways in which behavior may be adaptive by allowing an animal to increase or even maxi- mize its reproductive success. This chapter examines both of these aspects of behavioral ecology. FIGURE 27.1 A snake in the throes of death—or is it? When threatened, many organisms feign death, as this snake is doing—foaming at the mouth and going limp or looking paralyzed. success, behavioral ecologists are interested in how a trait can lead to greater reproductive success. By enhancing en- ergy intake, thus increasing the number of offspring pro- duced? By improving success in getting more matings? By decreasing the chance of predation? The job of a behav- ioral ecologist is to determine the effect of a behavioral trait on each of these activities and then to discover whether increases in, for example, foraging efficiency, translate into increased fitness. Behavioral ecology is the study of how natural selection shapes behavior. 554 Part VII Ecology and Behavior Behavioral Ecology In an important essay, Nobel laureate Niko Tinbergen outlined the different types of questions biologists can ask about animal behavior. In essence, he divided the investi- gation of behavior into the study of its development, physiological basis, and function (evolutionary signifi- cance). One type of evolutionary analysis pioneered by Tinbergen himself was the study of the survival value of behavior. That is, how does an animal’s behavior allow it to stay alive or keep its offspring alive? For example, Tin- bergen observed that after gull nestlings hatch, the par- ents remove the eggshells from the nest. To understand why this behavior occurs, he camouflaged chicken eggs by painting them to resemble the natural background where they would lie and distributed them throughout the area in which the gulls were nesting (figure 27.2). He placed broken eggshells next to some of the eggs, and as a con- trol, he left other camouflaged eggs alone without eggshells. He then noted which eggs were found more easily by crows. Because the crows could use the white in- terior of a broken eggshell as a cue, they ate more of the camouflaged eggs that were near eggshells. Thus, Tinber- gen concluded that eggshell removal behavior is adaptive: it reduces predation and thus increases the offspring’s chances of survival. Tinbergen is credited with being one of the founders of the field of behavioral ecology, the study of how natural selection shapes behavior. This branch of ecology examines the adaptive significance of behavior, or how behavior may increase survival and reproduction. Current research in behavioral ecology focuses on the contribution behavior makes to an animal’s reproductive success, or fitness. As we saw in chapter 26, differences in behavior among indi- viduals often result from genetic differences. Thus, natural selection operating on behavior has the potential to pro- duce evolutionary change. To study the relation between behavior and fitness, then, is to study the process of adapta- tion itself. Consequently, the field of behavioral ecology is con- cerned with two questions. First, is behavior adaptive? Although it is tempting to assume that the behavior pro- duced by individuals must in some way represent an adaptive response to the environment, this need not be the case. As we saw in chapter 20, traits can evolve for many reasons other than natural selection, such as ge- netic drift or gene flow. Moreover, traits may be present in a population because they evolved as adaptations in the past, but no longer are useful. These possibilities hold true for behavioral traits as much as they do for any other kind of trait. If a trait is adaptive, the question then becomes: how is it adaptive? Although the ultimate criterion is reproductive 27.1 Evolutionary forces shape behavior. FIGURE 27.2 The adaptive value of egg coloration. Niko Tinbergen painted chicken eggs to resemble the mottled brown camouflage of gull eggs. The eggs were used to test the hypothesis that camouflaged eggs are more difficult for predators to find and thus increase the young’s chances of survival.. Foraging Behavior The best introduction to behavioral ecology is the exami- nation of one well-defined behavior in detail. While many behaviors might be chosen, we will focus on forag- ing behavior. For many animals, food comes in a variety of sizes. Larger foods may contain more energy but may be harder to capture and less abundant. In addition, some types of food may be farther away than other types. Hence, foraging for these animals involves a trade-off be- tween a food’s energy content and the cost of obtaining it. The net energy (in calories or Joules) gained by feeding on each size prey is simply the energy content of the prey minus the energy costs of pursuing and handling it. Ac- cording to optimal foraging theory, natural selection favors individuals whose foraging behavior is as energeti- cally efficient as possible. In other words, animals tend to feed on prey that maximize their net energy intake per unit of foraging time. A number of studies have demonstrated that foragers do preferentially utilize prey that maximize the energy return. Shore crabs, for example, tend to feed primarily on intermediate-sized mussels which provide the greatest energetic return; larger mussels provide more energy, but also take considerably more energy to crack open (figure 27.3). This optimal foraging approach makes two assump- tions. First, natural selection will only favor behavior that maximizes energy acquisition if increased energy reserves lead to increases in reproductive success. In some cases, this is true. For example, in both Columbian ground squirrels and captive zebra finches, a direct relationship exists between net energy intake and the number of off- spring raised; similarly, the reproductive success of orb- weaving spiders is related to how much food they can capture. However, animals have other needs beside energy acqui- sition, and sometimes these needs come in conflict. One obvious alternative is avoiding predators: oftentimes the behavior that maximizes energy intake is not the one that minimizes predation risk. Thus, the behavior that maxi- mizes fitness often may reflect a trade-off between obtain- ing the most energy at the least risk of being eaten. Not surprisingly, many studies have shown that a wide variety of animal species alter their foraging behavior when preda- tors are present. Still another alternative is finding mates: males of many species, for example, will greatly reduce their feeding rate in order to enhance their ability to attract and defend females. The second assumption of optimal foraging theory is that it has resulted from natural selection. As we have seen, natural selection can lead to evolutionary change only when differences among individuals have a genetic basis. Few studies have investigated whether differences among individuals in their ability to maximize energy in- take is the result of genetic differences, but there are some exceptions. For example, one study found that female zebra finches that were particularly successful in maximiz- ing net energy intake tended to have offspring that were similarly successful. Because birds were removed from their mothers before they left the nest, this similarity likely reflected a genetic basis for foraging behavior, rather than being a result of young birds learning to for- age from their mothers. Differences among individuals in foraging behavior may also be a function of age. Inexperienced yellow-eyed juncos (a small North American bird), for example, have not learned how to handle large prey items efficiently. As a re- sult, the energetic costs of eating such prey are higher than the benefits, and as a result they tend to focus on smaller prey. Only when the birds are older and more experienced do they learn to easily dispatch these prey, which are then included in the diet. Natural selection may favor the evolution of foraging behaviors that maximize the amount of energy gained per unit time spent foraging. Animals that acquire energy efficiently during foraging may increase their fitness by having more energy available for reproduction, but other considerations, such as avoiding predators, also are important in determining reproductive success. Chapter 27 Behavioral Ecology 555 6.0 Energy gain (J/s) No . of m ussels eaten per da y Length of mussel (mm) 10 20 30 40 4.0 2.0 6 4 2 5 3 1 FIGURE 27.3 Optimal diet. The shore crab selects a diet of energetically profitable prey. The curve describes the net energy gain (equal to energy gained minus energy expended) derived from feeding on different sizes of mussels. The bar graph shows the numbers of mussels of each size in the diet. Shore crabs most often feed on those mussels that provide the most energy. Territorial Behavior Animals often move over a large area, or home range, during their daily course of activity. In many animal species, the home ranges of several individuals may over- lap in time or in space, but each individual defends a por- tion of its home range and uses it exclusively. This behav- ior, in which individual members of a species maintain exclusive use of an area that contains some limiting re- source, such as foraging ground, food, or potential mates, is called territoriality (figure 27.4). The critical aspect of territorial behavior is defense against intrusion by other in- dividuals. Territories are defended by displays that adver- tise that the territories are occupied and by overt aggres- sion. A bird sings from its perch within a territory to prevent a takeover by a neighboring bird. If an intruder is not deterred by the song, it may be attacked. However, territorial defense has its costs. Singing is energetically expensive, and attacks can lead to injury. In addition, ad- vertisement through song or visual display can reveal one’s position to a predator. Why does an animal bear the costs of territorial de- fense? Over the past two decades, it has become increas- ingly clear that an economic approach can be useful in an- swering this question. Although there are costs to defending a territory, there are also benefits; these benefits may take the form of increased food intake, exclusive ac- cess to mates, or access to refuges from predators. Studies of nectar-feeding birds like hummingbirds and sunbirds provide an example (figure 27.5). A bird benefits from hav- ing the exclusive use of a patch of flowers because it can efficiently harvest the nectar they produce. In order to maintain exclusive use, however, the bird must actively de- fend the flowers. The benefits of exclusive use outweigh the costs of defense only under certain conditions. Sun- birds, for example, expend 3000 calories per hour chasing intruders from a territory. Whether or not the benefit of defending a territory will exceed this cost depends upon the amount of nectar in the flowers and how efficiently the bird can collect it. If flowers are very scarce or nectar lev- els are very low, for example, a nectar-feeding bird may not gain enough energy to balance the energy used in de- fense. Under this circumstance, it is not advantageous to be territorial. Similarly, if flowers are very abundant, a bird can efficiently meet its daily energy requirements without behaving territorially and adding the costs of de- fense. From an energetic standpoint, defending abundant resources isn’t worth the cost. Territoriality thus only oc- curs at intermediate levels of flower availability and higher levels of nectar production, where the benefits of defense outweigh the costs. In many species, exclusive access to females is a more important determinant of territory size of males than is food availability. In some lizards, for example, males maintain enormous territories during the breeding sea- son. These territories, which encompass the territories of several females, are much larger than what is required to supply enough food and are defended vigorously. In the nonbreeding season, by contrast, male territory size de- creases dramatically, as does aggressive territorial behavior. An economic approach can be used to explain the evolution and ecology of reproductive behaviors such as territoriality. This approach assumes that animals that gain more energy from a behavior than they expend will have an advantage in survival and reproduction over animals that behave in less efficient ways. 556 Part VII Ecology and Behavior 0 100 m 9 9 10 10 R R R R R R 7 7 8 8 5 5 6 6 3 3 4 4 1 1 2 2 N N N N FIGURE 27.4 Competition for space. Territory size in birds is adjusted according to the number of competitors. When six pairs of great tits (Parus major) were removed from their territories (indicated by R in the left figure), their territories were taken over by other birds in the area and by four new pairs (indicated by N in the right figure). Numbers correspond to the birds present before and after. FIGURE 27.5 The benefit of territoriality. Sunbirds increase nectar availability by defending flowers. Searching for a place to nest, finding a mate, and rearing young involve a collection of behaviors loosely referred to as reproductive behavior. These behaviors often in- volve seeking and defending a particular territory, mak- ing choices about mates and about the amount of energy to devote to the rearing of young. Mate selection, in par- ticular, often involves intense natural selection. We will look briefly at each of these components of reproductive behavior. During the breeding season, animals make several im- portant “decisions” concerning their choice of mates, how many mates to have, and how much time and energy to devote to rearing offspring. These decisions are all aspects of an animal’s reproductive strategy, a set of behaviors that presumably have evolved to maximize reproductive success. Reproductive strategies have evolved partly in re- sponse to the energetic costs of reproduction and the way food resources, nest sites, and members of the opposite sex are spatially distributed in the environment. Parental Investment and Mate Choice Males and females usually differ in their reproductive strategies. Darwin was the first to observe that females often do not simply mate with the first male they en- counter, but instead seem to evaluate a male’s quality and then decide whether to mate. This behavior, called mate choice, has since been described in many invertebrate and vertebrate species. By contrast, mate choice by males is much less common. Why should this be? Many of the differences in reproduc- tive strategies between the sexes can be understood by comparing the parental investment made by males and fe- males. Parental investment refers to the contributions each sex makes in producing and rearing offspring; it is, in effect, an estimate of the energy expended by males and fe- males in each reproductive event. Many studies have shown that parental investment is high in females. One reason is that eggs are much larger than sperm—195,000 times larger in humans! Eggs contain proteins and lipids in the yolk and other nutrients for the developing embryo, but sperm are little more than mobile DNA. Furthermore, in some groups of animals, females are responsible for gestation and lactation, costly reproductive functions only they can carry out. The consequence of such great disparities in reproduc- tive investment is that the sexes should face very different selective pressures. Because any single reproductive event is relatively cheap for mates, they can best increase their fit- ness by mating with as many females as possible—male fit- ness is rarely limited by the amount of sperm they can pro- duce. By contrast, each reproductive event for females is much more costly and the number of eggs that can be pro- duced often does limit reproductive success. For this rea- son, females have an incentive to be choosy, trying to pick the male the can provide the greatest benefit to her off- spring. As we shall see, this benefit can take a number of different forms. These conclusions only hold when female reproductive investment is much greater than that of males. In species with parental care, males may contribute equally to the cost of raising young; in this case, the degree of mate choice should be equal between the sexes. Furthermore, in some cases, male investment exceeds that of females. For example, male mormon crickets transfer a protein-containing spermatophore to females during mating. Almost 30% of a male’s body weight is made up by the spermatophore, which provides nutrition for the female, and helps her develop her eggs. As one might expect, in this case it is the females that compete with each other for access to males, and the males that are the choosy sex. Indeed, males are quite selective, favoring heavier females. The selective advantage of this strategy results because heavier females have more eggs; thus, males that choose larger females leave more offspring (figure 27.6). Reproductive investment by the sexes is strongly influenced by differences in the degree of parental investment. Chapter 27 Behavioral Ecology 557 27.2 Reproductive behavior involves many choices influenced by natural selection. 120 100 80 Female body weight Number of mature eggs 60 40 20 0 FIGURE 27.6 The advantage of male mate choice. Male mormon crickets choose heavier females as mates, and larger females have more eggs. Thus, male mate selection increases fitness. Reproductive Competition and Sexual Selection In chapter 20, we learned that the reproductive success of an individual is determined by a number of factors: how long the individual lives, how successful it is in obtaining matings, and how many offspring it produces per mating. The second of these factors, competition for mating oppor- tunities, has been termed sexual selection. Some people consider sexual selection to be distinctive from natural se- lection, but others see it as a subset of natural selection, just one of a number of ways in which organisms can increase their fitness. Sexual selection involves both intrasexual selection, or interactions between members of one sex (“the power to conquer other males in battle,” as Darwin put it), and in- tersexual selection, essentially mate choice (“the power to charm”). Sexual selection thus leads to the evolution of structures used in combat with other males, such as a deer’s antlers and a ram’s horns, as well as ornamentation used to “persuade” members of the opposite sex to mate, such as long tail feathers and bright plumage (figure 27.7a). These traits are called secondary sexual characteristics. Intrasexual Selection In many species, individuals of one sex—usually males— compete with each other for the opportunity to mate with individuals of the other sex. These competitions may take place over ownership of a territory in which females reside or direct control of the females themselves. The latter case is exemplified by many species, such as impala, in which fe- males travel in large groups with a single male that gets ex- clusive rights to mate with the females and thus strives vig- orously to defend these rights against other males which would like to supplant him. In mating systems such as these, a few males may get an inordinate number of matings and most males do not mate at all. In elephant seals, in which males control territories on the breeding beaches, a few dominant males do most of the breeding. On one beach, for example, eight males im- pregnated 348 females, while the remaining males got very little action (or, we could say, while the remaining males mated rarely, if at all). For this reason, selection will strongly favor any trait that confers greater ability to outcompete other males. In many cases, size determines mating success: the larger male is able to dominate the smaller one. As a result, in many territorial species, males have evolved to be considerably larger than females, for the simple reason that the largest males are the ones that get to mate. Such differences be- tween the sexes are referred to as sexual dimorphism. In other species, males have evolved structures used for fight- ing, such as horns, antlers, and large canine teeth. These traits are also often sexually dimorphic and may have evolved because of the advantage they give in intrasexual conflicts. Intersexual Selection Peahens prefer to mate with peacocks that have more spots in their long tail feathers (figure 27.7b,c). Similarly, female frogs prefer to mate with males with more complex calls. Why did such mating preferences evolve? 558 Part VII Ecology and Behavior 140 150 160 Number of eyespots in tail feathers Number of mates 0 5 ? ??? ?? ? ? ? ? FIGURE 27.7 Products of sexual selection. Attracting mates with long feathers is common in bird species such as the African paradise whydah (a) and the peacock (b), which show pronounced sexual dimorphism. (c) Female peahens prefer to mate with males with greater numbers of eyespots in their tail feathers. (a) (b) (c) The Benefits of Mate Choice In some cases, the benefits are obvious. In many species of birds and mammals, and some species of other types of ani- mals, males help raise the offspring. In these cases, females would benefit by choosing the male that can provide the best care—the better the parent, the more offspring she is likely to rear. In other species, males provide no care, but maintain territories that provide food, nesting sites, and predator refuges. In such species, females that choose males with the best territories will maximize their reproductive success. Indirect Benefits In other species, however, males provide no direct benefits of any kind to females. In such cases, it is not intuitively obvious what females have to gain by being choosy. More- over, what could be the possible benefit of choosing a male with an extremely long tail or a complex song? A number of theories have been proposed to explain the evolution of such preferences. One idea is that females choose the male that is the healthiest or oldest. Large males, for example, have probably been successful at living long, acquiring a lot of food and resisting parasites and dis- ease. Similarly, in guppies and some birds, the brightness of a male’s color is a reflection of the quality of his diet and overall health. Females may gain two benefits from mating with large or colorful males. First, to the extent that the males’ success in living long and prospering is the result of a good genetic makeup, the female will be ensuring that her offspring receive good genes from their father. Indeed, several studies have demonstrated that males that are pre- ferred by females produce offspring that are more vigorous and survive better than offspring of males that are not pre- ferred. Second, healthy males are less likely to be carrying diseases, which might be transmitted to the female during mating. A variant of this theory goes one step further. In some cases, females prefer mates with traits that are detrimental to survival (figure 27.8). The long tail of the peacock is a hindrance in flying and makes males more vulnerable to predators. Why should females prefer males with such traits? The handicap hypothesis states that only geneti- cally superior mates can survive with such a handicap. By choosing a male with the largest handicap, the female is en- suring that her offspring will receive these quality genes. Of course, the male offspring will also inherit the genes for the handicap. For this reason, evolutionary biologists are still debating the merits of this hypothesis. Other courtship displays appear to have evolved from a predisposition in the female’s sensory system to be stimu- lated by a certain type of stimulus. For example, females may be better able to detect particular colors or sounds at a certain frequency. Sensory exploitation involves the evolu- tion in males of an attractive signal that “exploits” these preexisting biases—if females are particularly adept at de- tecting red objects, for example, then males will evolve red coloration. Consider the vocalizations of the Túngara frog (Physalaemus pustulosus) (see figure 27.8). Unlike related species, males include a “chuck” in their calls. Recent re- search suggests that even females of related species are par- ticularly attracted to calls of this sort, even though males of these species do not produce “chucks.” Why this prefer- ence evolved is unknown, but males of the Túngara frog have evolved to take advantage of it. A great variety of other theories have been proposed to explain the evolution of mating preferences. Many of these theories may be correct in some circumstances and none seems capable of explaining all of the variation in mating behavior in the animal world. This is an area of vibrant re- search with new discoveries appearing regularly. Natural selection has favored the evolution of behaviors that maximize the reproductive success of males and females. By evaluating and selecting mates with superior qualities, an animal can increase its reproductive success. Chapter 27 Behavioral Ecology 559 1 2 0 0.2 Time (s) Frequency (kHz) 0.4 3 0 1 2 3 0 1 2 3 0 1 2 3 4 FIGURE 27.8 The benefits and costs of vocalizing. (a) The male Túngara frog, Physalaemus pustulosus. (b) The males’ calls attract females as well as predatory bats. Calls of greater complexity are represented from top to bottom in (c). Females prefer more complex calls, but these calls are detected particularly well by bats. Consequently, males that females prefer are at the greatest risk of being captured. (a) (b) (c) Mating Systems The number of individuals with which an animal mates during the breeding season varies throughout the animal kingdom. Mating systems such as monogamy (one male mates with one female); polygyny (one male mates with more than one female; figure 27.9), and polyandry (one female mates with more than one male) are aspects of male and female reproductive strategy that concern how many mates an individual has during the breeding season. Like mate choice, mating systems have evolved to maxi- mize reproductive fitness. Much research has shown that mating systems are strongly influenced by ecology. For instance, a male may defend a territory that holds nest sites or food sources necessary for a female to reproduce, and the territory might have resources sufficient for more than one female. If males differ in the quality of the terri- tories they hold, a female’s fitness will be maximized if she mates with a male holding a high-quality territory. Such a male may already have a mate, but it is still more advantageous for the female to breed with that male than with an unmated male that defends a low-quality terri- tory. In this way, natural selection would favor the evolu- tion of polygyny. Mating systems are also constrained by the needs of off- spring. If the presence of both parents is necessary for young to be reared successfully, then monogamy may be favored. This is generally the case in birds, in which over 90% of all species are monogamous. A male may either re- main with his mate and provide care for the offspring or desert that mate to search for others; both strategies may increase his fitness. The strategy that natural selection will favor depends upon the requirement for male assistance in feeding or defending the offspring. In some species, off- spring are altricial—they require prolonged and extensive care. In these species, the need for care by two parents will reduce the tendency for the male to desert his mate and seek other matings. In species where the young are preco- cial (requiring little parental care), males may be more likely to be polygynous. Although polygyny is much more common, polyandrous systems—in which one female mates with several males— are known in a variety of animals. For example, in spotted sandpipers, males take care of all incubation and parenting, and females mate and leave eggs with two or more males. In recent years, researchers have uncovered many unex- pected aspects of animal reproductive systems. Some of these discoveries have resulted from the application of new technologies, whereas others have come from detailed and intensive field studies. Extra-Pair Copulations In chapter 19, we saw how DNA fingerprinting can be used to identify blood samples. Another common use of this technology is to establish paternity. DNA fingerprints are so variable that each individual’s is unique. Thus, by com- paring the DNA of a man and a child, experts can establish with a relatively high degree of confidence whether the man is the child’s father. This approach is now commonly used in paternity law- suits, but it has also become a standard weapon in the arse- nal of behavioral ecologists. By establishing paternity, re- searchers can precisely quantify the reproductive success of individual males and thus assess how successful their partic- ular reproductive strategies have been (figure 27.10a). In one classic study of red-winged blackbirds (figure 27.10b), researchers established that half of all nests contained at least one bird fertilized by a male other than the territory owner; overall, 20% of the offspring were the result of such extra-pair copulations (EPCs). Studies such as this have established that EPCs—“cheat- ing”—are much more pervasive in the bird world than originally suspected. Even in some species that were be- lieved to be monogamous on the basis of behavioral obser- vations, the incidence of offspring being fathered by a male other than the female’s mate is sometimes surprisingly high. Why do individuals have extra-pair copulations? For males, the answer is obvious: increased reproductive suc- cess. For females, it is less clear, as in most cases, it does not result in an increased number of offspring. One possi- 560 Part VII Ecology and Behavior FIGURE 27.9 Female defense polygyny in bats. The male at the lower right is guarding a group of females. bility is that females mate with genetically superior individ- uals, thus enhancing the genes passed on to their offspring. Another possibility is that females can increase the amount of help they get in raising their offspring. If a female mates with more than one male, each male may help raise the off- spring. This is exactly what happens in a common English bird, the dunnock. Females mate not only with the terri- tory owner, but also with subordinate males that hang around the edge of the territory. If these subordinates mate enough with a female, they will help raise her young, pre- sumably because some of these young may have been fa- thered by this male. Alternative Mating Tactics Natural selection has led to the evolution of a variety of other means of increasing reproductive success. For ex- ample, in many species of fish, there are two genetic classes of males. One group is large and defends territo- ries to obtain matings. The other type of male is small and adopts a completely different strategy. They do not maintain territories, but hang around the edge of the ter- ritories of large males. Just at the end of a male’s courtship, when the female is laying her eggs and the ter- ritorial male is depositing sperm, the smaller male will dart in and release its own sperm into the water, thus fer- tilizing some of the eggs. If this strategy is successful, natural selection will favor the evolution of these two dif- ferent male reproductive strategies. Similar patterns are seen in other organisms. In some dung beetles, territorial males have large horns that they use to guard the chambers in which females reside, whereas genetically small males don’t have horns; in- stead, they dig side tunnels and attempt to intercept the female inside her chamber. In isopods, there are three genetic size classes. The medium-sized males pass for fe- males and enter a large male’s territory in this way; the smallest class are so tiny, they are able to sneak in com- pletely undetected. This is just a glimpse of the rich diversity in mating sys- tems that have evolved. The bottom line is: if there is a way of increasing reproductive success, natural selection will favor its evolution. Mating systems represent reproductive adaptations to ecological conditions. The need for parental care, the ability of both sexes to provide it, and the timing of female reproduction are important influences on the evolution of monogamy, polygyny, and polyandry. Detailed study of animal mating systems, along with the use of modern molecular techniques, are revealing many surprises in animal mating systems. This diversity is a testament to the power of natural selection to favor any trait that increases an animal’s fitness. Chapter 27 Behavioral Ecology 561 2 2 2 2 1 1 1 1 1 3 3 4 3 3/3 2/4 5/5 6/8 7/7 11/14 1/8 2/4 3/3 2/5 5/9 0/4 5/6 100 m (a) (b) FIGURE 27.10 The study of paternity. (a) A DNA fingerprinting gel from the dunnock. The bands represent fragments of DNA of different lengths. The four nestlings (D-G) were in the nest of the female. By comparing the bands present in the two males, we can determine which male fathered which offspring. The triangles point to the bands which are diagnostic for one male and not the other. In this case, the beta male fathered three of the four offspring. (b) Results of a DNA fingerprinting study in red- winged blackbirds. Fractions indicate the proportion of offspring fathered by the male in whose territory the nest occurred. Arrows indicate how many offspring were fathered by particular males outside of each territory. Nests on some territories were not sampled. Factors Favoring Altruism and Group Living Altruism—the performance of an action that benefits an- other individual at a cost to the actor—occurs in many guises in the animal world. In many bird species, for exam- ple, parents are assisted in raising their young by other birds, which are called helpers at the nest. In species of both mammals and birds, individuals that spy a predator will give an alarm call, alerting other members of their group, even though such an act would seem to call the predator’s attention to the caller. Finally, lionesses with cubs will allow all cubs in the pride to nurse, including cubs of other females. The existence of altruism has long perplexed evolution- ary biologists. If altruism imposes a cost to an individual, how could an allele for altruism be favored by natural selec- tion? One would expect such alleles to be at a disadvantage and thus their frequency in the gene pool should decrease through time. A number of explanations have been put forward to ex- plain the evolution of altruism. One suggestion often heard on television documentaries is that such traits evolve for the good of the species. The problem with such explanations is that natural selection operates on individu- als within species, not on species themselves. Thus, it is even possible for traits to evolve that are detrimental to the species as a whole, as long as they benefit the individ- ual. In some cases, selection can operate on groups of in- dividuals, but this is rare. For example, if an allele for su- percannibalism evolved within a population, individuals with that allele would be favored, as they would have more to eat; however, the group might eventually eat it- self to extinction, and the allele would be removed from the species. In certain circumstances, such group selec- tion can occur, but the conditions for it to occur are rarely met in nature. In most cases, consequently, the “good of the species” cannot explain the evolution of al- truistic traits. Another possibility is that seemingly altruistic acts aren’t altruistic after all. For example, helpers at the nest are often young and gain valuable parenting experience by assisting established breeders. Moreover, by hanging around an area, such individuals may inherit the territory when the es- tablished breeders die. Similarly, alarm callers may actually be beneficial by causing other animals to panic. In the en- suing confusion, the caller may be able to slip off unde- tected. Detailed field studies in recent years have demon- strated that some acts truly are altruistic, but others are not as they seemed. Reciprocity Robert Trivers, now of Rutgers University, proposed that individuals may form “partnerships” in which mutual ex- changes of altruistic acts occur, because it benefits both participants to do so. In the evolution of such reciprocal altruism, “cheaters” (nonreciprocators) are discriminated against and are cut off from receiving future aid. Accord- ing to Trivers, if the altruistic act is relatively inexpensive, the small benefit a cheater receives by not reciprocating is far outweighed by the potential cost of not receiving fu- ture aid. Under these conditions, cheating should not occur. Vampire bats roost in hollow trees in groups of 8 to 12 individuals. Because these bats have a high metabolic rate, individuals that have not fed recently may die. Bats that have found a host imbibe a great deal of blood; giv- ing up a small amount presents no great energy cost to the donor, and it can keep a roostmate from starvation. Vampire bats tend to share blood with past reciprocators. If an individual fails to give blood to a bat from which it had received blood in the past, it will be excluded from future bloodsharing. Kin Selection The most influential explanation for the origin of altru- ism was presented by William D. Hamilton in 1964. It is perhaps best introduced by quoting a passing remark made in a pub in 1932 by the great population geneticist J. B. S. Haldane. Haldane said that he would willingly lay down his life for two brothers or eight first cousins. Evolu- tionarily speaking, Haldane’s statement makes sense, be- cause for each allele Haldane received from his parents, his brothers each had a 50% chance of receiving the same allele (figure 27.11). Consequently, it is statistically ex- pected that two of his brothers would pass on as many of Haldane’s particular combination of alleles to the next generation as Haldane himself would. Similarly, Haldane and a first cousin would share an eighth of their alleles (see figure 27.11). Their parents, which are siblings, would each share half their alleles, and each of their chil- dren would receive half of these, of which half on the av- erage would be in common: one-half × one-half × one- half = one-eighth. Eight first cousins would therefore pass on as many of those alleles to the next generation as Haldane himself would. Hamilton saw Haldane’s point clearly: natural selection will favor any strategy that in- creases the net flow of an individual’s alleles to the next generation. 562 Part VII Ecology and Behavior 27.3 There is considerable controversy about the evolution of social behavior. Hamilton showed that by directing aid toward kin, or close genetic relatives, an altruist may increase the repro- ductive success of its relatives enough to compensate for the reduction in its own fitness. Because the altruist’s be- havior increases the propagation of alleles in relatives, it will be favored by natural selection. Selection that favors al- truism directed toward relatives is called kin selection. Al- though the behaviors being favored are cooperative, the genes are actually “behaving selfishly,” because they en- courage the organism to support copies of themselves in other individuals. Hamilton’s kin selection model predicts that altruism is likely to be directed toward close relatives. The more closely related two individuals are, the greater the poten- tial genetic payoff. This relationship is described by Hamilton’s rule, which states that altruistic acts are fa- vored when b/c > 1/r. In this expression, b and c are the benefits and costs of the altruistic act, respectively, and r is the coefficient of relatedness, the proportion of alleles shared by two individuals through common descent. For example, an individual should be willing to have one less child if such actions allow a half-sibling, which shares one-quarter of its genes, to have more than four addi- tional offspring. Many factors could be responsible for the evolution of altruistic behaviors. Chapter 27 Behavioral Ecology 563 AB WX 1 2 JK AC XZ 1 3 JM AD WY 1 3 KM FF TT 7 7 RH EE SS 8 8 NQ EA SX 8 3 NM DF WT 3 7 KR CD YZ 3 4 LM Parents Brothers Cousins Unrelated female Unrelated female Gene 1 Gene 2 Gene 3 Gene 4 FIGURE 27.11 Hypothetical example of genetic relationship. On average, full siblings will share half of their alleles. By contrast, cousins will, on average, only share one-eighth of their alleles. Examples of Kin Selection Many examples of kin selection are known from the ani- mal world. For example, Belding’s ground squirrel give alarm calls when they spot a predator such as a coyote or a badger. Such predators may attack a calling squirrel, so giving a signal places the caller at risk. The social unit of a ground squirrel colony consists of a female and her daughters, sisters, aunts, and nieces. Males in the colony are not genetically related to these females. By marking all squirrels in a colony with an individual dye pattern on their fur and by recording which individuals gave calls and the social circumstances of their calling, researchers found that females who have relatives living nearby are more likely to give alarm calls than females with no kin nearby. Males tend to call much less frequently as would be expected as they are not related to most colony members. Another example of kin selection comes from a bird called the white-fronted bee-eater which lives along rivers in Africa in colonies of 100 to 200 birds. In contrast to the ground squirrels, it is the males that usually remain in the colony in which they were born, and the females that dis- perse to join new colonies. Many bee-eaters do not raise their own offspring, but rather help others. Many of these birds are relatively young, but helpers also include older birds whose nesting attempts have failed. The presence of a single helper, on average, doubles the number of off- spring that survive. Two lines of evidence support the idea that kin selection is important in determining help- ing behavior in this species. First, helpers are usually males, which are usually related to other birds in the colony, and not females, which are not related. Second, when birds have the choice of helping different parents, they almost invariably choose the parents to which they are most closely related. Haplodiploidy and Hymenopteran Social Evolution Probably the most famous application of kin selection theory has been to social insects. A hive of honeybees consists of a single queen, who is the sole egg-layer, and up to 50,000 of her offspring, nearly all of whom are fe- male workers with nonfunctional ovaries (figure 27.12), a situation termed eusociality. The sterility of the work- ers is altruistic: these offspring gave up their personal reproduction to help their mother rear more of their sisters. Hamilton explained the origin of altruism in hy- menopterans (that is, bees, wasps, and ants) with his kin selection model. In these insects, males are haploid and females are diploid. This unusual system of sex determi- nation, called haplodiploidy, leads to an unusual situa- tion. If the queen is fertilized by a single male, then all female offspring will inherit exactly the same alleles from their father (because he is haploid and has only one copy of each allele). These female offspring will also share among themselves, on average, half of the alleles they get from the queen. Consequently, each female offspring will share on average 75% of her alleles with each sister (to verify this, rework figure 27.11, but allow the father to only have one allele for each gene). By contrast, should she have offspring of her own, she would only share half of her alleles with these offspring (the other half would come from their father). Thus, because of this close ge- netic relatedness, workers propagate more alleles by giving up their own reproduction to assist their mother in rearing their sisters, some of whom will be new queens and start new colonies and reproduce. Thus, this unusual haplodiploid sys- tem may have set the stage for the evolution of eusocial- ity in hymenopterans and, indeed, such systems have evolved as many as 12 or many times in the Hy- menoptera. One wrinkle in this theory, however, is that eusocial systems have evolved in several other groups, including thrips, termites, and naked mole rats. Although thrips are also haplodiploid, both termites and naked mole rats are not. Thus, although haplodiploidy may have facili- tated the evolution of eusociality, it is not a necessary prerequisite. Kin selection is a potent force favoring, in some situations, the evolution of altruism and even complex social systems. 564 Part VII Ecology and Behavior FIGURE 27.12 Reproductive division of labor in honeybees. The queen (shown here with a red spot painted on her thorax) is the sole egg- layer. Her daughters are sterile workers. Group Living and the Evolution of Social Systems Organisms as diverse as bacteria, cnidarians, in- sects, fish, birds, prairie dogs, lions, whales, and chimpanzees exist in social groups. To encom- pass the wide variety of social phenomena, we can broadly define a society as a group of organ- isms of the same species that are organized in a co- operative manner. Why have individuals in some species given up a solitary existence to become members of a group? We have just seen that one explana- tion is kin selection: groups may be composed of close relatives. In other cases, individuals may benefit directly from social living. For ex- ample, a bird that joins a flock may receive greater protection from predators. As flock size increases, the risk of predation decreases because there are more individuals to scan the environment for predators (figure 27.13). A member of a flock may also increase its feed- ing success if it can acquire information from other flock members about the location of new, rich food sources. In some predators, hunting in groups can increase success and allow the group to tackle prey too large for any one individual. Insect Societies In insects, sociality has chiefly evolved in two orders, the Hymenoptera (ants, bees, and wasps) and the Isoptera (ter- mites), although a few other insect groups include social species. All ants, some bees, some wasps, and all termites are eusocial (truly social): they have a division of labor in reproduction (a fertile queen and sterile workers), coopera- tive care of brood and an overlap of generations so that the queen lives alongside her offspring. Social insect colonies are composed of different castes of workers that differ in size and morphology and have different tasks they perform, such as workers and soldiers. In honeybees, the queen maintains her dominance in the hive by secreting a pheromone, called “queen sub- stance,” that suppresses development of the ovaries in other females, turning them into sterile workers. Drones (male bees) are produced only for purposes of mating. When the colony grows larger in the spring, some mem- bers do not receive a sufficient quantity of queen sub- stance, and the colony begins preparations for swarming. Workers make several new queen chambers, in which new queens begin to develop. Scout workers look for a new nest site and communicate its location to the colony. The old queen and a swarm of female workers then move to the new site. Left behind, a new queen emerges, kills the other potential queens, flies out to mate, and returns to assume “rule” of the hive. The leafcutter ants provide another fascinating exam- ple of the remarkable lifestyles of social insects. Leafcut- ters live in colonies of up to several million individuals, growing crops of fungi beneath the ground. Their mound-like nests are underground “cities” covering more than 100 square meters, with hundreds of entrances and chambers as deep as 5 meters beneath the ground. The division of labor among the worker ants is related to their size. Every day, workers travel along trails from the nest to a tree or a bush, cut its leaves into small pieces, and carry the pieces back to the nest. Smaller workers chew the leaf fragments into a mulch, which they spread like a carpet in the underground fungus chambers. Even smaller workers implant fungal hyphae in the mulch. Soon a luxuriant garden of fungi is growing. While other workers weed out undesirable kinds of fungi, nurse ants carry the larvae of the nest to choice spots in the garden, where the larvae graze. This elaborate social system has evolved to produce reproductive queens that will disperse from the parent nest and start new colonies, repeating the cycle. Eusocial insect workers exhibit an advanced social structure that includes division of labor in reproduction and workers with different tasks. Chapter 27 Behavioral Ecology 565 20 40 0 1 2-10 (a) (b) 11-50 50+ 60 80 100 20 40 0 1 2-10 11-50 Number of pigeons in flock Percent attack success Median reaction distance (m) Number of pigeons in flock 50+ 60 80 100 FIGURE 27.13 Flocking behavior decreases predation. (a) As the size of a pigeon flock increases, hawks are less successful at capturing pigeons. (b) When more pigeons are present in the flock, they can detect hawks at greater distances, thus allowing more time for the pigeons to escape. Vertebrate Societies In contrast to the highly structured and integrated insect societies and their remarkable forms of altruism, vertebrate social groups are usually less rigidly organized and cohe- sive. It seems paradoxical that vertebrates, which have larger brains and are capable of more complex behaviors, are generally less altruistic than insects. Nevertheless, in some complex vertebrate social systems individuals may be exhibiting both reciprocity and kin-selected altruism. But vertebrate societies also display more conflict and aggres- sion among group members than do insect societies. Con- flict in vertebrate societies generally centers on access to food and mates. Vertebrate societies, like insect societies, have particular types of organization. Each social group of vertebrates has a certain size, stability of members, number of breeding males and females, and type of mating system. Behavioral ecologists have learned that the way a group is organized is influenced most often by ecological factors such as food type and predation (figure 27.14). African weaver birds, which construct nests from vege- tation, provide an excellent example to illustrate the rela- tionship between ecology and social organization. Their roughly 90 species can be divided according to the type of social group they form. One set of species lives in the forest and builds camouflaged, solitary nests. Males and females are monogamous; they forage for insects to feed their young. The second group of species nests in colonies in trees on the savanna. They are polygynous and feed in flocks on seeds. The feeding and nesting habits of these two sets of species are correlated with their mating systems. In the forest, insects are hard to find, and both parents must cooperate in feeding the young. The camouflaged nests do not call the attention of predators to their brood. On the open savanna, build- ing a hidden nest is not an option. Rather, savanna- dwelling weaver birds protect their young from predators by nesting in trees which are not very abundant. This shortage of safe nest sites means that birds must nest to- gether in colonies. Because seeds occur abundantly, a fe- male can acquire all the food needed to rear young with- out a male’s help. The male, free from the duties of parenting, spends his time courting many females—a polygynous mating system. One exception to the general rule that vertebrate soci- eties are not organized like those of insects is the naked mole rat, a small, hairless rodent that lives in and near East Africa. Unlike other kinds of mole rats, which live alone or in small family groups, naked mole rats form large under- ground colonies with a far-ranging system of tunnels and a central nesting area. It is not unusual for a colony to con- tain 80 individuals. Naked mole rats feed on bulbs, roots and tubers, which they locate by constant tunneling. As in insect so- cieties, there is a division of labor among the colony members, with some mole rats working as tunnelers while others perform different tasks, depending upon the size of their body. Large mole rats defend the colony and dig tunnels. Naked mole rat colonies have a reproductive division of labor similar to the one normally associated with the euso- cial insects. All of the breeding is done by a single female or “queen,” who has one or two male consorts. The workers, consisting of both sexes, keep the tunnels clear and forage for food. Social behavior in vertebrates is often characterized by kin-selected altruism. Altruistic behavior is involved in cooperative breeding in birds and alarm-calling in mammals. 566 Part VII Ecology and Behavior 27.4 Vertebrates exhibit a broad range of social behaviors. FIGURE 27.14 Foraging and predator avoidance. A meerkat sentinel on duty. Meerkats, Suricata suricata, are a species of highly social mongoose living in the semiarid sands of the Kalahari Desert. This meerkat is taking its turn to act as a lookout for predators. Under the security of its vigilance, the other group members can focus their attention on foraging. Human Sociobiology As a social species, humans have an unparalleled com- plexity. Indeed, we are the only species with the intelli- gence to contemplate the social behavior of other ani- mals. Intelligence is just one human trait. If an ethologist were to take an inventory of human behavior, he or she would list kin-selected altruism; reciprocity and other elaborate social contracts; extensive parental care; con- flicts between parents and offspring; violence and war- fare; infanticide; a variety of mating systems, including monogamy, polygyny, and polyandry; along with sexual behaviors such as extra-pair copulation (“adultery”) and homosexuality; and behaviors like adoption that appear to defy evolutionary explanation. This incredible variety of behaviors occurs in one species, and any trait can change within any individual. Are these behaviors rooted in human biology? Biological and Cultural Evolution During the course of human evolution and the emergence of civilization, two processes have led to adaptive change. One is biological evolution. We have a primate heritage, reflected in the extensive amount of genetic material we share with our closest relatives, the chimpanzees. Our up- right posture, bipedal locomotion, and powerful, precise hand grips are adaptations whose origins are traceable through our primate ancestors. Kin-selected and recipro- cal altruism, as well as other shared traits like aggression and different types of mating systems, can also be seen in nonhuman primates, in whom we can demonstrate that these social traits are adaptive. We may speculate, based on various lines of evidence, that similar traits evolved in early humans. If individuals with certain social traits had an advantage in reproduction over other individuals that lacked the traits, and if these traits had a genetic basis, then the alleles for their expression would now be ex- pected to be part of the human genome and to influence our behavior. The second process that has underscored the emer- gence of civilization and led to adaptive change is cultural evolution, the transfer across generations of information necessary for survival. This is a nongenetic mode of adap- tation. Many adaptations—the use of tools, the formation of cooperative hunting groups, the construction of shel- ters, and marriage practices—do not follow Mendelian rules of inheritance and are passed from generation to generation by tradition. Nonetheless, cultural inheritance is as valid a way to convey adaptations across generations as genetic inheritance. Human cultures are also extraordi- narily diverse. The ways in which children are socialized among Trobriand Islanders, Pygmies, and Yanomamo In- dians are very different. Again, we must remember that this fantastic variation occurs within one species, and that individual behavior is very flexible. Identifying the Biological Components of Human Behavior Given this great flexibility, how can the biological compo- nents of human behavior be identified? One way is to look for common patterns that appear in a wide variety of cul- tures, that is, to study behaviors that are cross-cultural. In spite of cultural variation, there are some traits that char- acterize all human societies. For example, all cultures have an incest taboo, forbidding marriages between close rela- tives. Incestuous matings lead to a greater chance of ex- posing disorders such as mental retardation and hemo- philia. Natural selection may have acted to create a behavioral disposition against incest, and that disposition is now a cultural norm. Genes responsible for guiding this behavior may have become fixed in human populations because of their adaptive effects. Genes thus guide the di- rection of culture. Although human mating systems vary, polygyny is found to be the most common among all cultures. Because most mammalian species are polygynous, the human pattern seems to reflect our mammalian evolutionary heritage and thus is a part of our biology. This conclusion is drawn from using the comparative approach, common in evolutionary science. Nonverbal communication patterns, like smiling and raising the hand in a greeting, also occur in many cul- tures. Perhaps these behaviors represent a common human heritage. The explanations sociobiology offers to understand human behavior have been and continue to be controver- sial. For example, the new discipline of evolutionary psychology seeks to understand the origins of the human mind. Human behaviors are viewed as being extensions of our genes. The diversity of human cultures are thought to have a common core of characteristics that are generated by our psychology, which evolved as an adap- tation to the lifestyle of our hunter-gatherer ancestors during the Pleistocene. Much of human behavior is seen as reflecting ancient, adaptive traits, now expressed in the context of modern civilization. In this controversial view, human behaviors such as jealousy and infidelity are viewed as adaptations; these behaviors increased the fit- ness of our ancestors, and thus are now part of the human psyche. Sociobiology offers general explanations of human behavior that are controversial, but are becoming more generally accepted than in the past. Chapter 27 Behavioral Ecology 567 568 Part VII Ecology and Behavior Chapter 27 Summary Questions Media Resources 27.1 Evolutionary forces shape behavior. ? Many behaviors are ecologically important and serve as adaptations. ? Foraging and territorial behaviors have evolved because they allow animals to use resources efficiently. 1. What does optimal foraging theory predict about an animal’s foraging behavior? What factors unrelated to this theory may also influence an animal’s foraging choices? 2. What are the benefits of territorial behavior, and what are its costs? Under what circumstances is territorial behavior disadvantageous? ? Male and female animals maximize their fitness with different reproductive behaviors. The differences relate to the extent to which each sex provides care for offspring. ? Usually, males are competitive and females show mate choice because females have higher reproductive costs. ? A species’ mating system is related to its ecology. 3. Why does natural selection favor mate choice? What factor is most important in determining which sex exhibits mate choice? 4. In birds, how does the amount of parental care required by the offspring affect the evolution of a species’ mating system? 27.2 Reproductive behavior involves many choices influenced by natural selection. ? Many animals show altruistic, or self-sacrificing, behavior. Altruism may evolve through reciprocity or be directed toward relatives. Cooperative behavior often increases an individual’s inclusive fitness. ? Individuals form social groups because it is advantageous for them to do so. ? The benefits of living in a group, such as enhanced feeding success, are often balanced by the cost of in- creased incidence of disease and parasitism. ? Animal societies are characterized by cooperation and conflict. The organization of a society is related to the ecology of a species. 5. What is reciprocal altruism? What is kin selection? How does kin selection increase an individual’s success in passing its genes on to the next generation? 27.3 There is considerable controversy about the evolution of social behavior. ? Human behavior is extremely rich and varied and may result from both biology and culture. ? Evolutionary theory can give us important insight into human nature, but such an approach to the study of human behavior may have political consequences. 6. In vertebrate societies, what are the costs to an individual who makes an alarm call? Based on research in ground squirrels, which individuals are most likely to make alarm calls, and what benefits do they receive by doing so? 27.4 Vertebrates exhibit a broad range of social behaviors. www.mhhe.com/raven6e www.biocourse.com ? Bioethics Case Study: Behavior Disordered Students ? On Science Article: Repetition and Learning ? On Science Article: Flipper, A Senseless Killer? 569 Identifying the Environmental Culprit Harming Amphibians What started out as a relatively standard field trip in 1995 turned into a bizarre experience for a group of middle- school science students in Minnesota. Their assignment: to collect frogs for their biology class. What they found in local ponds were not frogs like you are accustomed to see- ing, frogs like the one shown here. What they found looked more like the result of some bizarre genetic experi- ment! Approximately half of the animals collected were deformed, with extra legs or missing legs or no eyes. Turning to the Internet, they soon discovered that the problem was not isolated to Minnesota. Neighboring states were reporting the same phenomenon—an alarming number of deformed frogs, all across the United States and Canada. Although deformed frogs such as those collected by the Minnesota students received national attention, a dif- ferent problem affecting amphibians has received even more. During the past 30 years, there has been a world- wide catastrophic decline in amphibian populations, with many local populations becoming extinct. The problem is a focus of intensive research, which indicates that four factors are contributing in a major way to the worldwide amphibian decline: (1) habitat destruction, particularly loss of wetlands, (2) the introduction of exotic species that outcompete local amphibian populations, (3) alter- ation of habitats by toxic chemicals or other human activ- ities (clear-cutting of trees, for example, drastically re- duces humidity), and (4) infection of amphibians by chytrid fungi or ranavirus, both of which are fatal to them. The developmental deformities reported in frogs are also a worldwide problem, but seem to arise from a differ- ent set of factors than those producing global declines in amphibian populations. The increase in deformities seems to reflect the fact that amphibians are particularly sensitive to their environment. Their semi-aquatic mode of living, depending on a watery environment to reproduce and keep their skin moist, means that they are exposed to all types of environmental changes. Amphibians are particularly vulnerable during early de- velopment, when their fertilized eggs lay in water, exposed to potential infection by trematodes that can disrupt devel- opment, to acid introduced to ponds by acid rain, to toxic chemical pollutants, and to increased levels of UV-B radia- tion produced by ozone depletion. While numerous experiments performed under labora- tory conditions have demonstrated the power of these fac- tors to produce developmental deformities, and in so doing to reduce population survival rates, it is important to understand that “can” does not equal “does.” To learn what is in fact going on, scientists have examined the ef- fects of these factors on amphibian development in the natural environment. Some environmental scientists suspected that toxic chemical pollutants in the water might be causing the de- formities and that the widespread occurrence of deformed frogs might well be an early warning of potential future problems in other species, including humans. Other scientists cautioned that a different factor might be responsible. Although chemicals such as pesticides cer- tainly couldproduce deformities in localized situations, say near a chemical spill, so too could other environmental factors affecting local habitats, particularly parasitic infec- tions by trematodes. Demonstrating this point, re- searchers in 1999 showed that the multilimb and missing limb phenomenon in frogs can be caused by trematodes that infect the developing tadpoles, disrupting develop- ment of their limbs. Responding to this alternative suggestion, those scien- tists nominating toxins as the principal culprit have cau- tioned that showing trematode parasites can have a sig- nificant effect on local populations is not the same thing as demonstrating that they have in fact done so. And, they add, it certainly doesn’t rule out a major contribu- tion to the problem by toxic environmental pollutants, or by any of the other potential disruptors of amphibian development. In a particularly clear example of the sort of investiga- tion that will be needed to sort out this complex issue, Andrew Blaustein of Oregon State University headed a team of scientists that set out to examine the effects of UV-B radiation on amphibians in natural populations. In a series of experiments carried out in the field, they at- tempted to assess the degree to which UV-B radiation Part VIII The Global Environment Disappearing amphibians. Populations of amphibians, like this Cas- cades frog (Rana cascadae), are declining in numbers in many regions 570 Part VIII The Global Environment promoted amphibian developmental deformities under natural conditions. Laboratory experiments examining the affects of UV-B on amphibian development had already shown a significant increase in embryonic mortality in some amphibian species, and not in others. Why only in some? Perhaps behaviors shared by many amphibian species might lead to an increased susceptibility to damage from UV-B radiation, behaviors such as laying eggs in open, shallow waters that offer significant exposure to UV-B ra- diation. Perhaps physiological traits of certain species make them particularly susceptible to damage from UV-B radia- tion, traits such as low levels of photolyase, an enzyme that removes harmful photoproducts induced by UV light. Blaustein’s group selected a specimen that exhibits these two factors, the long-toed salamander, Ambystoma macro- dactylum. The Experiment The goal of Blaustein’s field experiment was to allow fertil- ized eggs to develop in their natural environment with and without a UV-B protective shield. Eggs in both groups were monitored for the appearance of deformities and for survival rates. Eggs were collected from natural shallow water sites (H1102120 cm deep) and randomly placed within enclosures con- taining either a UV-B blocking Mylar shield or a UV-B trans- mitting acetate cover (50 eggs per each enclosure replicated four times). The enclosures were placed in small, unperfo- rated plastic pools containing pond water and the pools were placed back in the pond, thereby exposing the eggs and devel- oping embryos to ambient conditions. The UV-B blocking Mylar shield filtered out more than 94% of ambient UV-B radiation, while the UV-B transmitting acetate cover allowed about 90% of ambient UV-B radiation to pass through. The Results Embryos under the UV-B shields had significantly higher hatching rates and fewer deformities compared with those under the UV-B transmitting acetate covers. Of the 29 UV-B exposed individuals that hatched, 25 had deformi- ties. This is significant compared to the 190 UV-B shielded individuals that hatched and only 1 showed deformities. These results support the hypothesis that naturally occur- ring UV-B radiation can adversely affect development in some amphibians, inducing deformities. Blaustein’s group speculates that the higher mortality rates and deformities in frogs and other amphibian species might in fact be due to lower than normal levels of pho- tolyase activity in their developing eggs and embryos, low levels such as found naturally in salamanders. Laboratory and field experiments seem to support this idea. For one thing, frog species that are not sensitive to UV-B have very high photolyase activity levels. Evaluating 10 different species, Blaustein’s team found a strong corre- lation between species exhibiting little UV-B radiation ef- fects and higher levels of photolyase activity in developing eggs and embryos. In these experiments, the Pacific tree frog (Hyla regilla)—whose populations have not shown deformities or decline—exhibited the highest photolyase activity and was not affected by UV-B radiation, showing no significant in- creases in mortality rates in UV-B exposed individuals. In parallel experiments, the Cascades frog (Rana cascadae) and the Western toad (Bufo boreas)—both of whose populations have been experiencing deformities and markedly declining populations—had less than one-third the photolyase activity seen in Hyla, and were strongly af- fected by UV-B radiation, showing significant increases in mortality rates when exposed to UV-B radiation. These results suggest that increased level of UV-B ra- diation resulting from ozone depletion may indeed be a major contributor to amphibian deformities and de- cline—in populations with low photolyase activity. Could chemical pollutants be acting to lower activity levels of this key enzyme? The investigation continues. Undoubt- edly, many factors are contributing to deformities in am- phibian population, and there are not going to be many simple answers. 3 6 10 Length of exposure (days) UV-B blocking shield UV-B transmitting cover 14 25 50 75 Survival rate (percent) 100 0 3610 Length of exposure (days) 14 25 50 75 Animals with deformities (percent) 100 0 Blaustein’s UV-B experiment.In the group of salamanders whose eggs were protected from UV-B radiation, hatching rates were higher and deformity rates were lower. 571 28 Dynamics of Ecosystems Concept Outline 28.1 Chemicals cycle within ecosystems. The Water Cycle. Water cycles between the atmosphere and the oceans, although deforestation has broken the cycle in some ecosystems. The Carbon Cycle. Photosynthesis captures carbon from the atmosphere; respiration returns it. The Nitrogen Cycle. Nitrogen is captured from the atmosphere by the metabolic activities of bacteria; other bacteria degrade organic nitrogen, returning it to the atmosphere. The Phosphorus Cycle. Of all nutrients that plants require, phosphorus tends to be the most limiting. Biogeochemical Cycles Illustrated: Recycling in a Forest Ecosystem. In a classic experiment, the role of forests in retaining nutrients is assessed. 28.2 Ecosystems are structured by who eats whom. Trophic Levels. Energy passes through ecosystems in a limited number of steps, typically three or four. 28.3 Energy flows through ecosystems. Primary Productivity. Plants produce biomass by photosynthesis, while animals produce biomass by consuming plants or other animals. The Energy in Food Chains. As energy passes through an ecosystem, a good deal is lost at each step. Ecological Pyramids. The biomass of a trophic level is less, the farther it is from the primary production of photosynthesizers. Interactions among Different Trophic Levels. Processes on one trophic level can have effects on higher or lower levels of the food chain. 28.4 Biodiversity promotes ecosystem stability. Effects of Species Richness. Species-rich communities are more productive and resistant to disturbance. Causes of Species Richness. Ecosystem productivity, spatial heterogeneity, and climate all affect the number of species in an ecosystem. Biogeographic Patterns of Species Diversity. Many more species occur in the tropics than in temperate regions. Island Biogeography. Species richness on islands may be a dynamic equilibrium between extinction and colonization. T he earth is a closed system with respect to chemicals, but an open system in terms of energy. Collectively, the organisms in ecosystems regulate the capture and ex- penditure of energy and the cycling of chemicals (figure 28.1). As we will see in this chapter, all organisms, includ- ing humans, depend on the ability of other organisms— plants, algae, and some bacteria—to recycle the basic com- ponents of life. In chapter 29, we consider the many different types of ecosystems that constitute the biosphere. Chapters 30 and 31 then discuss the many threats to the biosphere and the species it contains. FIGURE 28.1 Mushrooms serve a greater function than haute cuisine. Mushrooms and other organisms are crucial recyclers in ecosystems, breaking down dead and decaying material and releasing critical elements such as carbon and nitrogen back into nutrient cycles. The Water Cycle The water cycle (figure 28.2) is the most familiar of all bio- geochemical cycles. All life depends directly on the pres- ence of water; the bodies of most organisms consist mainly of this substance. Water is the source of hydrogen ions, whose movements generate ATP in organisms. For that reason alone, it is indispensable to their functioning. The Path of Free Water The oceans cover three-fourths of the earth’s surface. From the oceans, water evaporates into the atmosphere, a process powered by energy from the sun. Over land approximately 90% of the water that reaches the atmosphere is moisture that evaporates from the surface of plants through a process called transpiration (see chapter 40). Most precipitation falls directly into the oceans, but some falls on land, where it passes into surface and subsurface bodies of fresh water. Only about 2% of all the water on earth is captured in any form—frozen, held in the soil, or incorporated into the bodies of organisms. All of the rest is free water, circulating between the atmosphere and the oceans. 572 Part VIII The Global Environment All of the chemical elements that occur in organisms cycle through ecosystems in biogeochemical cycles, cyclical paths involving both biological and chemical processes. On a global scale, only a very small portion of these substances is contained within the bodies of organisms; almost all ex- ists in nonliving reservoirs: the atmosphere, water, or rocks. Carbon (in the form of carbon dioxide), nitrogen, and oxy- gen enter the bodies of organisms primarily from the at- mosphere, while phosphorus, potassium, sulfur, magne- sium, calcium, sodium, iron, and cobalt come from rocks. All organisms require carbon, hydrogen, oxygen, nitrogen, phosphorus, and sulfur in relatively large quantities; they require other elements in smaller amounts. The cycling of materials in ecosystems begins when these chemicals are incorporated into the bodies of organ- isms from nonliving reservoirs such as the atmosphere or the waters of oceans or rivers. Many minerals, for example, first enter water from weathered rock, then pass into or- ganisms when they drink the water. Materials pass from the organisms that first acquire them into the bodies of other organisms that eat them, until ultimately, through decom- position, they complete the cycle and return to the nonliv- ing world. 28.1 Chemicals cycle within ecosystems. Lakes Runoff Percolation in soil Evaporation Transpiration Precipitation Oceans Solar energy Groundwater Aquifer FIGURE 28.2 The water cycle.Water circulates from atmosphere to earth and back again. The Importance of Water to Organisms Organisms live or die on the basis of their ability to capture water and incorporate it into their bodies. Plants take up water from the earth in a continuous stream. Crop plants require about 1000 kilograms of water to produce one kilo- gram of food, and the ratio in natural communities is simi- lar. Animals obtain water directly or from the plants or other animals they eat. The amount of free water available at a particular place often determines the nature and abun- dance of the living organisms present there. Groundwater Much less obvious than surface water, which we see in streams, lakes, and ponds, is groundwater, which occurs in aquifers—permeable, saturated, underground layers of rock, sand, and gravel. In many areas, groundwater is the most important reservoir of water. It amounts to more than 96% of all fresh water in the United States. The upper, unconfined portion of the groundwater consti- tutes the water table, which flows into streams and is partly accessible to plants; the lower confined layers are generally out of reach, although they can be “mined” by humans. The water table is recharged by water that per- colates through the soil from precipitation as well as by water that seeps downward from ponds, lakes, and streams. The deep aquifers are recharged very slowly from the water table. Groundwater flows much more slowly than surface water, anywhere from a few millimeters to a meter or so per day. In the United States, groundwater provides about 25% of the water used for all purposes and provides about 50% of the population with drinking water. Rural areas tend to depend almost exclusively on wells to access groundwater, and its use is growing at about twice the rate of surface water use. In the Great Plains of the central United States, the extensive use of the Ogallala Aquifer as a source of water for agricultural needs as well as for drink- ing water is depleting it faster than it can be naturally recharged. This seriously threatens the agricultural produc- tion of the area and similar problems are appearing throughout the drier portions of the globe. Because of the greater rate of groundwater use, and be- cause it flows so slowly, the increasing chemical pollution of groundwater is also a very serious problem. It is esti- mated that about 2% of the groundwater in the United States is already polluted, and the situation is worsening. Pesticides, herbicides, and fertilizers have become a serious threat to water purity. Another key source of groundwater pollution consists of the roughly 200,000 surface pits, ponds, and lagoons that are actively used for the disposal of chemical wastes in the United States alone. Because of the large volume of water, its slow rate of turnover, and its in- accessibility, removing pollutants from aquifers is virtually impossible. Breaking the Water Cycle In dense forest ecosystems such as tropical rainforests, more than 90% of the moisture in the ecosystem is taken up by plants and then transpired back into the air. Because so many plants in a rainforest are doing this, the vegetation is the primary source of local rainfall. In a very real sense, these plants create their own rain: the moisture that travels up from the plants into the atmosphere falls back to earth as rain. Where forests are cut down, the organismic water cycle is broken, and moisture is not returned to the atmos- phere. Water drains away from the area to the sea instead of rising to the clouds and falling again on the forest. As early as the late 1700s, the great German explorer Alexan- der von Humbolt reported that stripping the trees from a tropical rainforest in Colombia prevented water from re- turning to the atmosphere and created a semiarid desert. It is a tragedy of our time that just such a transformation is occurring in many tropical areas, as tropical and tem- perate rainforests are being clear-cut or burned in the name of “development” (figure 28.3). Much of Madagas- car, a California-sized island off the east coast of Africa, has been transformed in this century from lush tropical forest into semiarid desert by deforestation. Because the rain no longer falls, there is no practical way to reforest this land. The water cycle, once broken, cannot be easily reestablished. Water cycles between oceans and atmosphere. Some 96% of the fresh water in the United States consists of groundwater, which provides 25% of all the water used in this country. Chapter 28 Dynamics of Ecosystems 573 FIGURE 28.3 Deforestation breaks the water cycle.As time goes by, the consequences of tropical deforestation may become even more severe, as the extensive erosion in this deforested area of Madagascar shows. The Carbon Cycle The carbon cycle is based on carbon dioxide, which makes up only about 0.03% of the atmosphere (figure 28.4). Worldwide, the synthesis of organic compounds from car- bon dioxide and water through photosynthesis (see chapter 10) utilizes about 10% of the roughly 700 billion metric tons of carbon dioxide in the atmosphere each year. This enormous amount of biological activity takes place as a re- sult of the combined activities of photosynthetic bacteria, protists, and plants. All terrestrial heterotrophic organisms obtain their carbon indirectly from photosynthetic organ- isms. When the bodies of dead organisms decompose, mi- croorganisms release carbon dioxide back to the atmo- sphere. From there, it can be reincorporated into the bodies of other organisms. Most of the organic compounds formed as a result of carbon dioxide fixation in the bodies of photosynthetic or- ganisms are ultimately broken down and released back into the atmosphere or water. Certain carbon-containing compounds, such as cellulose, are more resistant to break- down than others, but certain bacteria and fungi, as well as a few kinds of insects, are able to accomplish this feat. Some cellulose, however, accumulates as undecomposed organic matter such as peat. The carbon in this cellulose may eventually be incorporated into fossil fuels such as oil or coal. In addition to the roughly 700 billion metric tons of car- bon dioxide in the atmosphere, approximately 1 trillion metric tons are dissolved in the ocean. More than half of this quantity is in the upper layers, where photosynthesis takes place. The fossil fuels, primarily oil and coal, contain more than 5 trillion additional metric tons of carbon, and between 600 million and 1 trillion metric tons are locked up in living organisms at any one time. In global terms, photosynthesis and respiration (see chapters 9 and 10) are approximately balanced, but the balance has been shifted recently because of the consumption of fossil fuels. The combustion of coal, oil, and natural gas has released large stores of carbon into the atmosphere as carbon dioxide. The increase of carbon dioxide in the atmosphere appears to be changing global climates, and may do so even more rapidly in the future, as we will discuss in chapter 30. About 10% of the estimated 700 billion metric tons of carbon dioxide in the atmosphere is fixed annually by the process of photosynthesis. 574 Part VIII The Global Environment CO 2 in atmosphere Diffusion Respiration Photosynthesis Photosynthesis Plants and algae Plants Animals Death and decay Industry and home Combustion of fuels Animals Carbonates in sediment Bicarbonates Death Fossil fuels (oil, gas, coal) Dissolved CO 2 FIGURE 28.4 The carbon cycle.Photosynthesis captures carbon; respiration returns it to the atmosphere. The Nitrogen Cycle Relatively few kinds of organisms—all of them bacteria— can convert, or fix, atmospheric nitrogen (78% of the earth’s atmosphere) into forms that can be used for biologi- cal processes via the nitrogen cycle (figure 28.5). The triple bond that links together the two atoms that make up diatomic atmospheric nitrogen (N 2 ) makes it a very stable molecule. In living systems the cleavage of atmospheric ni- trogen is catalyzed by a complex of three proteins—ferre- doxin, nitrogen reductase, and nitrogenase. This process uses ATP as a source of energy, electrons derived from photosynthesis or respiration, and a powerful reducing agent. The overall reaction of nitrogen fixation is written: N 2 + 3H 2 →2NH 3 Some genera of bacteria have the ability to fix atmo- spheric nitrogen. Most are free-living, but some form sym- biotic relationships with the roots of legumes (plants of the pea family, Fabaceae) and other plants. Only the symbiotic bacteria fix enough nitrogen to be of major significance in nitrogen production. Because of the activities of such organ- isms in the past, a large reservoir of ammonia and nitrates now exists in most ecosystems. This reservoir is the imme- diate source of much of the nitrogen used by organisms. Nitrogen-containing compounds, such as proteins in plant and animal bodies, are decomposed rapidly by certain bacteria and fungi. These bacteria and fungi use the amino acids they obtain through decomposition to synthesize their own proteins and to release excess nitrogen in the form of ammonium ions (NH 4 + ), a process known as am- monification. The ammonium ions can be converted to soil nitrites and nitrates by certain kinds of organisms and which then can be absorbed by plants. A certain proportion of the fixed nitrogen in the soil is steadily lost. Under anaerobic conditions, nitrate is often converted to nitrogen gas (N 2 ) and nitrous oxide (N 2 O), both of which return to the atmosphere. This process, which several genera of bacteria carry out, is called denitrification. Nitrogen becomes available to organisms almost entirely through the metabolic activities of bacteria, some free-living and others which live symbiotically in the roots of legumes and other plants. Chapter 28 Dynamics of Ecosystems 575 Birds Herbivores Plants Amino acids Carnivores Atmospheric nitrogen Loss to deep sediments Fish Plankton with nitrogen-fixing bacteria Nitrogen-fixing bacteria (plant roots) Nitrogen-fixing bacteria (soil) Denitrifying bacteria Death, excretion, feces Decomposing bacteria Ammonifying bacteria Nitrifying bacteria Soil nitrates FIGURE 28.5 The nitrogen cycle.Certain bacteria fix atmospheric nitrogen, converting it to a form living organisms can use. Other bacteria decompose nitrogen-containing compounds from plant and animal materials, returning it to the atmosphere. The Phosphorus Cycle In all biogeochemical cycles other than those involving water, carbon, oxygen, and nitrogen, the reservoir of the nutrient exists in mineral form, rather than in the atmo- sphere. The phosphorus cycle (figure 28.6) is presented as a representative example of all other mineral cycles. Phos- phorus, a component of ATP, phospholipids, and nucleic acid, plays a critical role in plant nutrition. Of all the required nutrients other than nitrogen, phos- phorus is the most likely to be scarce enough to limit plant growth. Phosphates, in the form of phosphorus anions, exist in soil only in small amounts. This is because they are relatively insoluble and are present only in certain kinds of rocks. As phosphates weather out of soils, they are trans- ported by rivers and streams to the oceans, where they ac- cumulate in sediments. They are naturally brought back up again only by the uplift of lands, such as occurs along the Pacific coast of North and South America, creating up- welling currents. Phosphates brought to the surface are as- similated by algae, and then by fish, which are in turn eaten by birds. Seabirds deposit enormous amounts of guano (feces) rich in phosphorus along certain coasts. Guano de- posits have traditionally been used for fertilizer. Crushed phosphate-rich rocks, found in certain regions, are also used for fertilizer. The seas are the only inexhaustible source of phosphorus, making deep-seabed mining look in- creasingly commercially attractive. Every year, millions of tons of phosphate are added to agricultural lands in the belief that it becomes fixed to and enriches the soil. In general, three times more phosphate than a crop requires is added each year. This is usually in the form of superphosphate, which is soluble calcium di- hydrogen phosphate, Ca(H 2 PO 4 ) 2 , derived by treating bones or apatite, the mineral form of calcium phosphate, with sulfuric acid. But the enormous quantities of phos- phates that are being added annually to the world’s agricul- tural lands are not leading to proportionate gains in crops. Plants can apparently use only so much of the phosphorus that is added to the soil. Phosphates are relatively insoluble and are present in most soils only in small amounts. They often are so scarce that their absence limits plant growth. 576 Part VIII The Global Environment Loss to deep sediment Rocks and minerals Soluble soil phosphate Plants and algae Plants Urine Land animals Precipitates Aquatic animals Animal tissue and feces Animal tissue and feces Decomposers (bacteria and fungi) Decomposers (bacteria and fungi) Phosphates in solution Loss in drainage FIGURE 28.6 The phosphorus cycle.Phosphates weather from soils into water, enter plants and animals, and are redeposited in the soil when plants and animals decompose. Biogeochemical Cycles Illustrated: Recycling in a Forest Ecosystem An ongoing series of studies conducted at the Hubbard Brook Experimental Forest in New Hampshire has re- vealed in impressive detail the overall recycling pattern of nutrients in an ecosystem. The way this particular ecosys- tem functions, and especially the way nutrients cycle within it, has been studied since 1963 by Herbert Bor- mann of the Yale School of Forestry and Environmental Studies, Gene Likens of the Institute of Ecosystem Stud- ies, and their colleagues. These studies have yielded much of the available information about the cycling of nutrients in forest ecosystems. They have also provided the basis for the development of much of the experimental methodology that is being applied successfully to the study of other ecosystems. Hubbard Brook is the central stream of a large water- shed that drains a region of temperate deciduous forest. To measure the flow of water and nutrients within the Hubbard Brook ecosystem, concrete weirs with V-shaped notches were built across six tributary streams. All of the water that flowed out of the valleys had to pass through the notches, as the weirs were anchored in bedrock. The researchers measured the precipitation that fell in the six valleys, and determined the amounts of nutrients that were present in the water flowing in the six streams. By these methods, they demonstrated that the undisturbed forests in this area were very efficient at retaining nutri- ents; the small amounts of nutrients that precipitated from the atmosphere with rain and snow were approxi- mately equal to the amounts of nutrients that ran out of the valleys. These quantities were very low in relation to the total amount of nutrients in the system. There was a small net loss of calcium—about 0.3% of the total calcium in the system per year—and small net gains of nitrogen and potassium. In 1965 and 1966, the investigators felled all the trees and shrubs in one of the six watersheds and then prevented regrowth by spraying the area with herbicides. The effects were dramatic. The amount of water running out of that valley increased by 40%. This indicated that water that previously would have been taken up by vegetation and ul- timately evaporated into the atmosphere was now running off. For the four-month period from June to September 1966, the runoff was four times higher than it had been during comparable periods in the preceding years. The amounts of nutrients running out of the system also greatly increased; for example, the loss of calcium was 10 times higher than it had been previously. Phosphorus, on the other hand, did not increase in the stream water; it appar- ently was locked up in the soil. The change in the status of nitrogen in the disturbed valley was especially striking (figure 28.7). The undis- turbed ecosystem in this valley had been accumulating ni- trogen at a rate of about 2 kilograms per hectare per year, but the deforested ecosystem lost nitrogen at a rate of about 120 kilograms per hectare per year. The nitrate level of the water rapidly increased to a level exceeding that judged safe for human consumption, and the stream that drained the area generated massive blooms of cyanobacteria and algae. In other words, the fertility of this logged-over valley decreased rapidly, while at the same time the danger of flooding greatly increased. This experiment is particularly instructive at the start of the twenty-first century, as large areas of tropical rain forest are being destroyed to make way for cropland, a topic that will be discussed further in chapter 30. When the trees and shrubs in one of the valleys in the Hubbard Brook watershed were cut down and the area was sprayed with herbicide, water runoff and the loss of nutrients from that valley increased. Nitrogen, which had been accumulating at a rate of about 2 kilograms per hectare per year, was lost at a rate of 120 kilograms per hectare per year. Chapter 28 Dynamics of Ecosystems 577 1965 1966 Year 2 0 4 40 80 Amount of nitrate (mg/ l ) 1967 1968 Deforestation (a) (b) FIGURE 28.7 The Hubbard Brook experiment.(a) A 38-acre watershed was completely deforested, and the runoff monitored for several years. (b) Deforestation greatly increased the loss of minerals in runoff water from the ecosystem. The red curve represents nitrate in the runoff water from the deforested watershed; the blue curve, nitrate in runoff water from an undisturbed neighboring watershed. Trophic Levels An ecosystem includes autotrophs and heterotrophs. Au- totrophs are plants, algae, and some bacteria that are able to capture light energy and manufacture their own food. To support themselves, heterotrophs, which include ani- mals, fungi, most protists and bacteria, and nongreen plants, must obtain organic molecules that have been syn- thesized by autotrophs. Autotrophs are also called primary producers,and heterotrophs are also called consumers. Once energy enters an ecosystem, usually as the result of photosynthesis, it is slowly released as metabolic processes proceed. The autotrophs that first acquire this energy pro- vide all of the energy heterotrophs use. The organisms that make up an ecosystem delay the release of the energy ob- tained from the sun back into space. Green plants, the primary producers of a terrestrial ecosystem, generally capture about 1% of the energy that falls on their leaves, converting it to food energy. In espe- cially productive systems, this percentage may be a little higher. When these plants are consumed by other organ- isms, only a portion of the plant’s accumulated energy is actually converted into the bodies of the organisms that consume them. Several different levels of consumers exist. The primary consumers, or herbivores, feed directly on the green plants. Secondary consumers, carnivores and the parasites of animals, feed in turn on the herbivores. Decomposers break down the organic matter accumulated in the bodies of other organisms. Another more general term that in- cludes decomposers is detritivores.Detritivores live on the refuse of an ecosystem. They include large scavengers, such as crabs, vultures, and jackals, as well as decomposers. All of these categories occur in any ecosystem. They represent different trophic levels, from the Greek word trophos, which means “feeder.” Organisms from each trophic level, feeding on one another, make up a series called a food chain (figure 28.8). The length and complex- ity of food chains vary greatly. In real life, it is rather rare for a given kind of organism to feed only on one other type of organism. Usually, each organism feeds on two or more kinds and in turn is eaten by several other kinds of organ- isms. When diagrammed, the relationship appears as a se- ries of branching lines, rather than a straight line; it is called a food web(figure 28.9). A certain amount of the chemical-bond energy ingested by the organisms at a given trophic level goes toward stay- ing alive (for example, carrying out mechanical motion). Using the chemical-bond energy converts it to heat, which organisms cannot use to do work. Another portion of the chemical-bond energy taken in is retained as chemical- bond energy within the organic molecules produced by growth. Usually 40% or less of the energy ingested is stored by growth. An invertebrate typically uses about a quarter of this 40% for growth; in other words, about 10% of the food an invertebrate eats is turned into its own body and thus into potential food for its predators. Although the comparable figure varies from approximately 5% in carni- vores to nearly 20% for herbivores, 10% is a good average value for the amount of organic matter that reaches the next trophic level. Energy passes through ecosystems, a good deal being lost at each step. 578 Part VIII The Global Environment 28.2 Ecosystems are structured by who eats whom. Bacteria Fungi Trophic level 4 Trophic level 3 Trophic level 2 Trophic level 1 Detritivores Producer Primary consumer Secondary consumer Tertiary consumer Top carnivore Carnivore Herbivore Sun FIGURE 28.8 Trophic levels within a food chain.Plants obtain their energy directly from the sun, placing them at trophic level 1. Animals that eat plants, such as grasshoppers, are primary consumers or herbivores and are at trophic level 2. Animals that eat plant-eating animals, such as shrews, are carnivores and are at trophic level 3 (secondary consumers); animals that eat carnivorous animals, such as hawks, are tertiary consumers at trophic level 4. Detritivores use all trophic levels for food. Chapter 28 Dynamics of Ecosystems 579 Birds of prey Birds BirdsMammals Mammals Arthropods Fish Algae Mollusks Annelids Meiofauna Bacteria and fungi Inorganic nutrients Humans Top carnivores Carnivores Herbivores Photosynthesizers Decomposers Inorganic nutrients Inorganic nutrients FIGURE 28.9 The food web in a salt marsh shows the complex interrelationships among organisms.The meiofauna are very small animals that live between the grains of sand. Primary Productivity Approximately 1 to 5% of the solar energy that falls on a plant is converted to the chemical bonds of organic mate- rial. Primary production or primary productivity are terms used to describe the amount of organic matter pro- duced from solar energy in a given area during a given pe- riod of time. Gross primary productivity is the total or- ganic matter produced, including that used by the photosynthetic organism for respiration. Net primary productivity (NPP), therefore, is a measure of the amount of organic matter produced in a community in a given time that is available for heterotrophs. It equals the gross primary productivity minus the amount of energy expended by the metabolic activities of the photosynthetic organisms. The net weight of all of the organisms living in an ecosystem, its biomass, increases as a result of its net production. Productive Biological Communities Some ecosystems have a high net primary productivity. For example, tropical forests and wetlands normally produce between 1500 and 3000 grams of organic material per square meter per year. By contrast, corresponding figures for other communities include 1200 to 1300 grams for temperate forests, 900 grams for savanna, and 90 grams for deserts (table 28.1). Secondary Productivity The rate of production by heterotrophs is called sec- ondary productivity. Because herbivores and carnivores cannot carry out photosynthesis, they do not manufac- ture biomolecules directly from CO 2 . Instead, they ob- tain them by eating plants or other heterotrophs. Sec- ondary productivity by herbivores is approximately an order of magnitude less than the primary productivity upon which it is based. Where does all the energy in plants that is not captured by herbivores go (figure 28.10)? First, much of the biomass is not consumed by herbivores and instead supports the decomposer commu- nity (bacteria, fungi and detritivorous animals). Second, some energy is not assimilated by the herbivore’s body but is passed on as feces to the decomposers. Third, not all the chemical-bond energy which herbivores assimilate is retained as chemical-bond energy in the organic mole- cules of their tissues. Some of it is lost as heat produced by work. Primary productivity occurs as a result of photosynthesis, which is carried out by green plants, algae, and some bacteria. Secondary productivity is the production of new biomass by heterotrophs. 580 Part VIII The Global Environment 28.3 Energy flows through ecosystems. 17% Growth 33% Cellular respiration 50% Feces FIGURE 28.10 How heterotrophs utilize food energy.A heterotroph assimilates only a fraction of the energy it consumes. For example, if the “bite” of a herbivorous insect comprises 500 Joules of energy (1 Joule = 0.239 calories), about 50%, 250 J, is lost in feces, about 33%, 165 J, is used to fuel cellular respiration, and about 17%, 85 J, is converted into insect biomass. Only this 85 J is available to the next trophic level. Table 28.1 Terrestrial Ecosystem Productivity Per Year Net Primary Productivity (NPP) Ecosystem NPP per Unit Area World NPP Type (g/m 2 ) (10 9 tons) Extreme desert, 3 0.07 rock, sand, and ice Desert and 90 1.6 semidesert shrub Tropical rain forest 2200 37.4 Savanna 900 13.5 Cultivated land 650 9.1 Boreal forest 800 9.6 Temperate 600 5.4 grassland Woodland and 700 6.0 shrubland Tundra and alpine 140 1.1 Tropical seasonal 1600 12.0 forest Temperate deciduous 1200 8.4 forest Temperate evergreen 1300 6.5 forest Wetlands 2000 4.0 Source:After Whittaker, 1975. The Energy in Food Chains Food chains generally consist of only three or four steps (figure 28.11). So much energy is lost at each step that very little usable energy remains in the system after it has been incorporated into the bodies of organisms at four successive trophic levels. Community Energy Budgets Lamont Cole of Cornell University studied the flow of en- ergy in a freshwater ecosystem in Cayuga Lake in upstate New York. He calculated that about 150 of each 1000 calo- ries of potential energy fixed by algae and cyanobacteria are transferred into the bodies of small heterotrophs (figure 28.12). Of these, about 30 calories are incorporated into the bodies of smelt, small fish that are the principal sec- ondary consumers of the system. If humans eat the smelt, they gain about 6 of the 1000 calories that originally en- tered the system. If trout eat the smelt and humans eat the trout, humans gain only about 1.2 calories. Factors Limiting Community Productivity Communities with higher productivity can in theory sup- port longer food chains. The limit on a community’s pro- ductivity is determined ultimately by the amount of sun- light it receives, for this determines how much photosynthesis can occur. This is why in the deciduous forests of North America the net primary productivity in- creases as the growing season lengthens. NPP is higher in warm climates than cold ones not only because of the longer growing seasons, but also because more nitrogen tends to be available in warm climates, where nitrogen- fixing bacteria are more active. Considerable energy is lost at each stage in food chains, which limits their length. In general, more productive food chains can support longer food chains. Chapter 28 Dynamics of Ecosystems 581 Primary consumerPrimary producer Secondary consumer Tertiary consumer FIGURE 28.11 A food chain. Because so much energy is lost at each step, food chains usually consist of just three or four steps. Algae and cyanobacteria Small heterotrophs Smelt Human Trout 1.2 calories 6 calories 30 calories 150 calories 1000 calories FIGURE 28.12 The food web in Cayuga Lake. Autotrophic plankton (algae and cyanobacteria) fix the energy of the sun, heterotrophic plankton feed on them, and are both consumed by smelt. The smelt are eaten by trout, with about a fivefold loss in fixed energy; for humans, the amount of smelt biomass is at least five times greater than that available in trout, although humans prefer to eat trout. Ecological Pyramids A plant fixes about 1% of the sun’s energy that falls on its green parts. The successive members of a food chain, in turn, process into their own bodies about 10% of the en- ergy available in the organisms on which they feed. For this reason, there are generally far more individuals at the lower trophic levels of any ecosystem than at the higher levels. Similarly, the biomass of the primary producers present in a given ecosystem is greater than the biomass of the pri- mary consumers, with successive trophic levels having a lower and lower biomass and correspondingly less potential energy. These relationships, if shown diagrammatically, appear as pyramids (figure 28.13). We can speak of “pyramids of biomass,” “pyramids of energy,” “pyramids of number,” and so forth, as characteristic of ecosystems. Inverted Pyramids Some aquatic ecosystems have inverted biomass pyramids. For example, in a planktonic ecosystem—dominated by small organisms floating in water—the turnover of photo- synthetic phytoplankton at the lowest level is very rapid, with zooplankton consuming phytoplankton so quickly that the phytoplankton (the producers at the base of the food chain) can never develop a large population size. Because the phytoplankton reproduce very rapidly, the community can support a population of heterotrophs that is larger in biomass and more numerous than the phytoplankton (see figure 28.13b). Top Carnivores The loss of energy that occurs at each trophic level places a limit on how many top-level carnivores a community can support. As we have seen, only about one-thousandth of the energy captured by photosynthesis passes all the way through a three-stage food chain to a tertiary consumer such as a snake or hawk. This explains why there are no predators that subsist on lions or eagles—the biomass of these animals is simply insufficient to support another trophic level. In the pyramid of numbers, top-level predators tend to be fairly large animals. Thus, the small residual biomass available at the top of the pyramid is concentrated in a rela- tively small number of individuals. Because energy is lost at every step of a food chain, the biomass of primary producers (photosynthesizers) tends to be greater than that of the herbivores that consume them, and herbivore biomass greater than the biomass of the predators that consume them. 582 Part VIII The Global Environment (c) (b) (a) Plankton (36,380 kilocalories/square meter/year) Plankton (807 grams/square meter) Plankton (4,000,000,000) 11 1 Carnivore Herbivore Decomposer (3890 kilocalories/ square meter/year) Decomposer (5 grams/ square meter) Phytoplankton (4 grams/square meter) Zooplankton and bottom fauna (21 grams/square meter) First-level carnivore (48 kilocalories/ square meter/year) Herbivore (596 kilocalories/ square meter/year) Herbivore (37 grams/square meter) First-level carnivore (11 grams/square meter) Second-level carnivore (1.5 grams/square meter) Pyramid of energy Pyramid of biomass Pyramid of numbers FIGURE 28.13 Ecological pyramids.Ecological pyramids measure different characteristics of each trophic level. (a) Pyramid of numbers. (b) Pyramids of biomass, both normal (top) and inverted (bottom). (c) Pyramid of energy. Interactions among Different Trophic Levels The existence of food webs creates the possibility of inter- actions among species at different trophic levels. Predators will not only have effects on the species upon which they prey, but also, indirectly, upon the plants eaten by these prey. Conversely, increases in primary productivity will not only provide more food for herbivores but, indirectly, lead also to more food for carnivores. Trophic Cascades When we look at the world around us, we see a profusion of plant life. Why is this? Why don’t herbivore populations increase to the extent that all available vegetation is con- sumed? The answer, of course, is that predators keep the herbivore populations in check, thus allowing plant popula- tions to thrive. This phenomenon, in which the effect of one trophic level flows down to lower levels, is called a trophic cascade. Experimental studies have confirmed the existence of trophic cascades. For example, in one study in New Zealand, sections of a stream were isolated with a mesh that prevented fish from entering. In some of the enclosures, brown trout were added, whereas other enclosures were left without large fish. After 10 days, the number of inverte- brates in the trout enclosures was one-half of that in the controls (figure 28.14). In turn, the biomass of algae, which invertebrates feed upon, was five times greater in the trout enclosures than in the controls. The logic of trophic cascades leads to the prediction that a fourth trophic level, carnivores that preyed on other car- nivores, would also lead to cascading effects. In this case, the top predators would keep lower-level predator popula- tions in check, which should lead to a profusion of herbi- vores and a paucity of vegetation. In an experiment similar to the one just described, enclosures were created in free- flowing streams in northern California. In this case, large predatory fish were added to some enclosures and not oth- ers. In the large fish enclosures, the number of smaller predators, such as damselfly nymphs was greatly reduced, leading to an increase in their prey, including algae-eating insects, which lead, in turn, to decreases in the biomass of algae (figure 28.15). Chapter 28 Dynamics of Ecosystems 583 Fish added No fish added Damselflies (number/m 2 ) Chironomids (number/g algae) Algae (g/m 2 ) Sample 1 (June 5) Sample 2 (June 22) 300 200 100 0 60 50 40 30 20 10 0 5000 4000 3000 2000 1000 0 ? ? ? ? ? ? ? ? ? ? ? ? ? ? FIGURE 28.14 Trophic cascades.Streams with trout have fewer herbivorous invertebrates and more algae than streams without trout. No fish Trout No fish Trout Invertebrates (number/m 2 ) 5000 4000 3000 2000 1000 0 2.0 1.5 1.0 0.5 0 Algae ( H9262 g chlorophyll a /cm 2 ) FIGURE 28.15 Four-level trophic cascades.Streams with fish have fewer lower- level predators, such as damselflies, more herbivorous insects (exemplified by the number of chironomids, a type of aquatic insect), and lower levels of algae. Human Effects on Trophic Cascades Humans have inadvertently created a test of the trophic cascade hypothesis by removing top predators from ecosys- tems. The great naturalist Aldo Leopold captured the re- sults long before the trophic cascade hypothesis had ever been scientifically articulated when he wrote in the Sand County Almanac: “I have lived to see state after state extirpate its wolves. I have watched the face of many a new wolfless mountain, and seen the south-facing slopes wrinkle with a maze of new deer trails. I have seen every edible bush and seedling browsed, first to anemic desuetude, and then to death. I have seen every edible tree defoliated to the height of a saddle horn.” Many similar examples exist in nature in which the re- moval of predators has led to cascading effects on lower trophic levels. On Barro Colorado Island, a hilltop turned into an island by the construction of the Panama Canal at the beginning of the last century, large predators such as jaguars and mountain lions are absent. As a result, smaller predators whose populations are normally held in check— including monkeys, peccaries (a relative of the pig), coat- imundis and armadillos—have become extraordinarily abundant. These animals will eat almost anything they find. Ground-nesting birds are particularly vulnerable, and many species have declined; at least 15 bird species have vanished from the island entirely. Similarly, in woodlots in the mid- western United States, raccoons, opossums, and foxes have become abundant due to the elimination of larger preda- tors, and populations of ground-nesting birds have declined greatly. Bottom-Up Effects Conversely, factors acting at the bottom of food webs may have consequences that ramify to higher trophic levels, leading to what are termed bottom-up effects. The basic idea is when the productivity of an ecosystem is low, her- bivore populations will be too small to support any preda- tors. Increases in productivity will be entirely devoured by the herbivores, whose populations will increase in size. At some point, herbivore populations will become large enough that predators can be supported. Thus, further in- creases in productivity will not lead to increases in herbi- vore populations, but, rather to increases in predator pop- ulations. Again, at some level, top predators will become established that can prey on lower-level predators. With the lower-level predator populations in check, herbivore populations will again increase with increasing productiv- ity (figure 28.16). Experimental evidence for the role of bottom-up ef- fects was provided in an elegant study conducted on the Eel River in northern California. Enclosures were con- structed that excluded large fish. A roof was placed above each enclosure. Some roofs were clear and let light pass 584 Part VIII The Global Environment Higher level predators Lower level predators Herbivores V egetation Productivity FIGURE 28.16 Bottom-up effects.At low levels of productivity, herbivore populations cannot be maintained. Above some threshold, increases in productivity lead to increases in herbivore biomass; vegetation biomass no longer increases with productivity because it is converted into herbivore biomass. Similarly, above another threshold, herbivore biomass gets converted to carnivore biomass. At this point, vegetation biomass is no longer constrained by herbivores, and so again increases with increasing productivity. through, whereas others produced light or deep shade. The result was that the enclosures differed in the amount of sunlight reaching them. As one might expect, the pri- mary productivity differed and was greatest in the un- shaded enclosures. This increased productivity led to both more vegetation and more predators, but the trophic level sandwiched in between, the herbivores, did not increase, precisely as the bottom-up hypothesis pre- dicted (figure 28.17). Relative Importance of Trophic Cascades and Bottom-Up Effects Neither trophic cascades nor bottom-up effects are in- evitable. For example, if two species of herbivores exist in an ecosystem and compete strongly, and if one species is much more vulnerable to predation than the other, then top-down effects will not propagate to the next lower trophic level. Rather, increased predation will simply de- crease the population of the vulnerable species while in- creasing the population of its competitor, with potentially no net change on the vegetation in the next lower trophic level. Similarly, productivity increases might not move up through all trophic levels. In some cases, for example, prey populations increase so quickly that their predators cannot control them. In such cases, increases in productivity would not move up the food chain. In other cases, trophic cascades and bottom-up effects may reinforce each other. In one experiment, large fish were removed from one lake, leaving only minnows, which ate most of the algae-eating zooplankton. By contrast, in the other lake, there were few minnows and much zoo- plankton. The researchers then added nutrients to both lakes. In the minnow lake, there were few zooplankton, so the resulting increase in algal productivity did not propa- gate up the food chain and large mats of algae formed. By comparison, in the large fish lake, increased productivity moved up the food chain and algae populations were con- trolled. In this case, both top-down and bottom-up processes were operating. Nature, of course, is not always so simple. In some cases, species may simultaneously operate on multiple trophic levels, such as the jaguar which eats both smaller carnivores and herbivores, or the bear which eats both fish and berries. Nature is often much more complicated than a simple, linear food chain, as figure 28.9 indicates. Ecolo- gists are currently working to apply theories of food chain interactions to these more complicated situations. Because of the linked nature of food webs, species on different trophic levels will effect each other, and these effects can promulgate both up and down the food web. Chapter 28 Dynamics of Ecosystems 585 ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ??? ? ? ? ? ? ? ? ? 1.2 1.0 0.8 0.6 0.4 0.2 0 0 300 600 900 1200 1500 Predator biomass(g/m 2 ) 8 6 4 2 0 6 2 4 8 10 12 0 300 600 900 1200 1500 0 0 300 600 900 1200 1500 Herbivore biomass (g/m 2 ) Productivity (H9262mol light/m 2 /s) V egetation biomass (g algae/m 2 ) FIGURE 28.17 Bottom-up effects on a stream ecosystem.As predicted, increases in productivity—which are a function of the amount of light hitting the stream and leading to photosynthesis—lead to increases in the amount of vegetation. However, herbivore biomass does not increase with increased productivity because it is converted into predator biomass. Effects of Species Richness Ecologists have long debated what are the consequences of differences in species richness among communities. One theory is that more species-rich communities are more sta- ble; that is, more constant in composition and better able to resist disturbance. This hypothesis has been elegantly studied by David Tilman and colleagues at the University of Minnesota’s Cedar Creek Natural History Area. These workers monitored 207 small rectangular plots of land (8 to 16 m 2 ) for 11 years. In each plot, they counted the number of prairie plant species and measured the total amount of plant biomass (that is, the mass of all plants on the plot). Over the course of the study, plant species richness was re- lated to community stability—plots with more species showed less year-to-year variation in biomass (figure 28.18). Moreover, in two drought years, the decline in bio- mass was negatively related to species richness; in other words, plots with more species were less affected. In a re- lated experiment, when seeds of other plant species were added to different plots, the ability of these species to be- come established was negatively related to species richness. More diverse communities, in other words, are more resis- tant to invasion by new species, another measure of com- munity stability. Species richness may also have effects on other ecosys- tem processes. In a follow-up study, Tilman established an- other 147 plots in which they experimentally varied the number of plant species. Each of the plots was monitored to estimate how much growth was occurring and how much nitrogen the growing plants were taking up from the soil. Tilman found that the more species a plot had, the greater nitrogen uptake and total amount of biomass pro- duced. In his study, increased biodiversity clearly leads to greater productivity (figure 28.19). Laboratory studies on artificial ecosystems have pro- vided similar results. In one elaborate study, ecosystems covering 1 m 2 were constructed in growth chambers that controlled temperature, light levels, air currents, and at- mospheric gas concentrations. A variety of plants, insects, and other animals were introduced to construct ecosys- tems composed of 9, 15, or 31 species with the lower di- versity treatments containing a subset of the species in the higher diversity enclosures. As with Tilman’s experi- ments, the amount of biomass produced was related to species richness, as was the amount of carbon dioxide consumed, a measure of respiration occurring in the ecosystem. Tilman’s conclusion that healthy ecosystems depend on diversity is not accepted by all ecologists. Critics ques- tion the validity and relevance of these biodiversity stud- ies, claiming their experimental design is critically flawed. Tilman’s Cedar Creek result was a statistical arti- fact, they argue—the more species you add to a mix, the greater the probability that you will add a highly produc- tive one. Adding taller or highly productive plants of course increases productivity, they explain. To show a real benefit from diversity, experimental plots would have to exhibit “overyielding”—plot productivity would have to be greater than that of the single most productive species grown in isolation. The long-simmering debate continues. Controversial experimental field studies support the hypothesis that species-rich communities are more stable. 586 Part VIII The Global Environment 28.4 Biodiversity promotes ecosystem stability. Average species richness V ariation in biomass 0 2 4 6 8 10121416182022 ? ?? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ?? ? ? ? ? ? ? ? FIGURE 28.18 Effect of species richness on ecosystem stability. In the Cedar Creek experimental fields, each square is a 100-square-foot experimental plot. Experimental plots with more plant species seem to show less variation in the total amount of biomass produced, and thus more community stability. ? ? ? ? ? ? ? Species richness Nitrogen in rooting zone (mg/kg) 0 5 10 15 20 25 0.10 0.15 0.20 0.25 0.30 0.35 0.40 FIGURE 28.19 Effect of species richness on productivity.In Tilman’s experimental studies, plots with more species took up more nitrogen from the soil, leaving less in the rooting zone. The increased amount of nitrogen absorption is an indicator of increased growth, increased biomass, and thus increased productivity. Causes of Species Richness While ecologists still argue about why some ecosystems are more stable than others—better able to avoid permanent change and return to normal after disturbances like land clearing, fire, invasion by plagues of insects, or severe storm damage—most ecologists now accept as a working hypothesis that biologically diverse ecosystems are gener- ally more stable than simple ones. Ecosystems with many different kinds of organisms support a more complex web of interactions, and an alternative niche is thus more likely to exist to compensate for the effect of a disruption. Factors Promoting Species Richness How does the number of species in a community affect the functioning of the ecosystem? How does ecosystem functioning affect the number of species in a community? It is often extremely difficult to sort out the relative con- tributions of different factors. With regard to determi- nants of species richness in a community, of the many variables that may play a role, we will discuss three: ecosystem productivity, spatial heterogeneity, and cli- mate. Two additional factors that may play an important role, the evolutionary age of the community and the de- gree to which the community has been disturbed, will be examined later in this chapter. Ecosystem Productivity. Ecosystems differ in produc- tivity, which is a measure of how much new growth they can produce. Surprisingly, the relationship between pro- ductivity and species richness is not linear. Rather, ecosys- tems with intermediate levels of productivity tend to have the most species (figure 28.20). Why this is so is a topic of considerable current debate. One possibility is that levels of productivity are linked to numbers of predators. At low productivity, there are few predators and superior competi- tors eliminate most species, whereas at high productivity, there are so many predators that only the most predation- resistant species survive. At intermediate levels, however, predators may act as keystone species, maintaining species richness. Spatial Heterogeneity. Environments that are more spatially heterogeneous—that contain more soil types, topographies, and other habitat variations—can be ex- pected to accommodate more species because they provide a greater variety of microhabitats, microclimates, places to hide from predators, and so on. In general, the species rich- ness of animals tends to reflect the species richness of the plants in their community, while plant species richness re- flects the spatial heterogeneity of the ecosystem. The plants provide a biologically derived spatial heterogeneity of microhabitats to the animals. Thus, the number of lizard species in the American Southwest mirrors the structural diversity of the plants (figure 28.21). Climate. The role of climate is more difficult to assess. On the one hand, more species might be expected to coex- ist in a seasonal environment than in a constant one, be- cause a changing climate may favor different species at dif- ferent times of the year. On the other hand, stable environments are able to support specialized species that would be unable to survive where conditions fluctuate. Thus, the number of mammal species along the west coast of North America increases as the temperature range de- creases (figure 28.22). Species richness promotes ecosystem productivity and is fostered by spatial heterogeneity and stable climate. Chapter 28 Dynamics of Ecosystems 587 Productivity (amount of biomass produced) Species richness of South African mountainous vegetation 30 20 10 0 0 100 200 300 400 ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? ? FIGURE 28.20 Productivity. In fynbos plant communities of mountainous areas of South Africa, species richness of plants peaks at intermediate levels of productivity (biomass). Plant structural complexity 0.10 0.2 0.3 0.4 0.5 0.6 0.7 0.8 4 5 6 7 8 9 10 Number of lizard species ? ? ??? ? ? ? ? ? FIGURE 28.21 Spatial heterogeneity. The species richness of desert lizards is positively correlated with the structural complexity of the plant cover in desert sites in the American Southwest. Temperature range (°C) 5010152025 50 100 150 Number of mammal species ? ? ? ? ? ? ? FIGURE 28.22 Climate.The species richness of mammals is inversely correlated with monthly mean temperature range along the west coast of North America. Biogeographic Patterns of Species Diversity Since before Darwin, biologists have recognized that there are more different kinds of animals and plants in the tropics than in temperate regions. For many species, there is a steady increase in species richness from the arctic to the tropics. Called a species diversity cline, such a biogeo- graphic gradient in numbers of species correlated with lati- tude has been reported for plants and animals, including birds (figure 28.23), mammals, reptiles. Why Are There More Species in the Tropics? For the better part of a century, ecologists have puzzled over the cline in species diversity from the arctic to the tropics. The difficulty has not been in forming a reasonable hypothesis of why there are more species in the tropics, but rather in sorting through the many reasonable hypotheses that suggest themselves. Here we will consider five of the most commonly discussed suggestions: Evolutionary age. It has often been proposed that the tropics have more species than temperate regions be- cause the tropics have existed over long and uninter- rupted periods of evolutionary time, while temperate re- gions have been subject to repeated glaciations. The greater age of tropical communities would have allowed complex population interactions to coevolve within them, fostering a greater variety of plants and animals in the tropics. However, recent work suggests that the long-term stability of tropical communities has been greatly exag- gerated. An examination of pollen within undisturbed soil cores reveals that during glaciations the tropical forests contracted to a few small refuges surrounded by grassland. This suggests that the tropics have not had a continuous record of species richness over long periods of evolutionary time. Higher productivity. A second often-advanced hy- pothesis is that the tropics contain more species because this part of the earth receives more solar radiation than temperate regions do. The argument is that more solar energy, coupled to a year-round growing season, greatly increases the overall photosynthetic activity of plants in the tropics. If we visualize the tropical forest as a pie (total resources) being cut into slices (species niches), we can see that a larger pie accommodates more slices. However, many field studies have indicated that species richness is highest at intermediate levels of productivity. Accordingly, increasing productivity would be expected to lead to lower, not higher, species richness. Perhaps the long column of vegetation down through which light passes in a tropical forest produces a wide range of fre- quencies and intensities, creating a greater variety of light environments and so promoting species diversity. Predictability. There are no winters in the tropics. Tropical temperatures are stable and predictable, one day much like the next. These unchanging environments might encourage specialization, with niches subdivided to partition resources and so avoid competition. The ex- pected result would be a larger number of more special- ized species in the tropics, which is what we see. Many field tests of this hypothesis have been carried out, and almost all support it, reporting larger numbers of nar- rower niches in tropical communities than in temperate areas. Predation. Many reports indicate that predation may be more intense in the tropics. In theory, more intense predation could reduce the importance of competition, permitting greater niche overlap and thus promoting greater species richness. Spatial heterogeneity. As noted earlier, spatial het- erogeneity promotes species richness. Tropical forests, by virtue of their complexity, create a variety of micro- habitats and so may foster larger numbers of species. No one really knows why there are more species in the tropics, but there are plenty of suggestions. 588 Part VIII The Global Environment Number of species 0-50 50-100 100-150 150-200 200-250 250-300 300-350 350-400 400-450 450-500 500-550 550-600 600-650 650-700 FIGURE 28.23 A latitudinal cline in species richness.Among North and Central American birds, a marked increase in the number of species occurs as one moves toward the tropics. Fewer than 100 species are found at arctic latitudes, while more than 600 species live in southern Central America. Island Biogeography One of the most reliable patterns in ecology is the observa- tion that larger islands contain more species than smaller islands. In 1967, Robert MacArthur of Princeton Univer- sity and Edward O. Wilson of Harvard University pro- posed that this species-area relationship was a result of the effect of area on the likelihood of species extinction and colonization. The Equilibrium Model MacArthur and Wilson reasoned that species are constantly being dispersed to islands, so islands have a tendency to ac- cumulate more and more species. At the same time that new species are added, however, other species are lost by extinction. As the number of species on an initially empty island increases, the rate of colonization must decrease as the pool of potential colonizing species not already present on the island becomes depleted. At the same time, the rate of extinction should increase—the more species on an is- land, the greater the likelihood that any given species will perish. As a result, at some point, the number of extinctions and colonizations should be equal and the number of species should then remain constant. Every island of a given size, then, has a characteristic equilibrium number of species that tends to persist through time (the intersection point in figure 28.24a), although the individual species will change as species become extinct and new species colonize. MacArthur and Wilson’s equilibrium theory proposes that island species richness is a dynamic equilibrium be- tween colonization and extinction. Both island size and dis- tance from the mainland would play important roles. We would expect smaller islands to have higher rates of extinc- tion because their population sizes would, on average, be smaller. Also, we would expect fewer colonizers to reach is- lands that lie farther from the mainland. Thus, small is- lands far from the mainland have the fewest species; large islands near the mainland have the most (figure 28.24b). The predictions of this simple model bear out well in field data. Asian Pacific bird species (figure 28.24c) exhibit a positive correlation of species richness with island size, but a negative correlation of species richness with distance from the mainland. Testing the Equilibrium Model Field studies in which small islands have been censused, cleared, and allowed to recolonize tend to support the equi- librium model. However, long-term experimental field studies are suggesting that the situation is more compli- cated than MacArthur and Wilson envisioned. Their the- ory predicts a high level of species turnover as some species perish and others arrive. However, studies on island birds and spiders indicate that very little turnover occurs from year to year. Moreover, those species that do come and go are a subset of species that never attain high popula- tions. A substantial proportion of the species appears to maintain high populations and rarely go extinct. These studies, of course, have only been going on for 20 years or less. It is possible that over periods of centuries, rare species may become common and vice versa so that, over such spans of time, the equilibrium theory is a good de- scription of what determines island species richness. Future research is necessary to fully understand the dynamics of species richness. Species richness on islands is a dynamic equilibrium between colonization and extinction. Chapter 28 Dynamics of Ecosystems 589 Number of species Colonization rate of new species Extinction rate of island species 0 (a) (b) (c) Rate Rate Number of species 0 Colonization r ate Extinction r ate Island near mainland Island far from mainland Small island Large island Island size (km 2 ) 10010 1000 10,000 100,000 10 100 1,000 More than 3200 km from New Guinea Number of Asian P acific bird species 800–3200 km from New Guinea Less than 800 km from New Guinea FIGURE 28.24 The equilibrium model of island biogeography.(a) Island species richness reaches an equilibrium (black dot) when the colonization rate of new species equals the extinction rate of species on the island. (b) The equilibrium shifts when the colonization rate is affected by distance from the mainland and when the extinction rate is affected by size of the island. Species richness is positively correlated with island size and inversely correlated with distance from the mainland. (c) The effect of distance from a larger island—which can be the source of colonizing species—is readily apparent. More distant islands have fewer species compared to nearer islands of the same size. 590 Part VIII The Global Environment Chapter 28 Summary Questions Media Resources 28.1 Chemicals cycle within ecosystems. ? Fully 98% of the water on earth cycles through the atmosphere. In the United States, 96% of the fresh water is groundwater. ? About 10% of the roughly 700 billion metric tons of free carbon dioxide in the atmosphere is fixed each year through photosynthesis. About as much carbon exists in living organisms at any one time as is present in the atmosphere. ? Carbon, nitrogen, and oxygen have gaseous or liquid reservoirs, as does water. All of the other nutrients, such as phosphorus, are contained in solid mineral reservoirs. ? Phosphorus is a key component of many biological molecules; it weathers out of soils and is transported to the world’s oceans. 1.What are the primary reservoirs for the chemicals in biogeochemical cycles? Are more of the life-sustaining chemicals found in these reservoirs or in the earth’s living organisms? 2.What is denitrification? Which organisms carry it out? 3.How is the phosphorus cycle different from the water, carbon, nitrogen, and oxygen cycles? What are the natural sources for phosphorus? 4.What effect does deforestation have on the water cycle and overall fertility of the land? ? Plants convert about 1 to 5% of the light energy that falls on their leaves to food energy. Producers, the herbivores that eat them, and the carnivores that eat the herbivores constitute three trophic levels. ? At each level, only about 10% of the energy available in the food is fixed in the body of the consumer. For this reason, food chains are always relatively short. 5.How might an increase in the number of predators affect lower levels of a food chain. How might an increase in nutrients affect upper levels? 28.2 Ecosystems are structured by who eats whom. ? The primary productivity of a community is a measure of the biomass photosynthesis produces within it. ? As energy passes through the trophic levels of an ecosystem, much is lost at each step. Ecological pyramids reflect this energy loss. 6.What is the difference between primary productivity, gross primary productivity, and net primary productivity? 7.Which type of diet, carnivorous or herbivorous, provides more food value to any given living organism? 28.3 Energy flows through ecosystems. ? Increasing the number of species in a community seems to promote ecosystem productivity. Controversial experiments suggest that communities with increased species richness are more stable and less vulnerable to disturbance. 8.Why might rain forests have high levels of species diversity? 9.Why do distant islands tend to have fewer species than nearer islands of the same size? Why do different-sized islands tend to differ in species number? 28.4 Biodiversity promotes ecosystem stability. www.mhhe.com/raven6e www.biocourse.com ? Activity: Nutrient Cycle ? Activity: Carbon Cycle ? Ecosystem Introduction ? Ecosystem Concept Quiz ? Water Cycle ? Ground Water ? Water Qaulity ? Nutrient Cycles ? Carbon Cycle ? Nitrogen Cycle ? Activity: Energy flow ? Energy Flow ? Exponential Population Growth ? Student Research: Assessing Paleoenvironments ? On Science Article: Is Biodiversity Good? ? Bioethics Case Study: Wolves in Yellowstone ? Book review: Island of the Colorblindby Sacks ? The Song of the Dodo by Quammen 591 29 The Biosphere Concept Outline 29.1 Organisms must cope with a varied environment. The Environmental Challenge. Habitats vary in ways important to survival. Organisms cope with environmental variation with physiological, morphological, and behavioral adaptations. 29.2 Climate shapes the character of ecosystems. The Sun and Atmospheric Circulation. The sun powers major movements in atmospheric circulation. Atmospheric Circulation, Precipitation, and Climate. Latitude and elevation have important effects on climate, although other factors affect regional climate. 29.3 Biomes are widespread terrestrial ecosystems. The Major Biomes. Characteristic communities called biomes occur in different climatic regions. Variations in temperature and precipitation are good predictors of what biomes will occur where. Major biomes include tropical rain forest, savanna, desert, grassland, temperate deciduous forest, temperate evergreen forest, taiga, and tundra. 29.4 Aquatic ecosystems cover much of the earth. Patterns of Circulation in the Oceans. The world’s oceans circulate in huge circles deflected by the continents. Life in the Oceans. Most of the major groups of organisms originated and are still represented in the sea. Marine Ecosystems. The communities of the ocean are delineated primarily by depth. Freshwater Habitats. Like miniature oceans, ponds and lakes support different communities at different depths. Productivity of Freshwater Ecosystems. Freshwater ecosystems are often highly productive. T he biosphere includes all living communities on earth, from the profusion of life in the tropical rain forests to the photosynthetic phytoplankton in the world’s oceans. In a very general sense, the distribution of life on earth re- flects variations in the world’s environments, principally in temperature and the availability of water. Figure 29.1 is a satellite image of North and South America, collected over eight years, the colors keyed to the relative abundance of chlorophyll, a good indicator of rich biological communi- ties. Phytoplankton and algae produce the dark red zones in the oceans and along the seacoasts. Green and dark green areas on land are dense forests, while orange areas like the deserts of western South America are largely bar- ren of life. FIGURE 29.1 Life in the biosphere. In this satellite image, orange zones are largely arid. Almost every environment on earth can be described in terms of temperature and moisture. These physical parameters have great bearing on the forms of life that are able to inhabit a particular region. altitudes, such as in the Andes, initially experience altitude sickness—the symptoms of which include heart palpita- tions, nausea, fatigue, headache, mental impairment and, in serious cases, pulmonary edema—because of the lower at- mospheric pressure and consequent lower oxygen availabil- ity in the air. After several days, however, the same people will feel fine, because of a number of physiological changes that increase the delivery of oxygen to body (table 29.1). Some insects avoid freezing in the winter by adding glycerol “antifreeze” to their blood; others tolerate freezing by converting much of their glycogen reserves into alcohols that protect their cell membranes from freeze damage. Morphology. Animals that maintain a constant internal temperature (endotherms) in a cold environment have adaptations that tend to minimize energy expenditure. Many other mammals grower thicker coats during the win- ter, utilizing their fur as insulation to retain body heat dur- ing the winter. In general, the thicker the fur, the greater the insulation (figure 29.3). Thus, a wolf’s fur is some three times as thick in winter as summer and insulates more than twice as well. Other mammals escape some of the costs of maintaining a constant body temperature during winter by hibernating during the coldest season, behaving, in effect, like conformers. 592 Part VIII The Global Environment The Environmental Challenge How Environments Vary The nature of the physical environment in large measure determines what organisms live in a place. Key elements include: Temperature. Most organisms are adapted to live within a relatively narrow range of temperatures and will not thrive if temperatures are colder or warmer. The growing season of plants, for example, is importantly in- fluenced by temperature. Water. Plants and all other organisms require water. On land, water is often scarce, so patterns of rainfall have a major influence on life. Sunlight. Almost all ecosystems rely on energy cap- tured by photosynthesis; the availability of sunlight in- fluences the amount of life an ecosystem can support, particularly below the surface in marine communities. Soil. The physical consistency, pH, and mineral com- position of soil often severely limit plant growth, partic- ularly the availability of nitrogen and phosphorus. Active and Passive Approaches to Coping with Environmental Variation An individual encountering environmental variation may choose to maintain a “steady-state” internal environment, an approach known as maintaining homeostasis. Many animals and plants actively employ physiological, mor- phological, or behavioral mechanisms to maintain home- ostasis. The beetle in figure 29.2 is using a behavioral mechanism to cope with drastic changes in water avail- ability. Other animals and plants simply conform to the environment in which they find themselves, their bodies adopting the temperature, salinity, and other aspects of their surroundings. Responses to environmental variation can be seen over both the short and the long term. In the short term, span- ning periods of a few minutes to an individual’s lifetime, organisms have a variety of ways of coping with environ- mental change. Over longer periods, natural selection can operate to make a population better adapted to the envi- ronment. Individual Response to Environmental Change Physiology. Many organisms are able to adapt to envi- ronmental change by making physiological adjustments. Thus, your body constricts the blood vessels on the surface of your face on a cold day, reducing heat loss (and also giv- ing your face a “flush”). Similarly, humans who visit high 29.1 Organisms must cope with a varied environment. FIGURE 29.2 Meeting the challenge of obtaining moisture in a desert. On the dry sand dunes of the Namib Desert in southwestern Africa, the beetle Onymacris unguicularis collects moisture from the fog by holding its abdomen up at the crest of a dune to gather condensed water. Table 29.1 Physiological changes at high altitude that increase the amount of oxygen delivered to body tissues Increased rate of breathing Increased erythrocyte production, increasing the amount of hemoglobin in the blood Decreased binding capacity of hemoglobin, thus increasing the rate at which oxygen is unloaded in body tissues Increased density of mitochondria, capillaries, and muscle myoglobin Based on Table 14-11 in A. J. Vander, J. H. Sherman, and D. S. Luciano, Human Physiology, 5th Ed., McGraw-Hill, 1990. Behavior. Many animals deal with variation in the envi- ronment by moving from one patch of habitat to another, avoiding areas that are unsuitable. The tropical lizards in figure 29.4 manage to maintain a fairly uniform body tem- perature in an open habitat by basking in patches of sun, retreating to the shade when they become too hot. By con- trast, in shaded forests, the same lizards do not have the op- portunity to regulate their body temperature through be- havioral means. Thus, they become conformers and adopt the temperature of their surroundings. Behavioral adaptations can be extreme. The spadefoot toad Scaphiophus, which lives in the deserts of North Amer- ica, can burrow nearly a meter below the surface and re- main there for as long as nine months of each year, its metabolic rate greatly reduced, living on fat reserves. When moist cool conditions return, the toads emerge and breed. The young toads mature rapidly and burrow back underground. Evolutionary Responses to Environmental Variation These examples represent different ways in which organ- isms may adjust to changing environmental conditions. The ability of an individual to alter its physiology, mor- phology, or behavior is itself an evolutionary adaptation, the result of natural selection. The results of natural selec- tion can also be detected by comparing closely related species that live in different environments. In such cases, species often exhibit striking adaptations to the particular environment in which they live. For example, animals that live in different climates show many differences. Mammals from colder climates tend to have shorter ears and limbs (Allen’s Rule) and larger bodies (Bergmann’s Rule) to limit heat loss. Both mechanisms re- duce the surface area across which animals lose heat. Lizards that live in different climates exhibit physiological adaptations for coping with life at different temperatures. Desert lizards are unaffected by high temperatures that would kill a lizard from northern Europe, but the northern lizards are capable of running, capturing prey, and digest- ing food at cooler temperatures at which desert lizards would be completely immobilized. Many species also exhibit adaptations to living in areas where water is scarce. Everyone knows of the camel, and other desert animals, which can go extended periods with- out drinking water. Another example of desert adaptation is seen in frogs. Most frogs have moist skins through which water permeates readily. Such animals could not survive in arid climates because they would rapidly dehydrate and dry. However, some frogs have solved this problem by greatly reducing the rate of water loss through the skin. One species, for example, secretes a waxy substance from spe- cialized glands that waterproofs its skin and reduces rates of water loss by 95%. Adaptation to different environments can also be stud- ied experimentally. For example, when strains of E. coli are grown at high temperatures (42?C), the speed at which resources are utilized improves through time. After 2000 generations, this ability increased 30% over what it had been when the experiment started. The mechanism by which efficiency of resource use was increased is still un- known and is the focus of current research. Organisms use a variety of physiological, morphological, and behavioral mechanisms to adjust to environmental variation. Over time, species evolve adaptations to living in different environments. Chapter 29 The Biosphere 593 1.0 0.5 1.0 1.5 2.0 Polar bear Polar bear Wolf Winter Summer Wolf 3.0 Thickness of fur (mm) Insulation ( ° C cal/m 2 /h) 4.0 5.0 6.0 FIGURE 29.3 Morphological adaptation. Fur thickness in North American mammals has a major impact on the degree of insulation the fur provides. 24 26 Open habitat 28 30 Hourly mean body temperature ( ° C) 24 26 28 30 32 Hourly mean air temperature (°C) Shaded forest FIGURE 29.4 Behavioral adaptation. The Puerto Rican lizard Anolis cristatellus maintains a relatively constant temperature by seeking out and basking in patches of sunlight; in shaded forests, this behavior is not possible and body temperature conforms to the surroundings. The distribution of biomes (see discussion later in this chapter) re- sults from the interaction of the features of the earth itself, such as different soil types or the occur- rence of mountains and valleys, with two key physical factors: (1) the amount of solar heat that reaches different parts of the earth and seasonal variations in that heat; and (2) global atmospheric circula- tion and the resulting patterns of oceanic circulation. Together these factors dictate local climate, and so determine the amounts and distrib- ution of precipitation. The Sun and Atmospheric Circulation The earth receives an enormous quantity of heat from the sun in the form of shortwave radiation, and it radiates an equal amount of heat back to space in the form of long- wave radiation. About 10 24 calories arrive at the upper surface of the earth’s atmosphere each year, or about 1.94 calories per square cen- timeter per minute. About half of this energy reaches the earth’s sur- face. The wavelengths that reach the earth’s surface are not identical to those that reach the outer atmos- phere. Most of the ultraviolet radia- tion is absorbed by the oxygen (O 2 ) and ozone (O 3 ) in the atmosphere. As we will see in chapter 30, the de- pletion of the ozone layer, appar- ently as a result of human activities, poses serious ecological problems. Why the Tropics Are Warmer The world contains a great diversity of biomes because its climate varies so much from place to place. On a given day, Miami, Florida, and Bangor, Maine, often have very different weather. There is no mystery about this. Be- cause the earth is a sphere, some parts of it receive more energy from the sun than others. This variation is re- sponsible for many of the major climatic differences that occur over the earth’s surface, and, indirectly, for much of the diversity of biomes. The tropics are warmer than temperate regions because the sun’s rays arrive almost perpendicular to regions near the equator. Near the poles the angle of incidence of the sun’s rays spreads them out over a much greater area, providing less energy per unit area (figure 29.5a). 594 Part VIII The Global Environment 29.2 Climate shapes the character of ecosystems. Equator (a) (b) 60 H11034 30 H11034 Equator 30 H11034 60 H11034 30 H11034 Equator 30 H11034 60 H11034 30 H11034 Equator 30 H11034 60 H11034 30 H11034 Equator 30 H11034 Sun 23 1 /2H11034 Vernal equinox (sun aims directly at equator) Summer solstice (northern hemisphere tilts toward the sun) Winter solstice (northern hemisphere tilts away from the sun) Autumnal equinox (sun aims directly at equator) Sunlight Sunlight FIGURE 29.5 Relationships between the earth and the sun are critical in determining the nature and distribution of life on earth. (a) A beam of solar energy striking the earth in the middle latitudes spreads over a wider area of the earth’s surface than a similar beam striking the earth near the equator. (b) The rotation of the earth around the sun has a profound effect on climate. In the northern and southern hemispheres, temperatures change in an annual cycle because the earth tilts slightly on its axis in relation to the path around the sun. The earth’s annual orbit around the sun and its daily ro- tation on its own axis are both important in determining world climate (figure 29.5b). Because of the annual cycle, and the inclination of the earth’s axis at approximately 23.5° from its plane of revolution around the sun, there is a progression of seasons in all parts of the earth away from the equator. One pole or the other is tilted closer to the sun at all times except during the spring and autumn equinoxes. Major Atmospheric Circulation Patterns The moisture-holding capacity of air increases when it warms and decreases when it cools. High temperatures near the equator encourage evaporation and create warm, moist air. As this air rises and flows toward the poles, it cools and loses most of its moisture (figure 29.6). Conse- quently, the greatest amounts of precipitation on earth fall near the equator. This equatorial region of rising air is one of low pressure, called the doldrums, which draws air from both north and south of the equator. When the air masses that have risen reach about 30° north and south latitude, the dry air, now cooler, sinks and becomes re- heated. As the air reheats, its evaporative capacity in- creases, creating a zone of decreased precipitation. The air, still warmer than in the polar regions, continues to flow toward the poles. It rises again at about 60° north and south latitude, producing another zone of high pre- cipitation. At this latitude there is another low-pressure area, the polar front. Some of this rising air flows back to the equator and some continues north and south, de- scending near the poles and producing another zone of low precipitation before it returns to the equator. Air Currents Generated by the Earth’s Rotation Related to these bands of north-south circulation are three major air currents generated mainly by the interac- tion of the earth’s rotation with patterns of worldwide heat gain. Between about 30° north latitude and 30° south latitude, the trade winds blow, from the east-southeast in the southern hemisphere and from the east-northeast in the northern hemisphere. The trade winds blow all year long and are the steadiest winds found anywhere on earth. They are stronger in winter and weaker in summer. Be- tween 30° and 60° north and south latitude, strong pre- vailing westerlies blow from west to east and dominate climatic patterns in these latitudes, particularly along the western edges of the continents. Weaker winds, blowing from east to west, occur farther north and south in their respective hemispheres. Warm air rises near the equator, descends and produces arid zones at about 30° north and south latitude, flows toward the poles, then rises again at about 60° north and south latitude, and moves back toward the equator. Part of this air, however, moves toward the poles, where it produces zones of low precipitation. Chapter 29 The Biosphere 595 E q u at or (a) 30H11034 30H11034 60H11034 60H11034 Equator Westerlies Westerlies Westerlies Northeast trades Northeast trades Doldrums Southeast trades 60° 30° 60° 30° (b) Doldrums Westerlies FIGURE 29.6 General patterns of atmospheric circulation. (a) The pattern of air movement toward and away from the earth’s surface. (b) The major wind currents across the face of the earth. Atmospheric Circulation, Precipitation, and Climate As we have discussed, precipitation is generally low near 30° north and south latitude, where air is falling and warm- ing, and relatively high near 60° north and south latitude, where it is rising and cooling. Partly as a result of these fac- tors, all the great deserts of the world lie near 30° north or south latitude. Other major deserts are formed in the inte- riors of large continents. These areas have limited precipi- tation because of their distance from the sea, the ultimate source of most moisture. Rain Shadows Other deserts occur because mountain ranges intercept moisture-laden winds from the sea. When this occurs, the air rises and the moisture-holding capacity of the air decreases, resulting in increased precipitation on the windward side of the mountains—the side from which the wind is blowing. As the air descends the other side of the mountains, the leeward side, it is warmed, and its moisture-holding capacity increases, tending to block precipitation. In California, for example, the eastern sides of the Sierra Nevada Mountains are much drier than the western sides, and the vegetation is often very different. This phenomenon is called the rain shadow effect (fig- ure 29.7). Regional Climates Four relatively small areas, each located on a different con- tinent, share a climate that resembles that of the Mediter- ranean region. So-called Mediterranean climates are found in portions of Baja, California, and Oregon; in central Chile; in southwestern Australia; and in the Cape region of South Africa. In all of these areas, the prevailing westerlies blow during the summer from a cool ocean onto warm land. As a result, the air’s moisture-holding capacity in- creases, the air absorbing moisture and creating hot rainless summers. Such climates are unusual on a world scale. In the five regions where they occur, many unique kinds of plants and animals, often local in distribution, have evolved. Because of the prevailing westerlies, the great deserts of the world (other than those in the interiors of continents) and the areas of Mediterranean climate lie on the western sides of the continents. Another kind of regional climate occurs in southern Asia. The monsoon climatic conditions characteristic of India and southern Asia occur during the summer months. During the winter, the trade winds blow from the east- northeast off the cool land onto the warm sea. From June to October, though, when the land is heated, the direction of the air flow reverses, and the winds veer around to blow onto the Indian subcontinent and adjacent areas from the southwest bringing rain. The duration and strength of the monsoon winds spell the difference between food suffi- ciency and starvation for hundreds of millions of people in this region each year. 596 Part VIII The Global Environment Pacific Ocean Wind direction Moist Sierra Nevada Arid Rain shadow FIGURE 29.7 The rain shadow effect. Moisture-laden winds from the Pacific Ocean rise and are cooled when they encounter the Sierra Nevada Mountains. As their moisture-holding capacity decreases, precipitation occurs, making the middle elevation of the range one of the snowiest regions on earth; it supports tall forests, including those that include the famous giant sequoias (Sequoiadendron giganteum). As the air descends on the east side of the range, its moisture-holding capacity increases again, and the air picks up rather than releases moisture from its surroundings. As a result, desert conditions prevail on the east side of the mountains. 60° N Variation in monthly means Annual mean Latitude T emperature ( ° C) –10 0 10 20 30 30° 0 30° 60° S FIGURE 29.8 Temperature varies with latitude. The blue line represents the annual mean temperature at latitudes from the North Pole to Antarctica. Latitude Temperatures are higher in tropical ecosystems for a sim- ple reason: more sunlight per unit area falls on tropical lati- tudes. Solar radiation is most intense when the sun is di- rectly overhead, and this only occurs in the tropics, where sunlight strikes the equator perpendicularly. As figure 29.8 shows, the highest mean global temperatures occur near the equator (that is, 0 latitude). Because there are no sea- sons in the tropics, there is little variation in mean monthly temperature in tropical ecosystems. As you move from the equator into temperate latitudes, sunlight strikes the earth at a more oblique angle, so that less falls on a given area. As a result, mean temperatures are lower. At temperate lati- tudes, temperature variation increases because of the in- creasingly marked seasons. Seasonal changes in wind circulation produce corre- sponding changes in ocean currents, sometimes causing nutrient-rich cold water to well up from ocean depths. This produces “blooms” among the plankton and other organisms living near the surface. Similar turnover occurs seasonally in freshwater lakes and ponds, bringing nutri- ents from the bottom to the surface in the fall and again in the spring. Elevation Temperature also varies with elevation, with higher alti- tudes becoming progressively colder. At any given lati- tude, air temperature falls about 6°C for every 1000- meter increase in elevation. The ecological consequences of temperature varying with elevation are the same as temperature varying with latitude (figure 29.9). Thus, in North America a 1000-meter increase in elevation results in a temperature drop equal to that of an 880-kilometer increase in latitude. This is one reason “timberline” (the elevation above which trees do not grow) occurs at pro- gressively lower elevations as one moves farther from the equator. Microclimate Climate also varies on a very fine scale within ecosystems. Within the litter on a forest floor, there is considerable variation in shading, local temperatures, and rates of evapo- ration from the soil. Called microclimate, these very local- ized climatic conditions can be very different from those of the overhead atmosphere. Gardeners spread straw over newly seeded lawns to create such a moisture-retaining mi- croclimate. The great deserts and associated arid areas of the world mostly lie along the western sides of continents at about 30° north and south latitude. Mountain ranges tend to intercept rain, creating deserts in their shadow. In general, temperatures are warmer in the tropics and at lower elevations. Chapter 29 The Biosphere 597 Equator North pole Polar ice Latitude Tundra Taiga Temperate forest Tropical rain forest Elevation Sea level 3500 m Elevation Polar ice Tundra Taiga Temperate forest Tropical rain forest FIGURE 29.9 Elevation affects the distribution of biomes much as latitude does. Biomes that normally occur far north and far south of the equator at sea level also occur in the tropics at high mountain elevations. Thus, on a tall mountain in southern Mexico or Guatemala, one might see a sequence of biomes like the one illustrated here. The Major Biomes Biomes are major communities of organisms that have a characteristic appearance and that are distributed over a wide land area defined largely by regional variations in cli- mate. As you might imagine from such a broad definition, there are many ways to classify biomes, and different ecolo- gists may assign the same community to different biomes. There is little disagreement, however, about the reality of biomes as major biological communities—only about how to best describe them. Distribution of the Major Biomes Eight major biome categories are presented in this text: tropical rain forest, savanna, desert, temperate grassland, temperate deciduous forest, temperate evergreen forest, taiga, and tundra. These biomes occur worldwide, occu- pying large regions that can be defined by rainfall and temperature. Six additional biomes are considered by some ecologists to be subsets of the eight major ones: polar ice, mountain zone, chaparral, warm moist evergreen forest, tropical monsoon forest, and semidesert. They vary remarkably from one another because they have evolved in regions with very different climates. Distributions of the 14 biomes are mapped in figure 29.10. Although each is by convention named for the domi- nant vegetation (deciduous forest, evergreen forest, grass- land, and so on) each biome is also characterized by partic- ular animals, fungi, and microorganisms adapted to live as members of that community. Wolves, caribou or reindeer, polar bears, hares, lynx, snowy owls, deer flies, and mosqui- toes inhabit the tundra all over the world and are as much a defining characteristic of the tundra biomes as the low, shrubby, matlike vegetation. 598 Part VIII The Global Environment 29.3 Biomes are widespread terrestrial ecosystems. Polar ice Tundra Taiga Mountain zone Temperate deciduous forest Temperate evergreen forest Warm, moist evergreen forest Tropical monsoon forest Tropical rain forest Chaparral Temperate grassland Savanna Semidesert Desert FIGURE 29.10 The distribution of biomes. Each biome is similar in structure and appearance wherever it occurs on earth. Biomes and Climate Many different environmental factors play a role in deter- mining which biomes are found where. Two key parame- ters are available moisture and temperature. Figure 29.11 presents data on ecosystem productivity as a function of an- nual precipitation and of annual mean temperature: ecosys- tem productivity is strongly influenced by both. This is not to say that other factors such as soil structure and its min- eral composition (discussed in detail in chapter 39), or sea- sonal versus constant climate, are not also important. Dif- ferent places with the same annual precipitation and temperature sometimes support different biomes, so other factors must also be important. Nevertheless, these two variables do a fine job of predicting what biomes will occur in most places, as figure 29.12 illustrates. If there were no mountains and no climatic effects caused by the irregular outlines of continents and by differ- ent sea temperatures, each biome would form an even belt around the globe, defined largely by latitude. In truth, these other factors also greatly affect the distribution of biomes. Distance from the ocean has a major impact on rainfall, and elevation affects temperature—the summits of the Rocky Mountains are covered with a vegetation type that resembles the tundra which normally occurs at a much higher latitude. Chapter 29 The Biosphere 599 5000 1000 2000 Precipitation (mm/year) Productivity (g /m 2 / year) 3000 4000 500 1000 1500 2000 2500 (a) 50 –15 –10 –5 0 5 10 15 20 25 30 100 Tundra Taiga Hot desert Semidesert Temperate grassland Savanna Tropical rain forest Temperate deciduous forest Temperate evergreen forest 150 200 250 Mean annual precipitation (cm) Mean annual temperature ( ° C) 300 350 400 450 FIGURE 29.11 The effects of precipitation and temperature on primary productivity. The net primary productivity of ecosystems at 52 locations around the globe depends significantly upon (a) mean annual precipitation and (b) mean annual temperature. Productivity (g /m 2 / year) Temperature (°C) –10 0–5 5 1510 2520 30 500 0 1000 1500 2000 2500 (b) FIGURE 29.12 Temperature and precipitation are excellent predictors of biome distribution. At mean annual precipitations between 50 and 150 cm, other factors such as seasonal drought, fire, and grazing also have a major influence on biome distribution. Tropical Rain Forests Rain forests, which receive 140 to 450 centimeters of rain a year, are the rich- est ecosystems on earth (figure 29.13). They contain at least half of the earth’s species of terrestrial plants and ani- mals—more than 2 million species! In a single square mile of tropical forest in Rondonia, Brazil, there are 1200 species of butterflies—twice the total number found in the United States and Canada combined. The communities that make up tropical rain forests are diverse in that each kind of animal, plant, or microorganism is often repre- sented in a given area by very few indi- viduals. There are extensive tropical rain forests in South America, Africa, and Southeast Asia. But the world’s rain forests are being destroyed, and countless species, many of them never seen by humans, are disappearing with them. A quarter of the world’s species will disappear with the rain forests dur- ing the lifetime of many of us. Savannas In the dry climates that border the tropics are the world’s great grasslands, called savannas. Savanna landscapes are open, often with widely spaced trees, and rainfall (75 to 125 centimeters annually) is seasonal. Many of the ani- mals and plants are active only during the rainy season. The huge herds of grazing animals that inhabit the African savanna are familiar to all of us. Such animal communities lived in North America during the Pleis- tocene epoch but have persisted mainly in Africa. On a global scale, the savanna biome is transitional between tropical rain forest and desert. As these savannas are in- creasingly converted to agricultural use to feed rapidly expanding human populations in subtropical areas, their inhabitants are struggling to survive. The elephant and rhino are now endangered species; lion, giraffe, and chee- tah will soon follow. Deserts In the interior of continents are the world’s great deserts, especially in Africa (the Sahara), Asia (the Gobi) and Aus- tralia (the Great Sandy Desert). Deserts are dry places where less than 25 centimeters of rain falls in a year—an amount so low that vegetation is sparse and survival de- pends on water conservation. Plants and animals may re- strict their activity to favorable times of the year, when water is present. To avoid high temperatures, most desert vertebrates live in deep, cool, and sometimes even some- what moist burrows. Those that are active over a greater portion of the year emerge only at night, when tempera- tures are relatively cool. Some, such as camels, can drink large quantities of water when it is available and then sur- vive long, dry periods. Many animals simply migrate to or through the desert, where they exploit food that may be abundant seasonally. Temperate Grasslands Halfway between the equator and the poles are temperate regions where rich grasslands grow. These grasslands once covered much of the interior of North America, and they were widespread in Eurasia and South America as well. Such grasslands are often highly productive when converted to agricultural use. Many of the rich agricul- tural lands in the United States and southern Canada were originally occupied by prairies, another name for temperate grasslands. The roots of perennial grasses characteristically penetrate far into the soil, and grassland soils tend to be deep and fertile. Temperate grasslands are often populated by herds of grazing mammals. In North America, huge herds of bison and pronghorns once inhabited the prairies. The herds are almost all gone now, with most of the prairies having been converted to the richest agricultural region on earth. 600 Part VIII The Global Environment FIGURE 29.13 Tropical rain forest. Temperate Deciduous Forests Mild climates (warm summers and cool winters) and plentiful rains promote the growth of deciduous (hardwood) forests in Eurasia, the northeastern United States, and eastern Canada (fig- ure 29.14). A deciduous tree is one that drops its leaves in the winter. Deer, bears, beavers, and raccoons are familiar animals of the temperate regions. Be- cause the temperate deciduous forests represent the remnants of more exten- sive forests that stretched across North America and Eurasia several million years ago, the remaining areas in eastern Asia and eastern North America share animals and plants that were once more widespread. Alligators, for example, are found today only in China and in the southeastern United States. The decidu- ous forest in eastern Asia is rich in species because climatic conditions have historically remained constant. Many perennial herbs live in areas of temper- ate deciduous forest. Temperate Evergreen Forests Temperate evergreen forests occur in regions where win- ters are cold and there is a strong, seasonal dry period. The pine forests of the western United States and California oak woodlands are typical temperate evergreen forests. Temperate evergreen forests are characteristic of regions with nutrient-poor soils. Temperate-mixed evergreen forests represent a broad transitional zone between temper- ate deciduous forests to the south and taiga to the north. Many of these forests are endangered by overlogging, par- ticularly in the western United States. Taiga A great ring of northern forests of coniferous trees (spruce, hemlock, and fir) extends across vast areas of Asia and North America. Coniferous trees are ones with leaves like needles that are kept all year long. This ecosystem, called taiga, is one of the largest on earth. Here, the winters are long and cold, and most of the limited precipitation falls in the summer. Because the taiga has too short a growing sea- son for farming, few people live there. Many large mam- mals, including elk, moose, deer, and such carnivores as wolves, bears, lynx, and wolverines, live in the taiga. Tradi- tionally, fur trapping has been extensive in this region, as has lumber production. Marshes, lakes, and ponds are com- mon and are often fringed by willows or birches. Most of the trees occur in dense stands of one or a few species. Tundra In the far north, above the great coniferous forests and south of the polar ice, few trees grow. There the grassland, called tundra, is open, windswept, and often boggy. Enor- mous in extent, this ecosystem covers one-fifth of the earth’s land surface. Very little rain or snow falls. When rain does fall during the brief arctic summer, it sits on frozen ground, creating a sea of boggy ground. Per- mafrost, or permanent ice, usually exists within a meter of the surface. Trees are small and are mostly confined to the margins of streams and lakes. As in taiga, herbs of the tun- dra are perennials that grow rapidly during the brief sum- mers. Large grazing mammals, including musk-oxen, cari- bou, reindeer, and carnivores, such as wolves, foxes, and lynx, live in the tundra. Lemming populations rise and fall on a long-term cycle, with important effects on the animals that prey on them. Major biological communities called biomes can be distinguished in different climatic regions. These communities, which occur in regions of similar climate, are much the same wherever they are found. Variation in annual mean temperature and precipitation are good predictors of what biome will occur where. Chapter 29 The Biosphere 601 FIGURE 29.14 Temperate deciduous forest. Patterns of Circulation in the Oceans Patterns of ocean circulation are determined by the pat- terns of atmospheric circulation, but they are modified by the locations of landmasses. Oceanic circulation is domi- nated by huge surface gyres (figure 29.15), which move around the subtropical zones of high pressure between ap- proximately 30° north and 30° south latitude. These gyres move clockwise in the northern hemisphere and counter- clockwise in the southern hemisphere. The ways they re- distribute heat profoundly affects life not only in the oceans but also on coastal lands. For example, the Gulf Stream, in the North Atlantic, swings away from North America near Cape Hatteras, North Carolina, and reaches Europe near the southern British Isles. Because of the Gulf Stream, western Europe is much warmer and more temperate than eastern North America at similar latitudes. As a general principle, western sides of continents in tem- perate zones of the northern hemisphere are warmer than their eastern sides; the opposite is true of the southern hemisphere. In addition, winds passing over cold water onto warm land increase their moisture-holding capacity, limiting precipitation. In South America, the Humboldt Current carries phosphorus-rich cold water northward up the west coast. Phosphorus is brought up from the ocean depths by the upwelling of cool water that occurs as offshore winds blow from the mountainous slopes that border the Pacific Ocean. This nutrient-rich current helps make possible the abundance of marine life that supports the fisheries of Peru and northern Chile. Marine birds, which feed on these organisms, are responsible for the commercially important, phosphorus-rich, guano deposits on the sea- coasts of these countries. 602 Part VIII The Global Environment 29.4 Aquatic ecosystems cover much of the earth. Antarctica South America Equatorial countercurrent N. Equatorial current Equator Gulf stream Cold water current Warm water current North America Africa Asia Europe L a b r a d o r c u r r e n t t n e r r u c t d l o b m u H J a p a n cu rre nt S . E q u a to ri a l c urren t A n ta rc ti c c ir cu m po la r c urr ent FIGURE 29.15 Ocean circulation. Water moves in the oceans in great surface spiral patterns called gyres; they profoundly affect the climate on adjacent lands. El Ni?o and Ocean Ecology Every Christmas a tepid current sweeps down the coast of Peru and Ecuador from the tropics, reducing the fish popu- lation slightly and giving local fishermen some time off. The local fishermen named this Christmas current El Ni?o (literally, “the child,” after “the Christ Child”). Now, though, the term is reserved for a catastrophic version of the same phenomenon, one that occurs every two to seven years and is felt not only locally but on a global scale. Scientists now have a pretty good idea of what goes on in an El Ni?o. Normally the Pacific Ocean is fanned by constantly blowing east-to-west trade winds that push warm surface water away from the ocean’s eastern side (Peru, Ecuador, and Chile) and allow cold water to well up from the depths in its place, carrying nutrients that feed plankton and hence fish. This surface water piles up in the west, around Australia and the Philippines, making it sev- eral degrees warmer and a meter or so higher than the east- ern side of the ocean. But if the winds slacken briefly, warm water begins to slosh back across the ocean. Once this happens, ocean and atmosphere conspire to ensure it keeps happening. The warmer the eastern ocean gets, the warmer and lighter the air above it becomes, and hence more similar to the air on the western side. This re- duces the difference in pressure across the ocean. Because a pressure difference is what makes winds blow, the easterly trades weaken further, letting the warm water continue its eastward advance. The end result is to shift the weather systems of the western Pacific Ocean 6000 km eastward. The tropical rainstorms that usually drench Indonesia and the Philip- pines are caused when warm seawater abutting these islands causes the air above it to rise, cool, and condense its mois- ture into clouds. When the warm water moves east, so do the clouds, leaving the previously rainy areas in drought. Conversely, the western edge of South America, its coastal waters usually too cold to trigger much rain, gets a soaking, while the upwelling slows down. During an El Ni?o, com- mercial fish stocks virtually disappear from the waters of Peru and northern Chile, and plankton drop to a twentieth of their normal abundance. That is just the beginning. El Ni?o’s effects are propa- gated across the world’s weather systems (figure 29.16). Vi- olent winter storms lash the coast of California, accompa- nied by flooding, and El Ni?o produces colder and wetter winters than normal in Florida and along the Gulf Coast. The American midwest experiences heavier-than-normal rains, as do Israel and its neighbors. Though the effects of El Ni?os are now fairly clear, what triggers them still remains a mystery. Models of these weather disturbances suggest that the climatic change that triggers El Ni?o is “chaotic.” Wind and ocean currents return again and again to the same condi- tion, but never in a regular pattern, and small nudges can send them off in many different directions—including an El Ni?o. The world’s oceans circulate in huge gyres deflected by continental landmasses. Circulation of ocean water redistributes heat, warming the western side of continents. Disturbances in ocean currents like El Ni?o can have profound influences on world climate. Chapter 29 The Biosphere 603 Warmer Warmer Drier and warmer Wetter Wetter and warmer El Nino Sea temperature higher than normal Wetter Drier Warmer Warmer Wetter and warmer Wetter and cooler Warmer Source: National Oceanic and Atmospheric Administration ? Drier FIGURE 29.16 An El Ni?o winter. El Ni?o currents produce unusual weather patterns all over the world as warm waters from the western Pacific move eastward. Life in the Oceans Nearly three-quarters of the earth’s surface is covered by ocean. Oceans have an average depth of more than 3 kilo- meters, and they are, for the most part, cold and dark. Het- erotrophic organisms inhabit even the greatest ocean depths, which reach nearly 11 kilometers in the Marianas Trench of the western Pacific Ocean. Photosynthetic or- ganisms are confined to the upper few hundred meters of water. Organisms that live below this level obtain almost all of their food indirectly, as a result of photosynthetic activi- ties that occur above. The supply of oxygen can often be critical in the ocean, and as water temperatures become warmer, the water holds less oxygen. For this reason, the amount of available oxygen becomes an important limiting factor for organ- isms in warmer marine regions of the globe. Carbon diox- ide, in contrast, is almost never limited in the oceans. The distribution of minerals is much more uniform in the ocean than it is on land, where individual soils reflect the composition of the parent rocks from which they have weathered. Frigid and bare, the floors of the deep sea have long been considered a biological desert. Recent close-up looks taken by marine biologists, however, paint a differ- ent picture (figure 29.17). The ocean floor is teeming with life. Often miles deep, thriving in pitch darkness under enormous pressure, crowds of marine invertebrates have been found in hundreds of deep samples from the Atlantic and Pacific. Rough estimates of deep-sea diver- sity have soared to millions of species. Many appear en- demic (local). The diversity of species is so high it may rival that of tropical rain forests! This profusion is unex- pected. New species usually require some kind of barrier in order to diverge (see chapter 22), and the ocean floor seems boringly uniform. However, little migration occurs among deep populations, thus allowing populations to di- verge and encouraging local specialization and species formation. A patchy environment may also contribute to species formation there; deep-sea ecologists find evidence that fine but nonetheless formidable resource barriers arise in the deep sea. Another conjecture is that the extra billion years or so that life has been evolving in the sea compared with land may be a factor in the unexpected biological richness of its deep recesses. Despite the many new forms of small invertebrates now being discovered on the seafloor, and the huge bio- mass that occurs in the sea, more than 90% of all described species of organisms occur on land. Each of the largest groups of organisms, including insects, mites, nematodes, fungi, and plants has marine representatives, but they constitute only a very small fraction of the total number of described species. There are two reasons for this. First, barriers between habitats are sharper on land, and varia- tions in elevation, parent rock, degree of exposure, and other factors have been crucial to the evolution of the millions of species of terrestrial organisms. Second, there are simply few taxonomists actively classifying the profu- sion of ocean floor life being brought to the surface. In terms of higher level diversity, the pattern is quite different. Of the major groups of organisms—phyla— most originated in the sea, and almost every one has rep- resentatives in the sea. Only a few phyla have been suc- cessful on land or in freshwater habitats, but these have given rise to an extraordinarily large number of described species. Although representatives of almost every phylum occur in the sea, an estimated 90% of living species of organisms are terrestrial. This is because of the enormous evolutionary success of a few phyla on land, where the boundaries between different habitats are sharper than they are in the sea. 604 Part VIII The Global Environment FIGURE 29.17 Food comes to the ocean floor from above. Looking for all the world like some undersea sunflower, the two sea anemones (actually animals) use a glass-sponge stalk to catch “marine snow,” food particles raining down on the ocean floor from the ocean surface miles above. Marine Ecosystems The marine environment consists of three major habitats: (1) the neritic zone, the zone of shallow waters along the coasts of continents; (2) the pelagic zone, the area of water above the ocean floor; and (3) the benthic zone, the actual ocean floor (figure 29.18). The part of the ocean floor that drops to depths where light does not penetrate is called the abyssal zone. The Neritic Zone The neritic zone of the ocean is the area less than 300 me- ters below the surface along the coasts of continents and is- lands. The zone is small in area, but it is inhabited by large numbers of species (figure 29.19). The intense and some- times violent interaction between sea and land in this zone gives a selective advantage to well-secured organisms that can withstand being washed away by the continual beating of the waves. Part of this zone, the intertidal region, sometimes called the littoral region, is exposed to the air whenever the tides recede. The world’s great fisheries are in shallow waters over continental shelves, either near the continents themselves or in the open ocean, where huge banks come near the surface. Nutrients, derived from land, are much more abundant in coastal and other shallow regions, where up- welling from the depths occurs, than in the open ocean. This accounts for the great productivity of the continen- tal shelf fisheries. The preservation of these fisheries, a source of high-quality protein exploited throughout the world, has become a growing concern. In Chesapeake Bay, where complex systems of rivers enter the ocean from heavily populated areas, environmental stresses have become so severe that they not only threaten the contin- ued existence of formerly highly productive fisheries, but also diminish the quality of human life in these regions. Increased runoff from farms and sewage effluent in areas like Chesapeake Bay add large amounts of nutrients to the water. This increased nutrient supply allows an in- crease in the numbers of some marine organisms. The in- creased populations then use up more and more of the oxygen in the water and thus may disturb established populations of organisms such as oysters. Climatic shifts may magnify these effects, and large numbers of marine animals die suddenly as a result. About three-fourths of the surface area of the world’s oceans are located in the tropics. In these waters, where the water temperature remains about 21°C, coral reefs can grow. These highly productive ecosystems can successfully concentrate nutrients, even from the relatively nutrient- poor waters characteristic of the tropics. Chapter 29 The Biosphere 605 Abyssal zone Limit of light penetration Continental shelf Intertidal or littoral region Neritic zone Benthic zone Pelagic zone FIGURE 29.18 Marine ecosystems. Ecologists classify marine communities into neritic, pelagic, benthic, and abyssal zones, according to depth (which affects how much light penetrates) and distance from shore. FIGURE 29.19 Diversity is great in coastal regions. Fishes and many other kinds of animals find food and shelter among the kelp beds in the coastal waters of temperate regions. The Pelagic Zone Drifting freely in the upper waters of the pelagic zone, a diverse biological community exists, primarily consisting of microscopic organisms called plankton. Fish and other larger or- ganisms that swim in these waters con- stitute the nekton, whose members feed on plankton and one another. Some members of the plankton, including protists and some bacteria, are photo- synthetic. Collectively, these organ- isms account for about 40% of all pho- tosynthesis that takes place on earth. Most plankton live in the top 100 me- ters of the sea, the zone into which light from the surface penetrates freely. Perhaps half of the total photo- synthesis in this zone is carried out by organisms less than 10 micrometers in diameter—at the lower limits of size for organisms—including cyanobacteria and algae, organ- isms so small that their abundance and ecological impor- tance have been unappreciated until relatively recently. Many heterotrophic protists and animals live in the plankton and feed directly on photosynthetic organisms and on one another. Gelatinous animals, especially jellyfish and ctenophores, are abundant in the plankton. The largest animals that have ever existed on earth, baleen whales, graze on plankton and nekton as do a number of other or- ganisms, such as fishes and crustaceans. Populations of organisms that make up plankton can in- crease rapidly, and the turnover of nutrients in the sea is great, although the productivity in these systems is quite low. Because nitrogen and phosphorus are often present in only small amounts and organisms may be relatively scarce, this productivity reflects rapid use and recycling rather than an abundance of these nutrients. The Benthic Zone The seafloor at depths below 1000 meters, the abyssal zone, has about twice the area of all the land on earth. The seafloor itself, sometimes called the benthic zone, is a thick blanket of mud, consisting of fine particles that have settled from the overlying water and accumulated over mil- lions of years. Because of high pressures (an additional at- mosphere of pressure for every 10 meters of depth), cold temperatures (2° to 3°C), darkness, and lack of food, biolo- gists thought that nothing could live on the seafloor. In fact, recent work has shown that the number of species that live at great depth is quite high. Most of these animals are only a few millimeters in size, although larger ones also occur in these regions. Some of the larger ones are biolu- minescent (figure 29.20a) and thus are able to communi- cate with one another or attract their prey. Animals on the sea bottom depend on the meager left- overs from organisms living kilometers overhead. The low densities and small size of most deep-sea bottom animals is in part a consequence of this limited food supply. In 1977, oceanographers diving in a research submarine were sur- prised to find dense clusters of large animals living on geo- thermal energy at a depth of 2500 meters. These deep-sea oases occur where seawater circulates through porous rock at sites where molten material from beneath the earth’s crust comes close to the rocky surface. A series of these areas occur on the Mid-Ocean Ridge, where basalt erupts through the ocean floor. This water is heated to temperatures in excess of 350°C and, in the process, becomes rich in reduced compounds. These compounds, such as hydrogen sulfide, provide en- ergy for bacterial primary production through chemosyn- thesis instead of photosynthesis. Mussels, clams, and large red-plumed worms in a phylum unrelated to any shallow- water invertebrates cluster around the vents (figure 29.20b). Bacteria live symbiotically within the tissues of these ani- mals. The animal supplies a place for the bacteria to live and transfers CO 2 , H 2 S, and O 2 to them for their growth; the bacteria supply the animal with organic compounds to use as food. Polychaete worms (see chapter 46), anemones, and limpets live on free-living chemosynthetic bacteria. Crabs act as scavengers and predators, and some of the fish are also predators. This is one of the few ecosystems on earth that does not depend on the sun’s energy. About 40% of the world’s photosynthetic productivity is estimated to occur in the oceans. The turnover of nutrients in the plankton is much more rapid than in most other ecosystems, and the total amounts of nutrients are very low. 606 Part VIII The Global Environment FIGURE 29.20 Life in the abyssal and benthic zones. (a) The luminous spot below the eye of this deep- sea fish results from the presence of a symbiotic colony of luminous bacteria. Similar luminous signals are a common feature of deep-sea animals that move about. (b) These giant beardworms live along vents where water jets from fissures at 350°C and then cools to the 2°C of the surrounding water. (a) (b) Freshwater Habitats Freshwater habitats are distinct from both marine and terrestrial ones, but they are limited in area. Inland lakes cover about 1.8% of the earth’s sur- face, and running water (streams and rivers) covers about 0.3%. All fresh- water habitats are strongly connected with terrestrial ones, with marshes and swamps constituting intermedi- ate habitats. In addition, a large amount of organic and inorganic ma- terial continuously enters bodies of fresh water from communities grow- ing on the land nearby (figure 29.21a). Many kinds of organisms are restricted to freshwater habitats (fig- ure 29.21b,c). When organisms live in rivers and streams, they must be able to swim against the current or attach themselves in such a way as to resist the effects of current, or risk being swept away. Ponds and Lakes Small bodies of fresh water are called ponds, and larger ones lakes. Because water absorbs light passing through it at wavelengths critical to photosynthesis (every meter absorbs 40% of the red and about 2% of the blue), the distribution of photosyn- thetic organisms is limited to the upper photic zone; heterotrophic organisms occur in the lower aphotic zone where very little light penetrates. Ponds and lakes, like the ocean, have three zones where organisms occur, distributed according to the depth of the water and its distance from shore (figure 29.22). The lit- toral zone is the shallow area along the shore. The limnetic zone is the well-illuminated surface water away from the shore, inhabited by plank- ton and other organisms that live in open water. The profundal zone is the area below the limits where light can effectively penetrate. Chapter 29 The Biosphere 607 FIGURE 29.21 A nutrient-rich stream. (a) Much organic material falls or seeps into streams from communities along the edges. This input increases the stream’s biological productivity. (b) This speckled darter and (c) this giant waterbug with eggs on its back can only live in freshwater habitats. (a) (b) (c) Limnetic zone Littoral zone Littoral zone Profundal zone FIGURE 29.22 The three zones in ponds and lakes. A shallow “edge” (littoral) zone lines the periphery of the lake, where attached algae and their insect herbivores live. An open-water surface (limnetic) zone lies across the entire lake and is inhabited by floating algae, zooplankton, and fish. A dark, deep-water (profundal) zone overlies the sediments at the bottom of the lake and contains numerous bacteria and wormlike organisms that consume dead debris settling at the bottom of the lake. Thermal Stratification Thermal stratification is characteristic of larger lakes in temperate regions (figure 29.23). In summer, warmer water forms a layer at the surface known as the epilimnion. Cooler water, called the hypolimnion (about 4°C), lies below. An abrupt change in temperature, the thermocline, separates these two layers. Depending on the climate of the particu- lar area, the epilimnion may become as much as 20 meters thick during the summer. In autumn the temperature of the epilimnion drops until it is the same as that of the hypolimnion, 4°C. When this occurs, epilimnion and hypolimnion mix—a process called fall overturn. Because water is densest at about 4°C, further cooling of the water as winter progresses creates a layer of cooler, lighter water, which freezes to form a layer of ice at the surface. Below the ice, the water tem- perature remains between 0° and 4°C, and plants and ani- mals can survive. In spring, the ice melts, and the surface water warms up. When it warms back to 4°C, it again mixes with the water below. This process is known as spring overturn. When lake waters mix in the spring and fall, nutrients formerly held in the depths of the lake are returned to the surface, and oxygen from surface waters is carried to the depths. Freshwater habitats include several distinct life zones. These zones shift seasonally in temperate lakes and ponds. In the spring and fall, when their temperatures are equal, shallower and deeper waters of the lake mix, with oxygen being carried to the depths and nutrients being brought to the surface. 608 Part VIII The Global Environment 18H11034 8H11034 20H11034 22H11034 6H11034 5H11034 4H11034 O 2 conc. Hypolimnion Thermocline Epilimnion Midsummer Spring overturn Fall overturn Winter Nutrients 4H11034 4H11034 4H11034 4H11034 4H11034 4H11034 4H11034 4H11034 4H11034 2H11034 0H11034 4H11034 4H11034 4H11034 Nutrients 4H11034 4H11034 4H11034 4H11034 4H11034 4H11034 4H11034 O 2 conc. O 2 conc. O 2 conc. FIGURE 29.23 Stratification in fresh water. The pattern stratification in a large pond or lake in temperate regions is upset in the spring and fall overturns. Of the three layers of water shown, the hypolimnion consists of the densest water, at 4°C; the epilimnion consists of warmer water that is less dense; and the thermocline is the zone of abrupt change in temperature that lies between them. If you have dived into a pond in temperate regions in the summer, you have experienced the existence of these layers. Productivity of Freshwater Ecosystems Some aquatic communities, such as fast-moving streams, are not highly productive. Because the moving water washes away plankton, the photosynthesis that supports the community is limited to algae attached to the surface and to rooted plants. The Productivity of Lakes Lakes can be divided into two categories based on their production of organic matter. Eutrophic lakes contain an abundant supply of minerals and organic matter. As the plentiful organic material drifts below the thermocline from the well-illuminated surface waters of the lake, it pro- vides a source of energy for other organisms. Most of these are oxygen-requiring organisms that can easily deplete the oxygen supply below the thermocline during the summer months. The oxygen supply of the deeper waters cannot be replenished until the layers mix in the fall. This lack of oxy- gen in the deeper waters of some lakes may have profound effects, such as allowing relatively harmless materials such as sulfates and nitrates to convert into toxic materials such as hydrogen sulfide and ammonia. In oligotrophic lakes, organic matter and nutrients are relatively scarce. Such lakes are often deeper than eu- trophic lakes and have very clear blue water. Their hy- polimnetic water is always rich in oxygen. Human activities can transform oligotrophic lakes into eutrophic ones. In many lakes, phosphorus is in short supply and is the nutrient that limits growth. When ex- cess phosphorus from sources such as fertilizer runoff, sewage, and detergents enters lakes, it can quickly lead to harmful effects. In many cases, this leads to perfect con- ditions for the growth of blue-green algae, which prolif- erate immensely. Soon, larger plants are outcompeted and disappear, along with the animals that live on them. In addition, as these phytoplankton die and decompose, oxygen in the water is used up, killing the natural fish and invertebrate populations. This situation can be reme- died if the continual input of phosphorus can be dimin- ished. Given time, lakes can recover and return to pre- pollution states, as happened with Lake Washington pictured in figure 29.24. The Productivity of Wetlands Swamps, marshes, bogs, and other wetlands covered with water support a wide variety of water-tolerant plants, called hydrophytes (“water plants”), and a rich di- versity of invertebrates, birds, and other animals. Wet- lands are among the most productive ecosystems on earth (table 29.2). They also play a key ecological role by pro- viding water storage basins that moderate flooding. Many wetlands are being disrupted by human “development” of what is sometimes perceived as otherwise useless land, but government efforts are now underway to protect the remaining wetlands. The most productive freshwater ecosystems are wetlands. Most lakes are far less productive, limited by lack of nutrients. Chapter 29 The Biosphere 609 Table 29.2 The Most Productive Ecosystems Net Primary Productivity Ecosystem per Unit Area (g/m 2 ) Coral reefs 2500 Tropical rain forest 2200 Wetlands 2000 Tropical seasonal forest 1600 Estuaries 1500 Temperate evergreen forest 1300 Temperate deciduous forest 1200 Savanna 900 Boreal forest 800 Cultivated land 650 Continental shelf 360 Lake and stream 250 Open ocean 125 Extreme desert, rock, sand, and ice 3 Source: Whitaker, 1975. FIGURE 29.24 Oligotrophic lakes are highly susceptible to pollution. Lake Washington is an oligotrophic lake near Seattle, Washington. The drainage from fertilizers applied to the plantings around residences, business concerns, and recreational facilities bordering the lake poses an ever-present threat to its deep blue water. By supplying phosphorus, the drainage promotes algal growth. Aerobic bacteria decomposing dead algae deplete the lake’s oxygen, killing much of the lake’s life. ? Biosphere Introduction ? Biosphere Quiz ? Climate 610 Part VIII The Global Environment Chapter 29 Summary Questions Media Resources 29.1 Organisms must cope with a varied environment. ? Organisms employ physiological, morphological, and behavioral mechanisms to cope with variations in the environment. 1. What are several ways that individual organisms adjust to changes in temperature during the course of a year? ? Warm air rises near the equator and flows toward the poles, descending at about 30° north and south latitude. Because the air falls in these regions, it is warmed, and its moisture-holding capacity increases. The great deserts of the world are formed in these drier latitudes. 2. Why are the majority of great deserts located near 30° north and south latitude? Is it more likely that a desert will form in the interior or at the edge of a continent? Explain why. 29.2 Climate shapes the character of ecosystems. ? The world’s major biomes, or terrestrial communities, can be grouped into eight major categories. These are (1) tropical rain forest; (2) savanna; (3) desert; (4) temperate grassland; (5) temperate deciduous forest; (6) temperate evergreen forest; (7) taiga; and (8) tundra. 3. What is a biome? What are the two key physical factors that affect the distribution of biomes across the earth? 29.3 Biomes are widespread terrestrial ecosystems. ? The ocean contains three major environments: the neritic zone, the pelagic zone, and the benthic zone. ? The neritic zone, which lies along the coasts, is small in area but very productive and rich in species. ? The surface layers of the pelagic zone are home to plankton (drifting organisms) and nekton (actively swimming ones). The productivity of this zone has been underestimated because of the very small size (less than 10 mm) of many of its key organisms and because of its rapid turnover of nutrients. ? The benthic zone is home to a surprising number of species. ? Freshwater habitats constitute only about 2.1% of the earth’s surface; most are ponds and lakes. These possess a littoral zone, a limnetic zone, and a profundal zone. The waters in these zones mix seasonally, delivering oxygen to the bottom and nutrients to the surface. 4. What is the difference between plankton and nekton in the ocean’s pelagic zone? How important are the photosynthetic plankton to the survival of the earth? Is the turnover of nutrients in the surface zone slow or fast? 5. What conditions of the abyssal zone led early deep-sea biologists to believe nothing lived there? What provides the energy for the deep-sea communities found around thermal vents? What kind of organisms live there? 6. Does much diversity occur in the abyssal zone? How are such ecosystems supported in the absence of light? 7. What is the difference between a eutrophic and an oligotrophic lake? Why have humans increased the frequency of lakes becoming eutrophied? 29.4 Aquatic ecosystems cover much of the earth. www.mhhe.com/raven6e www.biocourse.com ? Four Seasons ? Global Air Circulation ? Rainshadow Effect ? Weather ? Soils ? Land Biomes ? Tropical Forests ? Temperate Forests ? Book Review: Savages by Kane ? El Nino Southern Oscillation ? Aquatic Systems ? Weather ? Student Research: Exotic Species and Freshwater Ecology ? On Science Article: Cold Winter in St. Louis 611 30 The Future of the Biosphere Concept Outline 30.1 The world’s human population is growing explosively. A Growing Population. The world’s population of 6 billion people is growing rapidly and at current rates will double in 39 years. 30.2 Improvements in agriculture are needed to feed a hungry world. The Future of Agriculture. Much of the effort in searching for new sources of food has focused on improving the productivity of existing crops. 30.3 Human activity is placing the environment under increasing stress. Nuclear Power. Nuclear power, a plentiful source of energy, is neither cheap nor safe. Carbon Dioxide and Global Warming. The world’s industrialization has led to a marked increase in the atmosphere’s level of CO 2 , with resulting warming of climates. Pollution. Human industrial and agricultural activity introduces significant levels of many harmful chemicals into ecosystems. Acid Precipitation. Burning of cheap high-sulfur coal has introduced sulfur to the upper atmosphere, where it combines with water to form sulfuric acid that falls back to earth, harming ecosystems. The Ozone Hole. Industrial chemicals called CFCs are destroying the atmosphere’s ozone layer, removing an essential shield from the sun’s UV radiation. Destruction of the Tropical Forests. Much of the world’s tropical forest is being destroyed by human activity. 30.4 Solving environmental problems requires individual involvement. Environmental Science. The commitment of one person often makes a key difference in solving environmental problems. Preserving Nonreplaceable Resources. Three key nonreplaceable resources are topsoil, groundwater, and biodiversity. T he view of New York City in figure 30.1 was pho- tographed from a satellite in the spring of 1985. At the moment this picture was taken, millions of people within its view were talking, hundreds of thousands of cars were struggling through traffic, hearts were being broken, babies born, and dead people buried. Our futures and those of everyone on the planet are linked to the unseen millions in this photograph, for we share the earth with them. A lot of people consume a lot of food and water, use a great deal of energy and raw materials, and produce a great deal of waste. They also have the potential to solve the problems that arise in an increasingly crowded world. In this chapter, we will study how human life affects the environment and how the efforts being mounted can lessen the adverse im- pact and increase the potential benefits of our burgeoning population. FIGURE 30.1 New York City by satellite. trialized countries will constitute a smaller and smaller proportion of the world’s population. If India, with a 1995 population level of about 930 million people (36% under 15 years old), managed to reach a simple replacement re- productive rate by the year 2000, its population would still not stop growing until the middle of the twenty-first cen- tury. At present rates of growth, India will have a popula- tion of nearly 1.4 billion people by 2025 and will still be growing rapidly. 612 Part VII The Global Environment A Growing Population The current world population of 6 billion people is plac- ing severe strains on the biosphere. How did it grow so large? For the past 300 years, the human birthrate (as a global average) has remained nearly constant, at about 30 births per year per 1000 people. Today it is about 25 births per year per 1000 people. However, at the same time, better sanitation and improved medical techniques have caused the death rate to fall steadily, from about 29 deaths per 1000 people per year to 13 per 1000 per year. Thus, while the birthrate has remained fairly constant and may have even decreased slightly, the tremendous fall in the death rate has produced today’s enormous pop- ulation. The difference between the birth and death rates amounts to an annual worldwide increase of approxi- mately 1.4%. This rate of increase may seem relatively small, but it would double the world’s population in only 39 years! The annual increase in world population today is nearly 77 million people, about equal to the current population of Germany. 210,000 people are added to the world each day, or more than 140 every minute! The world population is expected to continue beyond its current level of 6 billion people, perhaps stabilizing at a figure anywhere between 8.5 billion and 20 billion during the next century. The Future Situation About 60% of the people in the world live in tropical or subtropical regions (figure 30.2). An additional 20% will be living in China, and the remaining 20% in the developed or industrialized countries: Europe, the successor states of the Soviet Union, Japan, United States, Canada, Australia, and New Zealand. Although populations of industrialized countries are growing at an annual rate of about 0.3%, those of the developing, mostly tropical countries (exclud- ing China) are growing at an annual rate estimated in 1995 to be about 2.2%. For every person living in an industrial- ized country like the United States in 1950, there were two people living elsewhere; in 2020, just 70 years later, there will be five. As you learned in chapter 24, the age structure of a population determines how fast the population will grow. To predict the future growth patterns of a population, it is essential to know what proportion of its individuals have not yet reached childbearing age. In industrialized coun- tries such as the United States, about a fifth of the popula- tion is under 15 years of age; in developing countries such as Mexico, the proportion is typically about twice as high. Even if most tropical and subtropical countries consis- tently carry out the policies they have established to limit population growth, their populations will continue to grow well into the twenty-first century (figure 30.3), and indus- 30.1 The world’s human population is growing explosively. 1950 100 1,000 10,000 2000 2050 Year Projected population (millions) 2100 2150 World Asia Sub-Saharan Africa Latin America U.S. Russia Japan Europe FIGURE 30.2 Anticipated growth of the global human population. Despite considerable progress in lowering birthrates, the human population will continue to grow for another century (data are presented above on a log scale). Much of the growth will center in sub-Saharan Africa, the poorest region on the globe, where the population could reach over 2 billion. Fertility rates there currently range from 3 to more than 5 children per woman, compared to fewer than 2.1 in Europe and the United States. Population Growth Rate Starting to Decline The United Nations has announced that the world popula- tion growth rate continues to decline, down from a high of 2.0% in the period 1965–1970 to 1.4% in 1998. Nonethe- less, because of the larger population, this amounts to an increase of 77 million people per year to the world popula- tion, compared to 53 million per year in the 1960s. The U.N. attributes the decline to increased family planning efforts and the increased economic power and so- cial status of women. While the U.N. applauds the United States for leading the world in funding family planning programs abroad, some oppose spending money on inter- national family planning. The opposition states that money is better spent on improving education and the economy in other countries, leading to an increased aware- ness and lowered fertility rates. The U.N. certainly sup- ports the improvement of education programs in develop- ing countries, but, interestingly, it has reported increased education levels following a decrease in family size as a re- sult of family planning. Most countries are devoting considerable attention to slowing the growth rate of their populations, and there are genuine signs of progress. If these efforts are main- tained, the world population may stabilize sometime in the next century. No one knows how many people the planet can support, but we clearly already have more peo- ple than can be sustainably supported with current technologies. However, population size is not the only factor that de- termines resource use; per capita consumption is also im- portant. In this respect, we in the developing world need to pay more attention to lessening the impact each of us makes, because, even though the vast majority of the world’s population is in developing countries, the vast ma- jority of resource consumption occurs in the developed world. Indeed, the wealthiest 20% of the world’s popula- tion accounts for 86% of the world’s consumption of re- sources and produces 53% of the world’s carbon dioxide emissions, whereas the poorest 20% of the world is respon- sible for only 1.3% of consumption and 3% of CO 2 emis- sions. Looked at another way, in terms of resource use, a child born today in the developed world will consume as many resources over the course of his or her life as 30 to 50 children born in the developing world. Building a sustainable world is the most important task facing humanity’s future. The quality of life available to our children in the next century will depend to a large extent on our success both in limiting population growth and the amount of per capita resource consumption. In 1998, the global human population of 6 billion people was growing at a rate of approximately 1.4% annually. At that rate, the population would double in 39 years. Growth rates, however, are declining, but consumption per capita in the developing world is also a significant drain on resources. Chapter 30 The Future of the Biosphere 613 FIGURE 30.3 Population growth is highest in tropical and subtropical countries. Mexico City, the world’s largest city, has well over 20 million inhabitants. The Future of Agriculture One of the greatest and most immediate challenges facing today’s world is producing enough food to feed our ex- panding population. This problem is often not appreciated by economists, who estimate that world food production has expanded 2.6 times since 1950, more rapidly than the human population. However, virtually all land that can be cultivated is already in use, and much of the world is popu- lated by large numbers of hungry people who are rapidly destroying the sustainable productivity of the lands they in- habit. Well over 20% of the world’s topsoil has been lost from agricultural lands since 1950. In the face of these mas- sive problems, we need to consider what the prospects are for increased agricultural productivity in the future. Finding New Food Plants How many food plants do we use at present? Just three species—rice, wheat, and corn—supply more than half of all human energy requirements. Just over 100 kinds of plants supply over 90% of the calories we consume. Only about 5000 have ever been used for food. There may be tens of thousands of additional kinds of plants, among the 250,000 known species, that could be used for human food if their properties were fully explored and they were brought into cultivation (figure 30.4). Agricultural scientists are attempting to identify such new crops, especially ones that will grow well in the tropics and subtropics, where the world’s population is expanding most rapidly. Nearly all major crops now grown in the world have been cultivated for hundreds or even thousands of years. Only a few, including rubber and oil palms, have entered widespread cultivation since 1800. One key feature for which nearly all of our important crops were first selected was ease of growth by relatively simple methods. Today, however, techniques of cultivation are far more sophisticated and are able to improve soil fer- tility and combat pests. This enables us to consider many more plants as potential crops. Agricultural scientists are searching systematically for new crops that fit the multiple needs of modern society, in ways that would not have been considered earlier. Improving the Productivity of Today’s Crops Searching for new crops is not a quick process. While the search proceeds, the most promising strategy to quickly ex- pand the world food supply is to improve the productivity of crops that are already being grown. Much of the im- 614 Part VII The Global Environment 30.2 Improvements in agriculture are needed to feed a hungry world. FIGURE 30.4 New food plants. (a) Grain amaranths (Amaranthus spp.) were important crops in the Latin American highlands during the days of the Incas and Aztecs. Grain amaranths are fast-growing plants that produce abundant grain rich in lysine, an amino acid rare in plant proteins but essential for animal nutrition. (b) The winged bean (Psophocarpus tetragonolobus) is a nitrogen-fixing tropical vine that produces highly nutritious leaves and tubers whose seeds produce large quantities of edible oil. First cultivated in New Guinea and Southeast Asia, the winged bean has spread since the 1970s throughout the tropics. (a) (b) provement in food production must take place in the trop- ics and subtropics, where the rapidly growing majority of the world’s population lives, including most of those en- during a life of extreme poverty. These people cannot be fed by exports from industrial nations, which contribute only about 8% of their total food at present and whose agricultural lands are already heavily exploited. During the 1950s and 1960s, the so-called Green Revolution intro- duced new, improved strains of wheat and rice. The pro- duction of wheat in Mexico increased nearly tenfold be- tween 1950 and 1970, and Mexico temporarily became an exporter of wheat rather than an importer. During the same decades, food production in India was largely able to outstrip even a population growth of approximately 2.3% annually, and China became self-sufficient in food. Despite the apparent success of the Green Revolution, improvements were limited. Raising the new agricultural strains of plants requires the expenditure of large amounts of energy and abundant supplies of fertilizers, pesticides, and herbicides, as well as adequate machinery. For exam- ple, in the United States it requires about 1000 times as much energy to produce the same amount of wheat pro- duced from traditional farming methods in India. Biologists are playing a crucial role in improving exist- ing crops and in developing new ones by applying tradi- tional methods of plant breeding and selection to many new, nontraditional crops in the tropics and subtropics (see figure 30.4). Genetic Engineering to Improve Crops Genetic engineering techniques (discussed in chapter 19) make it possible to produce plants resistant to specific her- bicides. These herbicides can then control weeds much more effectively, without damaging crop plants. Genetic engineers are also developing new strains of plants that will grow successfully in areas where they previously could not grow. Desirable characteristics are being introduced into important crop plants. Genetically modified rice, for exam- ple, is no longer deficient in ascorbic acid and iron, provid- ing a major improvement in human nutrition. Other modi- fications allow crops to tolerate irrigation with salt water, fix nitrogen, carry out C 4 photosynthesis, and produce sub- stances that deter pests and diseases. Genetically modified crops (so-called GM foods) have proven to be a highly controversial issue, one currently being debated in legislative bodies all over the globe. Crit- ics fear loss of genetic diversity, escape of engineered vari- eties into the environment, harm to insects feeding near GM crops, undo influence of seed companies, and many other real or imagined potential problems. The issue of risk is assessed in chapter 19. While risks must be carefully con- sidered, the ability to transfer genes between organisms, first accomplished in a laboratory in 1973, has tremendous potential for the improvement of crop plants as the twenty- first century opens. New Approaches to Cultivation Several new approaches may improve crop production. “No-till” agriculture, spreading widely in the United States and elsewhere in the 1990s, conserves topsoil and so is a desirable agricultural practice for many areas. On the other hand, hydroponics, the cultivation of plants in water containing an appropriate mixture of nutrients, holds less promise. It does not differ remarkably in its re- quirements and challenges from growing plants on land. It requires as much fertilizer and other chemicals, as well as the water itself. The oceans were once regarded as an inexhaustible source of food, but overexploitation of their resources is limiting the world catch more each year, and these catches are costing more in terms of energy. Mismanagement of fisheries, mainly through overfishing, local pollution, and the destruction of fish breeding and feeding grounds, has lowered the catch of fish in the sea by about 20% from maximum levels. Many fishing areas that were until re- cently important sources of food have been depleted or closed. For example, the Grand Banks in the North At- lantic Ocean off Newfoundland, a major source of cod and other fish, are now nearly depleted. In 1994, the Canadian government prohibited all cod fishing there indefinitely, throwing 27,000 fishermen out of work, and the United States government banned all fishing on Georges Bank and other defined New England waters. Populations of At- lantic bluefin tuna have dropped 90% since 1975. The United Nations Food and Agriculture organization esti- mated in 1993 that 13 of 17 major ocean fisheries are in trouble, with the annual marine fish catch dropping from 86 million metric tons in 1986 to 82.5 million tons by 1992 and continuing to fall each year as the intensity of the fishing increases. The development of new kinds of food, such as mi- croorganisms cultured in nutrient solutions, should defi- nitely be pursued. For example, the photosynthetic, nitrogen-fixing cyanobacterium Spirulina is being investi- gated in several countries as a possible commercial food source. It is a traditional food in Africa, Mexico, and other regions. Spirulina thrives in very alkaline water, and it has a higher protein content than soybeans. Ponds in which it grows are 10 times more productive than wheat fields. Such protein-rich concentrates of microorganisms could provide important nutritional supplements. How- ever, psychological barriers must be overcome to per- suade people to eat such foods, and the processing re- quired tends to be energy-expensive. Just over 100 kinds of plants, out of the roughly 250,000 known, supply more than 90% of all the calories we consume. Many more could be developed by a careful search for new crops. Chapter 30 The Future of the Biosphere 615 The simplest way to gain a feeling for the dimensions of the global environmental problem we face is simply to scan the front pages of any newspaper or news magazine or to watch television. Although they are only a sam- pling, features selected by these media teach us a great deal about the scale and complexity of the challenge we face. We will discuss a few of the most important issues here. Nuclear Power At 1:24 A.M. on April 26, 1986, one of the four reactors of the Chernobyl nuclear power plant blew up. Located in Ukraine 100 kilometers north of Kiev, Chernobyl was one of the largest nuclear power plants in Europe, producing 1000 megawatts of electricity, enough to light a medium- sized city. Before dawn on April 26, workers at the plant hurried to complete a series of tests of how Reactor Num- ber 4 performed during a power reduction and took a fool- ish short-cut: they shut off all the safety systems. Reactors at Chernobyl were graphite reactors designed with a series of emergency systems that shut the reactors down at low power, because the core is unstable then—and these are the emergency systems the workers turned off. A power surge occurred during the test, and there was nothing to dampen it. Power zoomed to hundreds of times the maximum, and a white-hot blast with the force of a ton of dynamite par- tially melted the fuel rods and heated a vast head of steam that blew the reactor apart. The explosion and heat sent up a plume 5 kilometers high, carrying several tons of uranium dioxide fuel and fis- sion products. The blast released over 100 megacuries of radioactivity, making it the largest nuclear accident ever reported; by comparison, the Three Mile Island accident in Pennsylvania in 1979 released 17 curies, millions of times less. This cloud traveled first northwest, then south- east, spreading the radioactivity in a band across central Europe from Scandinavia to Greece. Within a 30-kilome- ter radius of the reactor, at least one-fifth of the popula- tion, some 24,000 people, received serious radiation doses (greater than 45 rem). Thirty-one individuals died as a di- rect result of radiation poisoning, most of them firefight- ers who succeeded in preventing the fire from spreading to nearby reactors. The rest of Europe received a much lower but still sig- nificant radiation dose. Data indicate that, because of the large numbers of people exposed, radiation outside of the immediate Chernobyl area can be expected to cause from 5000 to 75,000 cancer deaths. The Promise of Nuclear Power Our industrial society has grown for over 200 years on a diet of cheap energy. Until recently, much of this energy has been derived from burning wood and fossil fuels: coal, gas, and oil. However, as these sources of fuel be- come increasingly scarce and the cost of locating and ex- tracting new deposits becomes more expensive, modern society is being forced to look elsewhere for energy. The great promise of nuclear power is that it provides an al- ternative source of plentiful energy. Although nuclear power is not cheap—power plants are expensive to build and operate—its raw material, uranium ore, is so com- mon in the earth’s crust that it is unlikely we will ever run out of it. Burning coal and oil to obtain energy produces two un- desirable chemical by-products: sulfur and carbon dioxide. The sulfur emitted from burning coal is a principal cause of acid rain, while the CO 2 produced from burning all fossil fuels is a major greenhouse gas (see the discussion of global warming in the next section). For these reasons, we need to find replacements for fossil fuels. For all of its promise of plentiful energy, nuclear power presents several new problems that must be ad- dressed before its full potential can be realized. First, safe operation of the world’s approximately 390 nuclear reac- tors must be ensured. A second challenge is the need to safely dispose of the radioactive wastes produced by the plants and to safely decommission plants that have reached the end of their useful lives (about 25 years). In 1997, over 35 plants were more than 25 years old, and not one has been safely decommissioned, its nuclear wastes disposed of. A third challenge is the need to guard against terrorism and sabotage, because the technology of nuclear power generation is closely linked to that of nu- clear weapons. For these reasons, it is important to continue to inves- tigate and develop other promising alternatives to fossil fuels, such as solar energy and wind energy. The genera- tion of electricity by burning fossil fuels accounts for up to 15% of global warming gas emissions in the United States. As much as 75% of the electricity produced in the United States and Canada currently is wasted through the use of inefficient appliances, according to scientists at Lawrence Berkeley Laboratory. Using highly efficient motors, lights, heaters, air conditioners, refrigerators, and other technologies already available could save huge amounts of energy and greatly reduce global warming gas emission. For example, a new, compact fluorescent light bulb uses only 20% of the amount of electricity a conven- tional light bulb uses, provides equal or better lighting, lasts up to 13 times longer, and provides substantial cost savings. Nuclear power offers plentiful energy for the world’s future, but its use involves significant problems and dangers. 616 Part VII The Global Environment 30.3 Human activity is placing the environment under increasing stress. Carbon Dioxide and Global Warming By studying earth’s history and mak- ing comparisons with other planets, scientists have determined that con- centrations of gases in the atmo- sphere, particularly carbon dioxide, maintain the average temperature on earth about 25°C higher than it would be if these gases were absent. Carbon dioxide and other gases trap the longer wavelengths of infrared light, or heat, radiating from the surface of the earth, creating what is known as a greenhouse effect (fig- ure 30.5). The atmosphere acts like the glass of a gigantic greenhouse surrounding the earth. Roughly seven times as much car- bon dioxide is locked up in fossil fuels as exists in the atmosphere today. Before industrialization, the concentration of carbon dioxide in the atmosphere was approximately 260 to 280 parts per million (ppm). Since the extensive use of fossil fuels, the amount of carbon dioxide in the atmosphere has been increas- ing rapidly. During the 25-year pe- riod starting in 1958, the concentra- tion of carbon dioxide increased from 315 ppm to more than 340 ppm and continues to rise. Climatol- ogists have calculated that the actual mean global temperature has in- creased about 1°C since 1900, a change known as global warming. In a recent study, the U.S. Na- tional Research Council estimated that the concentration of carbon dioxide in the atmosphere would pass 600 ppm (roughly double the current level) by the third quarter of the next century, and might exceed that level as soon as 2035. These concentrations of carbon dioxide, if actually reached, would warm global surface air by between 1.5° and 4.5°C. The actual increase might be considerably greater, however, because a number of trace gases, such as nitrous oxide, methane, ozone, and chlorofluorocar- bons, are also increasing rapidly in the atmosphere as a result of human activities. These gases have warming, or “greenhouse,” effects similar to those of carbon dioxide. One, methane, increased from 1.14 ppm in the atmo- sphere in 1951 to 1.68 ppm in 1986—nearly a 50% increase. Major problems associated with climatic warming in- clude rising sea levels. Sea levels may have already risen 2 to 5 centimeters from global warming. If the climate be- comes so warm that the polar ice caps melt, sea levels would rise by more than 150 meters, flooding the entire Atlantic coast of North America for an average distance of several hundred kilometers inland. Changes in the distribution of precipitation are difficult to model. Certainly, changing climatic patterns are likely to make some of the best farmlands much drier than they are at present. If the climate warms as rapidly as many scien- tists project, the next 50 years may see greatly altered weather patterns, a rising sea level, and major shifts of deserts and fertile regions. As the global concentration of carbon dioxide increases, the world’s temperature is rising, with great potential impact on the world’s climate. Chapter 30 The Future of the Biosphere 617 '58 316 312 320 324 60.5 328 332 336 340 344 348 352 60 61 59.5 59 58.5 58 356 360 364 368 372 '60 '62 '64 '66 '68 '70 '72 '74 '76 '78 Year (1900s) Carbon dioxide concentration (parts per million) T emperature (degrees Fahrenheit) '80 '82 '84 '86 '88 '90 '92 '94 '96 '97 '98 '99 '2000 Average mean global temperature, 1958–1996 FIGURE 30.5 The greenhouse effect. The concentration of carbon dioxide in the atmosphere has steadily increased since the 1950s (blue line). The red line shows the general increase in average global temperature for the same period of time. Source: Data from Geophysical Monograph, American Geophysical Union, National Academy of Sciences, and National Center for Atmospheric Research. Pollution The River Rhine is a broad ribbon of water that runs through the heart of Europe. From high in the Alps that separate Italy and Switzerland, the Rhine flows north across the industrial regions of Germany before reaching Holland and the sea. Where it crosses the mountains be- tween Mainz and Coblenz, Germany, the Rhine is one of the most beautiful rivers on earth. On the first day of No- vember 1986, the Rhine almost died. The blow that struck at the life of the Rhine did not at first seem deadly. Firefighters were battling a blaze that morning in Basel, Switzerland. The fire was gutting a huge warehouse, into which firefighters shot streams of water to dampen the flames. The warehouse belonged to Sandoz, a giant chemical company. In the rush to contain the fire, no one thought to ask what chemicals were stored in the warehouse. By the time the fire was out, streams of water had washed 30 tons of mercury and pes- ticides into the Rhine. Flowing downriver, the deadly wall of poison killed everything it passed. For hundreds of kilometers, dead fish blanketed the surface of the river. Many cities that use the water of the Rhine for drinking had little time to make other arrangements. Even the plants in the river began to die. All across Germany, from Switzerland to the sea, the river reeked of rotting fish, and not one drop of water was safe to drink. Six months later, Swiss and German environmental sci- entists monitoring the effects of the accident were able to report that the blow to the Rhine was not mortal. Enough small aquatic invertebrates and plants had survived to pro- vide a basis for the eventual return of fish and other water life, and the river was rapidly washing out the remaining residues from the spill. A lesson difficult to ignore, the spill on the Rhine has caused the governments of Germany and Switzerland to intensify efforts to protect the river from fu- ture industrial accidents and to regulate the growth of chemical and industrial plants on its shores. The Threat of Pollution The pollution of the Rhine is a story that can be told countless times in different places in the industrial world, from Love Canal in New York to the James River in Vir- ginia to the town of Times Beach in Missouri. Nor are all pollutants that threaten the sustainability of life immedi- ately toxic. Many forms of pollution arise as by-products of industry. For example, the polymers known as plastics, which we produce in abundance, break down slowly in na- ture. Much is burned or otherwise degraded to smaller vinyl chloride units. Virtually all of the plastic that has ever been produced is still with us, in one form or another. Col- lectively, it constitutes a new form of pollution. Widespread agriculture, carried out increasingly by modern methods, introduces large amounts of many new kinds of chemicals into the global ecosystem, including pesticides, herbicides, and fertilizers. Industrialized coun- tries like the United States now attempt to carefully moni- tor side effects of these chemicals. Unfortunately, large quantities of many toxic chemicals no longer manufactured still circulate in the ecosystem. For example, the chlorinated hydrocarbons, a class of compounds that includes DDT, chlordane, lindane, and dieldrin, have all been banned for normal use in the United States, where they were once widely used. They are still manufactured in the United States, however, and exported to other countries, where their use continues. Chlorinated hydrocarbon molecules break down slowly and accumulate in animal fat. Furthermore, as they pass through a food chain, they become increasingly concentrated in a process called biological magnification (figure 30.6). DDT caused serious problems by leading to the production of thin, frag- ile eggshells in many predatory bird species in the United States and elsewhere until the late 1960s, when it was banned in time to save the birds from extinction. Chlori- nated compounds have other undesirable side effects and exhibit hormonelike activities in the bodies of animals, dis- rupting normal hormonal cycles with sometimes poten- tially serious consequences. Chemical pollution is causing ecosystems to accumulate many harmful substances, as the result of spills and runoff from agricultural or urban use. 618 Part VII The Global Environment DDT Concentration 25 ppm in predatory birds 2 ppm in large fish 0.5 ppm in small fish 0.04 ppm in zooplankton 0.000003 ppm in water FIGURE 30.6 Biological magnification of DDT. Because DDT accumulates in animal fat, the compound becomes increasingly concentrated in higher levels of the food chain. Before DDT was banned in the United States, predatory bird populations drastically declined because DDT made their eggshells thin and fragile enough to break during incubation. Acid Precipitation The Four Corners power plant in New Mexico burns coal, sending smoke up high into the atmosphere through its smokestacks, each over 65 meters tall. The smoke the stacks belch out contains high concentrations of sulfur dioxide and other sulfates, which produce acid when they combine with water vapor in the air. The intent of those who designed the plant was to release the sulfur-rich smoke high in the atmosphere, where winds would disperse and dilute it, carrying the acids far away. Environmental effects of this acidity are serious. Sul- fur introduced into the upper atmosphere combines with water vapor to produce sulfuric acid, and when the water later falls as rain or snow, the precipitation is acid. Nat- ural rainwater rarely has a pH lower than 5.6; in the northeastern United States, however, rain and snow now have a pH of about 3.8, roughly 100 times as acid (figure 30.7). Acid precipitation destroys life. Thousands of lakes in southern Sweden and Norway no longer support fish; these lakes are now eerily clear. In the northeastern United States and eastern Canada, tens of thousands of lakes are dying biologically as a result of acid precipitation. At pH levels below 5.0, many fish species and other aquatic ani- mals die, unable to reproduce. In southern Sweden and elsewhere, groundwater now has a pH between 4.0 and 6.0, as acid precipitation slowly filters down into the under- ground reservoirs. There has been enormous forest damage in the Black Forest in Germany and in the forests of the eastern United States and Canada. It has been estimated that at least 3.5 million hectares of forest in the northern hemisphere are being affected by acid precipitation (figure 30.8), and the problem is clearly growing. Its solution at first seems obvious: capture and remove the emissions instead of releasing them into the atmo- sphere. However, there are serious difficulties in executing this solution. First, it is expensive. The costs of installing and maintaining the necessary “scrubbers” in the United States are estimated to be 4 to 5 billion dollars per year. An additional difficulty is that the polluter and the recipient of the pollution are far from each other, and neither wants to pay for what they view as someone else’s problem. The Clean Air Act revisions of 1990 addressed this problem in the United States significantly for the first time, and sub- stantial worldwide progress has been made in implement- ing a solution. Industrial pollutants such as nitric and sulfuric acids, introduced into the upper atmosphere by factory smokestacks, are spread over wide areas by the prevailing winds and fall to earth with precipitation called “acid rain,’’ lowering the pH of water on the ground and killing life. Chapter 30 The Future of the Biosphere 619 Precipitation pH H110214.3H110225.3 FIGURE 30.7 pH values of rainwater in the United States. Precipitation in the United States, especially in the Northeast, is more acidic than that of natural rainwater, which has a pH of about 5.6. FIGURE 30.8 Damage to trees at Clingman’s Dome, Tennessee. Acid precipitation weakens trees and makes them more susceptible to pests and predators. The Ozone Hole The swirling colors of the satellite photos in figure 30.9 represent different concentrations of ozone (O 3 ), a differ- ent form of oxygen gas than O 2 . As you can see, over Antarctica there is an “ozone hole” three times the size of the United States, an area within which the ozone concen- tration is much less than elsewhere. The ozone thinning appeared for the first time in 1975. The hole is not a per- manent feature, but rather becomes evident each year for a few months during Antarctic winter. Every September from 1975 onward, the ozone “hole” has reappeared. Each year the layer of ozone is thinner and the hole is larger. The major cause of the ozone depletion had already been suggested in 1974 by Sherwood Roland and Mario Molina, who were awarded the Nobel Prize for their work in 1995. They proposed that chlorofluorocarbons (CFCs), relatively inert chemicals used in cooling systems, fire ex- tinguishers, and Styrofoam containers, were percolating up through the atmosphere and reducing O 3 molecules to O 2 . One chlorine atom from a CFC molecule could destroy 100,000 ozone molecules in the following mechanism: UV radiation causes CFCs to release Cl atoms: UV CCl 3 F ?→ Cl + CCl 2 F UV creates oxygen free radicals: O 2 ?→ 2O Cl atoms and O free radicals interact with ozone: 2Cl + 2O 3 ?→ 2ClO + 2O 2 2ClO + 2O ?→ 2Cl + 2O 2 Net reaction: 2O 3 ?→ 3O 2 Although other factors have also been implicated in ozone depletion, the role of CFCs is so predominant that worldwide agreements have been signed to phase out their production. The United States banned the production of CFCs and other ozone-destroying chemicals after 1995. Nonetheless, the CFCs that were manufactured earlier are moving slowly upward through the atmosphere. The ozone layer will be further depleted before it begins to form again. Thinning of the ozone layer in the stratosphere, 25 to 40 kilometers above the surface of the earth, is a matter of serious concern. This layer protects life from the harmful ultraviolet rays that bombard the earth continuously from the sun. Life appeared on land only after the oxygen layer was sufficiently thick to generate enough ozone to shield the surface of the earth from these destructive rays. Ultraviolet radiation is a serious human health concern. Every 1% drop in atmospheric ozone is estimated to lead to a 6% increase in the incidence of skin cancers. At middle latitudes, the approximately 3% drop that has already oc- curred worldwide is estimated to have increased skin can- cers by as much as 20%. A type of skin cancer (melanoma) is one of the more lethal human diseases. Industrial CFCs released into the atmosphere react at very cold temperatures with ozone, converting it to oxygen gas. This has the effect of destroying the earth’s ozone shield and exposing the earth’s surface to increased levels of harmful UV radiation. 620 Part VII The Global Environment August September September 9, 2000 October November December 0 1 2 3 4 5 6 7 8 9 10 11 12 Southern hemisphere ozone hole area (millions of square miles) 2000 1999 1990-99 average FIGURE 30.9 The ozone hole over Antarctica is still growing. For decades NASA satellites have tracked the extent of ozone depletion over Antarctica. Every year since 1979 an ozone “hole” has appeared in August when sunlight triggers chemical reactions in cold air trapped over the South Pole during Antarctic winter. The hole intensifies during September before tailing off as temperatures rise in November- December. In 2000, the 11.4 million square-mile hole (dark blue in the satellite image) covered an area larger than the United States, Canada, and Mexico combined, the largest hole ever recorded. In September 2000, the hole extended over Punta Arenas, a city of about 120,000 people southern Chile, exposing residents to very high levels of UV radiation. (a) (b) Destruction of the Tropical Forests More than half of the world’s human population lives in the tropics, and this percentage is increasing rapidly. For global stability, and for the sus- tainable management of the world ecosystem, it will be necessary to solve the problems of food production and regional stability in these areas. World trade, political and economic stability, and the future of most species of plants, animals, fungi, and microorganisms depend on our ad- dressing these problems. Rain Forests Are Rapidly Disappearing Tropical rain forests are biologically the richest of the world’s biomes. Most other kinds of tropical forest, such as seasonally dry forests and sa- vanna forests, have already been largely destroyed—because they tend to grow on more fertile soils, they were exploited by humans a long time ago. Now the rain forests, which grow on poor soils, are being de- stroyed. In the mid-1990s, it is estimated that only about 5.5 million square kilometers of tropical rain forest still exist in a relatively undisturbed form. This area, about two-thirds of the size of the United States (excluding Alaska), represents about half of the original extent of the rain forest. From it, about 160,000 square kilometers are being clear-cut every year, with perhaps an equivalent amount severely disturbed by shifting cultivation, fire- wood gathering, and the clearing of land for cattle ranch- ing. The total area of tropical rain forest destroyed—and therefore permanently removed from the world total— amounts to an area greater than the size of Indiana each year. At this rate, all of the tropical rain forest in the world will be gone in about 30 years; but in many regions, the rate of destruction is much more rapid. As a result of this overexploitation, experts predict there will be little undisturbed tropical forest left anywhere in the world by early in the next century. Many areas now occupied by dense, species-rich forests may still be tree-covered, but the stands will be sparse and species-poor. A Serious Matter Not only does the disappearance of tropical forests repre- sent a tragic loss of largely unknown biodiversity, but the loss of the forests themselves is ecologically a serious mat- ter. Tropical forests are complex, productive ecosystems that function well in the areas where they have evolved. When people cut a forest or open a prairie in the north temperate zone, they provide farmland that we know can be worked for generations. In most areas of the tropics, people are unable to engage in continuous agriculture. When they clear a tropical forest, they engage in a one- time consumption of natural resources that will never be available again (figure 30.10). The complex ecosystems built up over millions of years are now being dismantled, in almost complete ignorance, by humans. What biologists must do is to learn more about the construction of sustainable agricultural ecosystems that will meet human needs in tropical and subtropical re- gions. The ecological concepts we have been reviewing in the last three chapters are universal principles. The undis- turbed tropical rain forest has one of the highest rates of net primary productivity of any plant community on earth, and it is therefore imperative to develop ways that it can be harvested for human purposes in a sustainable, intelligent way. More than half of the tropical rain forests have been destroyed by human activity, and the rate of loss is accelerating. Chapter 30 The Future of the Biosphere 621 FIGURE 30.10 Destroying the tropical forests. (a) When tropical forests are cleared, the ecological consequences can be disastrous. These fires are destroying rain forest in Brazil and clearing it for cattle pasture. (b) The consequences of deforestation can be seen on these middle- elevation slopes in Ecuador, which now support only low-grade pastures and permit topsoil to erode into the rivers (note the color of the water, stained brown by high levels of soil erosion). These areas used to support highly productive forest, which protected the watersheds of the area, in the 1970s. (a) (b) Environmental Science Environmental scientists attempt to find solutions to en- vironmental problems, considering them in a broad con- text. Unlike biology or ecology, sciences that seek to learn general principles about how life functions, environmental science is an applied science dedicated to solving practical problems. Its basic tools are derived from ecology, geology, meteorology, social sciences, and many other areas of knowledge that bear on the functioning of the environment and our management of it. Environmental science ad- dresses the problems created by rapid human population growth: an increasing need for energy, a depletion of re- sources, and a growing level of pollution. Solving Environmental Problems The problems our severely stressed planet faces are not in- surmountable. A combination of scientific investigation and public action, when brought to bear effectively, can solve environmental problems that seem intractable. Viewed simply, there are five components to solving any environ- mental problem: 1. Assessment. The first stage in addressing any envi- ronmental problem is scientific analysis, the gather- ing of information. Data must be collected and exper- iments performed to construct a model that describes the situation. This model can be used to make predic- tions about the future course of events. 2. Risk analysis. Using the results of scientific analysis as a tool, it is possible to analyze what could be expected to happen if a particular course of action were followed. It is necessary to evaluate not only the potential for solving the environmental problem, but also any adverse effects a plan of ac- tion might create. 3. Public education. When a clear choice can be made among alternative courses of action, the public must be informed. This involves explaining the prob- lem in terms the public can understand, presenting the alternatives available, and explaining the probable costs and results of the different choices. 4. Political action. The public, through its elected officials selects a course of action and implements it. Choices are particularly difficult to implement when environmental problems transcend national boundaries. 5. Follow-through. The results of any action should be carefully monitored to see whether the environ- mental problem is being solved as well as to evaluate and improve the initial modeling of the problem. Every environmental intervention is an experiment, and we need the knowledge gained from each one to better address future problems. Individuals Can Make the Difference The development of appropriate solutions to the world’s environmental problems must rest partly on the shoulders of politicians, economists, bankers, engineers—many kinds of public and commercial activity will be required. How- ever, it is important not to lose sight of the key role often played by informed individuals in solving environmental problems. Often one person has made the difference; two examples serve to illustrate the point. The Nashua River. Running through the heart of New England, the Nashua River was severely polluted by mills established in Massachusetts in the early 1900s. By the 1960s, the river was clogged with pollution and declared ecologically dead. When Marion Stoddart moved to a town along the river in 1962, she was appalled. She approached the state about setting aside a “greenway” (trees running the length of the river on both sides), but the state wasn’t interested in buying land along a filthy river. So Stoddart organized the Nashua River Cleanup Committee and began a campaign to ban the dumping of chemicals and wastes into the river. The committee presented bottles of dirty river water to politicians, spoke at town meetings, re- cruited businesspeople to help finance a waste treatment plant, and began to clean garbage from the Nashua’s banks. This citizen’s campaign, coordinated by Stoddart, greatly aided passage of the Massachusetts Clean Water Act of 1966. Industrial dumping into the river is now banned, and the river has largely recovered. Lake Washington. A large, 86 km 2 freshwater lake east of Seattle, Lake Washington became surrounded by Seattle suburbs in the building boom following the Second World War. Between 1940 and 1953, a ring of 10 municipal sewage plants discharged their treated effluent into the lake. Safe enough to drink, the effluent was believed “harmless.” By the mid-1950s a great deal of effluent had been dumped into the lake (try multiplying 80 million liters/day × 365 days/year × 10 years). In 1954, an ecology professor at the University of Washington in Seattle, W. T. Edmondson, noted that his research students were reporting filamentous blue-green algae growing in the lake. Such algae require plentiful nutrients, which deep fresh- water lakes usually lack—the sewage had been fertilizing the lake! Edmondson, alarmed, began a campaign in 1956 to educate public officials to the danger: bacteria decom- posing dead algae would soon so deplete the lake’s oxygen that the lake would die. After five years, joint municipal taxes financed the building of a sewer to carry the effluent out to sea. The lake is now clean. In solving environmental problems, the commitment of one person can make a critical difference. 622 Part VII The Global Environment 30.4 Solving environmental problems requires individual involvement. Preserving Nonreplaceable Resources Among the many ways ecosystems are suffering damage, one class of problem stands out as more serious than the rest: consuming or destroying resources that we cannot re- place in the future. While a polluted stream can be cleaned up, no one can restore an extinct species. In the United States, we are consuming three nonreplaceable resources at alarming rates: topsoil, groundwater, and biodiversity. We will briefly discuss the first two of these in this chapter, with a more detailed discussion of biodiversity in the fol- lowing chapter. Topsoil The United States is one of the most productive agricul- tural countries on earth, largely because much of it is covered with particularly fertile soils. Our midwestern farm belt sits astride what was once a great prairie. The topsoil of that ecosystem accumulated bit by bit from countless generations of animals and plants until, by the time humans began to plow it, the rich soil extended down several feet. We can never replace this rich topsoil, the capital upon which our country’s greatness is built, yet we are al- lowing it to be lost at a rate of centimeters every decade. By repeatedly tilling (turning the soil over) to eliminate weeds, we permit rain to wash more and more of the top- soil away, into rivers, and eventually out to sea. Our country has lost one-quarter of its topsoil since 1950! New approaches are desperately needed to lessen our re- liance on intensive cultivation. Some possible solutions include using genetic engineering to make crops resistant to weed-killing herbicides and terracing to recapture lost topsoil. Groundwater A second resource we cannot replace is groundwater, water trapped beneath the soil within porous rock reser- voirs called aquifers (figure 30.11). This water seeped into its underground reservoir very slowly during the last ice age over 12,000 years ago. We should not waste this trea- sure, for we cannot replace it. In most areas of the United States, local governments exert relatively little control over the use of groundwater. As a result, a large portion is wasted watering lawns, wash- ing cars, and running fountains. A great deal more is inad- vertently polluted by poor disposal of chemical wastes— and once pollution enters the groundwater, there is no effective means of removing it. Topsoil and groundwater are essential for agriculture and other human activities. Replenishment of these resources occurs at a very slow rate. Current levels of consumption are not sustainable and will cause serious problems in the near future. Chapter 30 The Future of the Biosphere 623 Ogallala Aquifer water depths 0-30 m 30-120 m 120-350 m Denver Wichita Amarillo SOUTH DAKOTA COLORADO KANSAS OKLAHOMA TEXAS NEW MEXICO NEBRASKA FIGURE 30.11 The Ogallala Aquifer. This massive deposit of groundwater lies under eight states, mainly Texas, Kansas, and Nebraska. Excessive pumping of this water for irrigation and other uses has caused the water level to drop 30 meters in some places. Continued excessive use of this kind endangers the survival of the Ogallala Aquifer, as it takes hundreds or even thousands of years for aquifers to recharge. 624 Part VII The Global Environment Chapter 30 Summary Questions Media Resources 30.1 The world’s human population is growing explosively. ? Population growth rates are declining throughout much of the world, but still the human population increases by 77 million people per year. At this rate, the global population will double in 39 years. ? An explosively growing human population is placing considerable stress on the environment. People in the developed world consume resources at a vastly higher rate than those in the nondeveloped world. Such high levels of consumption are not sustainable and are as important a problem as global overpopulation. 1. What biological event fostered the rapid growth of human populations? How did this event affect the location in which humans lived? What major cultural event eventually took place? 2. Why, in some respects, is the population size of the developed world more of a consideration in discussing resource use than the population of the nondeveloped world? ? Much current effort is focused on improving the productivity of existing crops, although the search for new crops continues. 3. What three species supply more than half of the human energy requirements on earth? How many plants supply over 90%? 30.2 Improvements in agriculture are needed to feed a hungry world. ? Human activities present many challenges to the environment, including the release of harmful materials into the environment. ? Burning fossil fuels releases carbon dioxide, which may increase the world’s temperature and alter weather and ocean levels. ? Release of pollutants into rivers may make the water unfit for aquatic life and human consumption. ? Release of industrial smoke into the upper atmosphere leads to acid precipitation that kills forests and lakes. ? Release of chemicals such as chlorofluorocarbons may destroy the atmosphere’s ozone and expose the world to dangerous levels of ultraviolet radiation. ? Cutting and burning the tropical rain forests of the world to make pasture and cropland is producing a massive wave of extinction. 4. What problems must we master before nuclear power’s full potential can be realized? 5. Why were chlorinated hydrocarbons banned in the United States? Why can you still find them as contaminants on fruits and vegetables? 6. How does acid precipitation form? Why has it been difficult to implement solutions to this problem? 7. What is the ozone layer? How is it formed? What are the harmful effects of decreasing the earth’s ozone layer? What may be the primary cause of this damage? 30.3 Human activity is placing the environment under increasing stress. ? All of these challenges to our future can and must be addressed. Today, environmental scientists and concerned citizens are actively searching for constructive solutions to these problems. 8. What sort of action might you take that would make a significant contribution to solving the world’s environmental problems? 30.4 Solving environmental problems requires individual involvement. www.mhhe.com/raven6e www.biocourse.com ? History of Human Population ? Food Needs ? Food Production ? Future Agricultural Prospects ? Land Degradation ? Agriculture-Related Problems ? Scientists on Science: History of Life ? On Science Article: Do-It-Yourself Environmentalism ? Global Warming ? Bioaccumulation ? Acid Rain ? Ozone Layer Depletion ? Student Research: Plants and Global Warming ? On Science Article: Shrinking Sea Ice 625 31 Conservation Biology Concept Outline 31.1 The new science of conservation biology is focused on conserving biodiversity. Overview of the Biodiversity Crisis. In prehistoric times, humans decimated the faunas of many areas. Worldwide extinction rates are accelerating. Species Endemism and Hot Spots. Some geographic areas are particularly rich in species that occur nowhere else. What’s So Bad about Losing Biodiversity? Biodiversity is of considerable direct economic value, and provides key support to the biosphere. 31.2 Vulnerable species are more likely to become extinct. Predicting Which Species Are Vulnerable to Extinction. Biologists carry out population viability analyses to assess danger of extinction. Dependence upon Other Species. Extinction of one species can have a cascading effect throughout the food web, making other species vulnerable as well. Categories of Vulnerable Species. Declining population size, loss of genetic variation, and commercial value all tend to increase a species’ vulnerability. 31.3 Causes of endangerment usually reflect human activities. Factors Responsible for Extinction. Most recorded extinctions can be attributed to a few causes. Habitat Loss. Without a place to live, species cannot survive. Case Study: Overexploitation Case Study: Introduced Species Case Study: Disruption of Ecological Relationships Case Study: Loss of Genetic Variation Case Study: Habitat Loss and Fragmentation 31.4 Successful recovery plans will need to be multidimensional. Many Approaches Exist for Preserving Endangered Species. Species recovery requires restoring degraded habitats, breeding in captivity, maintaining population diversity, and maintaining keystone species. Conservation of Ecosystems. Maintaining large preserves and focusing on the health of the entire ecosystem may be the best means of preserving biodiversity. A mong the greatest challenges facing the biosphere is the accelerating pace of species extinctions—not since the Cretaceous have so many species become extinct in so short a period of time (figure 31.1). This challenge has led to the emergence in the last decade of the new discipline of conservation biology. Conservation biology is an applied discipline that seeks to learn how to preserve species, com- munities, and ecosystems. It both studies the causes of de- clines in species richness and attempts to develop methods to prevent such declines.In this chapter we will first exam- ine the biodiversity crisis and its importance. Then, we will assess the sorts of species which seem vulnerable to extinc- tion. Using case histories, we go on to identify and study five factors that have played key roles in many extinctions. We finish with a review of recovery efforts at the species and community level. FIGURE 31.1 Endangered. The Siberian tiger is in grave danger of extinction, hunted for its pelt and having its natural habitat greatly reduced. A concerted effort is being made to save it, using many of the ap- proaches discussed in this chapter. Similar results have followed the arrival of humans around the globe. Forty thousand years ago, Australia was occupied by a wide variety of large animals, including mar- supials similar in size and ecology to hippos and leopards, a kangaroo nine feet tall, and a 20-foot-long monitor lizard. These all disappeared, at approximately the same time as humans arrived. Smaller islands have also been devastated. On Madagscar, at least 15 species of lemurs, including one the size of a gorilla, a pygmy hippopotamus , and the flight- less elephant bird, Aepyornis, the largest bird to ever live (more than 3 meters tall and weighing 450 kilograms) all perished. On New Zealand, 30 species of birds went extinct, including all 13 species of moas, another group of large, flightless birds. Interestingly, one continent that seems to have been spared these megafaunal extinctions is Africa. Sci- entists speculate that this lack of extinction in prehistoric Africa may have resulted because much of human evolution occurred in Africa. Consequently, other African species had been coevolving with humans for several million years and thus had evolved counteradaptations to human predation. Extinctions in Historical Time Historical extinction rates are best known for birds and mammals because these species are conspicuous—rela- tively large and well studied. Estimates of extinction rates for other species are much rougher. The data presented 626 Part VIII The Global Environment Overview of the Biodiversity Crisis Extinction is a fact of life, as normal and nec- essary as species formation is to a stable world ecosystem. Most species, probably all, go extinct eventually. More than 99% of species known to science (most from the fos- sil record) are now extinct. However, current rates are alarmingly high. Taking into ac- count the rapid and accelerating loss of habi- tat that is occurring at present, especially in the tropics, it has been calculated that as much as 20% of the world’s biodiversity may be lost during the next 30 years. In addition, many of these species may be lost before we are even aware of their extinction. Scientists estimate that no more than 15% of the world’s eukaryotic organisms have been dis- covered and given scientific names, and this proportion probably is much lower for tropi- cal species. These losses will not just affect poorly known groups. As many as 50,000 species of the world’s total of 250,000 species of plants, 4000 of the world’s 20,000 species of butter- flies, and nearly 2000 of the world’s 9000 species of birds could be lost during this short period of time. Considering that our species has been in existence for only 500,000 years of the world’s 4.5-billion-year history, and that our ancestors developed agriculture only about 10,000 years ago, this is an astonishing—and dubious—accomplishment. Extinctions Due to Prehistoric Humans A great deal can be learned about current rates of extinction by studying the past, and in particular the impact of human- caused extinctions. In prehistoric times, Homo sapiens wreaked havoc whenever they entered a new area. For ex- ample, at the end of the last ice age, approximately 12,000 years ago, the fauna of North America was composed of a diversity of large mammals similar to Africa today: mam- moths and mastodons, horses, camels, giant ground-sloths, saber-toothed cats, and lions, among others (figure 31.2). Shortly after humans arrived, 74 to 86% of the megafauna (that is, animals weighing more than 100 pounds) became extinct. These extinctions are thought to have been caused by hunting, and indirectly by burning and clearing forests (some scientists attribute these extinctions to climate change, but that hypothesis doesn’t explain why the end of earlier ice ages was not associated with mass extinctions, nor does it explain why extinctions occurred primarily among larger animals, with smaller species relatively unaffected). 31.1 The new science of conservation biology is focused on conserving biodiversity. FIGURE 31.2 North America before human inhabitants.Animals found in North America prior to the migration of humans included large mammals and birds such as the ancient North American camel, saber-toothed cat, giant ground-sloth, and the teratorn vulture. in table 31.1, based on the best available evidence, shows recorded extinctions from 1600 to the present. These es- timates indicate that about 85 species of mammals and 113 species of birds have become extinct since the year 1600. That is about 2.1% of known mammal species and 1.3% of known birds. The majority of extinctions have come in the last 150 years. The extinction rate for birds and mammals was about one species every decade from 1600 to 1700, but it rose to one species every year during the period from 1850 to 1950, and four species per year between 1986 and 1990 (figure 31.3). It is this increase in the rate of extinction that is the heart of the biodiversity crisis. The majority of historic extinctions—though by no means all of them—have occurred on islands. For example, of the 90 species of mammals that have gone extinct in the last 500 years, 73% lived on islands (and another 19% on Australia). The particular vulnerability of island species probably results from a number of factors: such species have often evolved in the absence of predators and so have lost their ability to escape both humans and introduced predators such as rats and cats. In addition, humans have introduced competitors and diseases (avian malaria, for ex- ample has devastated the bird fauna of the Hawaiian Is- lands). Finally, island populations are often relatively small, and thus particularly vulnerable to extinction, as we shall see later in the chapter. In recent years, however, the extinction crisis has moved from islands to continents. Most species now threatened with extinction occur on continents, and it is these areas which will bear the brunt of the extinction crisis in this century. Some people have argued that we should not be con- cerned because extinctions are a natural event and mass extinctions have occurred in the past. Indeed, as we saw in chapter 21, mass extinctions have occurred several times over the past half billion years. However, the cur- rent mass extinction event is notable in several respects. First, it is the only such event triggered by a single species. Moreover, although species diversity usually re- covers after a few million years, this is a long time to deny our descendants the benefits and joys of biodiver- sity. In addition, it is not clear that biodiversity will re- bound this time. After previous mass extinction events, new species have evolved to utilize resources available due to species extinctions. Today, however, such re- sources are unlikely to be available, because humans are destroying the habitats and taking the resources for their own use. Biologists estimate rates of extinction both by studying recorded extinction events and by analyzing trends in habitat loss and disruption. Since prehistoric times, humans have had a devastating effect on biodiversity almost everywhere in the world. Chapter 31 Conservation Biology 627 Table 31.1 Recorded Extinctions since 1600 a.d. Recorded Extinctions Approximate Percent of Number of Taxon Taxon Mainland Island Ocean Total Species Extinct Mammals 30 51 4 85 4,000 2.1 Birds 21 92 0 113 9,000 1.3 Reptiles 1 20 0 21 6,300 0.3 Amphibians* 2 0 0 2 4,200 0.05 Fish 22 1 0 23 19,100 0.1 Invertebrates 49 48 1 98 1,000,000+ 0.01 Flowering plants 245 139 0 384 250,000 0.2 Source: Reid and Miller, 1989; data from various sources. *There has been an alarming decline in amphibian populations recently, and many species may be on the verge of extinction. 0.4 0.3 0.2 0.1 1600 1700 1800 Year T axonomic extinction (%) 1900 2000 Birds Mammals Reptiles Fishes Amphibians FIGURE 31.3 Trends in species loss. The graphs above present data on re- corded animal extinctions since 1600. The majority of extinctions have occurred on islands, with birds and mammals particularly affected (although this may reflect to some degree our more limited knowledge of other groups). Species Endemism and Hot Spots A species found naturally in only one geographic area and no place else is said to be endemic to that area. The area over which an endemic species is found may be very large. The black cherry tree (Prunus serotina), for example, is en- demic to all of temperate North America. More typically, however, endemic species occupy restricted ranges. The Komodo dragon (Varanus komodoensis) lives only on a few small islands in the Indonesian archipelago, while the Mauna Kea silversword (Argyroxiphium sandwicense) lives in a single volcano crater on the island of Hawaii. Isolated geographical areas, such as oceanic islands, lakes, and mountain peaks, often have high percentages of endemic species, often in significant danger of extinction. The number of endemic plant species varies greatly in the United States from one state to another. Thus, 379 plant species are found in Texas and nowhere else, whereas New York has only one endemic plant species. California, with its varied array of habitats, including deserts, mountains, seacoast, old growth forests, grasslands, and many others, is home to more endemic species than any other state. Worldwide, notable concentrations of endemic species occur in particular “hot spots” of high endemism. Such hot spots are found in Madagascar, in a variety of tropical rain forests, in the eastern Himalayas, in areas with Mediter- ranean climates like California, South Africa, and Australia, and in several other climatic areas (figure 31.4 and table 31.2). Unfortunately, many of these areas are experiencing high rates of habitat destruction with consequent species extinctions. In Madagascar, it is estimated that 90% of the original forest has already been lost, this in an island in which 85% of the species are found nowhere else in the world. In the forests of the Atlantic coast of Brazil, the ex- tent of deforestation is even higher: 95% of the original forest is gone. Some areas of the earth have particularly high levels of species endemism. Unfortunately, many of these areas are currently in great jeopardy due to habitat destruction with correspondingly high rates of species extinction. 628 Part VIII The Global Environment Table 31.2 Numbers of Endemic Vertebrate Species in Some “Hot Spot” Areas Region Mammals Reptiles Amphibians Atlantic coastal Brazil 40 92 168 Colombian Chocó 8 137 111 Philippines 98 120 41 Northern Borneo 42 69 47 Southwestern Australia 10 25 22 Madagascar 86 234 142 Cae region (South Africa) 16 43 23 California Floristic Province 15 25 7 New Cledonia 2 21 0 Eastern Himalayas — 20 25 Source: Data from Myers 1988; World Conservation and Monitoring Center 1992. Hawaii Colombian Chocó Western Ecuador Uplands of western Amazonia California floral province Atlantic forest region of eastern BrazilCentral Chile Eastern Himalayas Western Ghats Eastern Arc forests, Tanzania Ivory Coast Cape floral province Eastern Madagascar Sri Lanka Philippines Northern Borneo Southwest Australia Peninsular Malaysia Queensland Australia New Caledonia FIGURE 31.4 “Hot spots” of high endemism. These areas are rich in endemic species under significant threat of imminent extinction. What’s So Bad about Losing Biodiversity? What’s so bad about losing species? What is the value of biodiversity? Its value can be divided into three principal components: (1) direct economic value of products we obtain from species of plants, animals, and other groups; (2) indi- rect economic value of benefits produced by species without our consuming them; and (3) ethicaland aestheticvalue. Direct Economic Value Many species have direct value, as sources of food, medi- cine, clothing, biomass (for energy and other purposes), and shelter. Most of the world’s food, for example, is de- rived from a small number of plants that were originally domesticated from wild plants in tropical and semi-arid re- gions. In the future, wild strains of these species may be needed for their genetic diversity if we are to improve yields, or find a way to breed resistance to new pests. About 40% of the prescription and nonprescription drugs used today have active ingredients extracted from plants or animals. Aspirin, the world’s most widely used drug, was first extracted from the leaves of the tropical wil- low, Salix alba. The rosy periwinkle, Catharanthus roseus, from Madagascar has yielded potent drugs for combating leukemia (figure 31.5). Only in the last few decades have biologists perfected the techniques that make possible the transfer of genes from one kind of organism to another. We are just begin- ning to be able to use genes obtained from other species to our advantage, as explored at length in chapter 19. So- called gene prospecting of the genomes of plants and ani- mals for useful genes has only begun. We have been able to examine only a minute proportion of the world’s organisms so far, to see whether any of their genes have useful proper- ties. By conserving biodiversity we maintain the option of finding useful benefit in the future. Indirect Economic Value Diverse biological communities are of vital importance to healthy ecosystems, in maintaining the chemical quality of natural water, in buffering ecosystems against floods and drought, in preserving soils and preventing loss of minerals and nutrients, in moderating local and regional climate, in absorbing pollution, and in promoting the breakdown of organic wastes and the cycling of minerals. By destroying biodiversity, we are creating conditions of instability and lessened productivity and promoting desertification, water- logging, mineralization, and many other undesirable out- comes throughout the world. Given the major role played by many species in main- taining healthy ecosystems, it is alarming how little we know about the details of how ecosystems and communi- ties function. It is impossible to predict all the conse- quences of removing a species, or to be sure that some of them will not be catastrophic. Imagine taking a part list for an airliner, and randomly changing a digit in one of the part numbers: you might change a cushion to a roll of toi- let paper—but you might as easily change a key bolt hold- ing up the wing to a pencil. The point is, you shouldn’t gamble if you cannot afford to lose, and in removing bio- diversity we are gambling with the future of ecosystems upon which we depend, and upon whose functioning we only little understand. Ethical and Aesthetic Value Many people believe that preserving biodiversity is an ethi- cal issue, feeling that every species is of value in its own right, even if humans are not able to exploit or benefit from it. It is clear that humans have the power to exploit and de- stroy other species, but it is not as ethically clear that they have the right to do so. Many people believe that along with power comes responsibility: as the only organisms ca- pable of eliminating species and entire ecosystems, and as the only organisms capable of reflecting upon what we are doing, we should act as guardians or stewards for the diver- sity of life around us. Almost no one would deny the aesthetic value of biodi- versity, of a beautiful flower or noble elephant, but how do we place a value on beauty? Perhaps the best we can do is to appreciate the deep sense of lack we feel at its permanent loss. Biodiversity is of great value, for the products with which it provides us, for its contributions to the health of the ecosystems upon which we all depend, and for the beauty it provides us, as well as being valuable in its own right. Chapter 31 Conservation Biology 629 FIGURE 31.5 The rosy periwinkle. Two drugs extracted from the Madagascar periwinkle Catharanthus roseus,vinblastine and vincristine, effectively treat common forms of childhood leukemia, increasing chances of survival from 20% to over 95%. Predicting Which Species Are Vulnerable to Extinction How can a biologist assess whether a particular species is vulnerable to extinction? To get some handle on this, con- servation biologists look for changes in population size and habitat availability. Species whose populations are shrink- ing rapidly, whose habitats are being destroyed (figure 31.6), or which are endemic to small areas can be consid- ered to be endangered. Population Viability Analysis Quantifying the risk faced by a particular species is not a simple or precise enterprise. Increasingly, conservation bi- ologists make a rough estimate of a population’s risk of local extinction in terms of a minimum viable population (MVP), the estimated number or density of individuals necessary for the population to maintain or increase its numbers. Some small populations are at high risk of extinction, while other populations equally small are at little or no risk. Conservation biologists carry out a population via- bility analysis (PVA) to assess how the size of a popula- tion influences its risk of becoming extinct over a specific time period, often 100 years. Many factors must be taken into account in a PVA. Two components of particular importance are demographic stochasticity (the amount of random variation in birth and death rates) and genetic sto- chasticity (fluctuations in a population’s level of genetic variation). Demographic stochasticity refers to random events that affect a population. The smaller the popula- tion, the more likely it is that a random event, such as a disease epidemic or an environmental disturbance (such as a flood or a fire) could decimate a population and lead to extinction. Similarly, small populations are most likely to lose genetic variation due to genetic drift (see chapter 20) and thus be vulnerable to both the short- and long- term consequences of genetic uniformity. For these rea- sons, small populations are at particularly great risk of ex- tinction. Many species are distributed as metapopulations, col- lections of small populations each occupying a suitable patch of habitat in an otherwise unsuitable landscape (see chapter 24). Each individual subpopulation may be quite small and in real threat of extinction, but the metapopu- lation may be quite safe from extinction so long as indi- viduals from other populations repopulate the habitat patches vacated by extinct populations. The extent of this rescue effect is an important component of the PVA of such species; if rates of population extinction increase, there may not be enough surviving populations to found new populations, and the species as a whole may slide to- ward extinction. Small populations are particularly in danger of extinction. To assess the risk of local extinction of a particular species, conservation biologists carry out a population viability analysis that takes into account demographic and genetic variation. 630 Part VIII The Global Environment 31.2 Vulnerable species are more likely to become extinct. FIGURE 31.6 Habitat removal. In this clear-cut lumbering of National Forest land in Washington State, few if any trees have been left standing, removing as well the home of the deer, birds, and other animal inhabitants of temperate forest. Until a replacement habitat is provided by replanting, this is a truly “lost” habitat. Dependence upon Other Species Species often become vulnerable to extinction when their web of ecological interactions becomes seriously disrupted. A recent case in point are the sea otters that live in the cold waters off Alaska and the Aleutian Islands. A keystone species in the kelp forest ecosystem, the otter populations have declined sharply in recent years. In a 500-mile stretch of coastline, otter numbers had dropped to an estimated 6000 from 53,000 in the 1970s, a plunge of nearly 90%. In- vestigating this catastrophic decline, marine ecologists un- covered a chain of interactions among the species of the ocean and kelp forest ecosystems, a falling domino chain of lethal effects. The first in a series of events leading to the sea otter’s decline seems to have been the heavy commercial harvest- ing of whales (see the case history later in this chapter). Without whales to keep their numbers in check, ocean zoo- plankton thrived, leading in turn to proliferation of a species of fish called pollock that feed on the now-abundant zooplankton. Given this ample food supply, the pollock proved to be very successful competitors of other northern Pacific fish like herring and ocean perch, so that levels of these other fish fell steeply in the 1970s. Now the falling chain of dominos begins to accelerate. The decline in the nutritious forage fish led to an ensuing crash in Alaskan populations of Steller’s sea lions and har- bor seals, for which pollock did not provide sufficient nour- ishment. Numbers of these pinniped species have fallen precipitously since the 1970s. Pinnipeds are the major food of orcas, also called killer whales. Faced with a food shortage, some orcas seem to have turned to the next best thing: sea otters. In one bay where the entrance from the sea was too narrow and shal- low for orcas to enter, only 12% of the sea otters have dis- appeared, while in a similar bay which orcas could enter easily, two-thirds of the otters disappeared in a year’s time. Without otters to eat them, the population of sea urchins in the ecosystem exploded, eating the kelp and so “deforesting” the kelp forests and denuding the ecosystem (figure 31.7). As a result, fish species that live in the kelp forest, like sculpins and greenlings (a cod relative), are de- clining. This chain reaction demonstrates why sea otters are considered to be a keystone species. Commercial whaling appears to have initiated a series of changes that have led to orcas feeding on sea otters, with disastrous effects on their kelp forest ecosystem. Chapter 31 Conservation Biology 631 Nutritious fish Populations of nutritious fish like ocean perch and herring declined, likely due to overfishing, competition with pollock, or climatic change. Sea lions and harbor seals Sea lion and harbor seal populations drastically declined in Alaska, probably because the less-nutritious pollock could not sustain them. Kelp forests Severely thinned by the sea urchins, the kelp beds no longer support a diversity of fish species, which may lead to a decline in populations of eagles that feed on the fish. Whales Overharvesting of plankton-eating whales may have caused an increase in plankton-eating pollock populations. Killer whales With the decline in their prey populations of sea lions and seals, killer whales turned to a new source of food: sea otters. Sea otters Sea otter populations declined so dramatically that they disappeared in some areas. Sea urchins Usually the preferred food of sea otters, sea urchin populations now exploded and fed on kelp. FIGURE 31.7 Disruption of the kelp forest ecosystem. Overharvesting by commercial whalers altered the balance of fish in the ocean ecosystem, inducing killer whales to feed on sea otters, a keystone species of the kelp forest ecosystem. Categories of Vulnerable Species Studying past extinctions of species and using population viability analyses of threatened ones, conservation biolo- gists have observed that some categories of species are par- ticularly vulnerable to extinction. Local Endemic Distribution Local endemic species typically occur at only one or a few sites in a restricted geographical range, which makes them particularly vulnerable to anything that harms the site, such as destruction of habitat by human activity. Bird species on oceanic islands have often become extinct as humans affect the island habitats. Many endemic fish species confined to a single lake undergo similar fates. Local endemic species often have small population sizes, placing them at particular risk of extinction be- cause of their greater vulnerability to demographic and genetic fluctuations. Indeed, population size by itself seems to be one of the best predictors of the extinction risk of populations. Local endemic species often have quite specialized niche requirements. Once a habitat is altered, it may no longer be able to support a particular local endemic, while remaining satisfactory for species with less particular re- quirements. For example, wetlands plants that require very specific and regular changes in water level may be rapidly eliminated when human activity affects the hy- drology of an area. Declining Population Size Species in which population size is declining are often at grave risk of extinction, particularly if the decline in num- bers of individuals is severe. Although there is no hard rule, population trends in nature tend to continue, so a popula- tion showing significant signs of decline should be consid- ered at risk of extinction unless the cause of the decline is identified and corrected. Darwin makes this point very clearly in On the Origin of Species: “To admit that species generally become rare before they become extinct, to feel no surprise at the rarity of the species, and yet to marvel greatly when the species ceases to exist, is much the same as to admit that sickness in the individual is the forerunner of death—to feel no surprise at sickness, but when the sick man dies, to wonder and to sus- pect that he dies of some deed of violence.” Although long-term trends toward smaller population numbers suggest that a species may be at risk in future years, abrupt recent declines in population numbers, partic- ularly when the population is small or locally endemic, fairly scream of risk of extinction. It is for this reason that PVA is best carried out with data on population sizes gath- ered over a period of time. Lack of Genetic Variability Species with little genetic variability are generally at signifi- cantly greater risk of extinction than more variable species, simply because they have a more limited arsenal with which to respond to the vagaries of environmental change. Species with extremely low genetic variability are particu- larly vulnerable when faced with a new disease, predator, or other environmental challenge. For example, the African cheetah (Acinonyx jubatus) has almost no genetic variability. This lack of genetic variability is considered to be a signifi- cant contributing factor to a lack of disease resistance in the cheetah—diseases that are of little consequence to other cat species can wipe out a colony of cheetahs (although envi- ronmental factors also seem to have played a key role in the cheetah’s decline). Hunted or Harvested by People Species that are hunted or harvested by people have histor- ically been at grave risk of extinction. Overharvesting of natural populations can rapidly reduce the population size of a species, even when that species is initially very abun- dant. A century ago the skies of North America were dark- ened by huge flocks of passenger pigeons; hunted as free and tasty food, they were driven to extinction. The buffalo that used to migrate in enormous herds across the central plains of North America only narrowly escaped the same fate, a few individuals preserved from this catastrophic ex- ercise in overhunting founding today’s modest herds. The existence of a commercial market often leads to overexploitation of a species. The international trade in furs, for example, has severely reduced the numbers of chinchilla, vicuna, otter, and many wild cat species. The harvesting of commercially valuable trees provides another telling example: almost all West Indies mahogany (Swiete- nia mahogani) have been logged from the Caribbean is- lands, and the extensive cedar forests of Lebanon, once widespread at high elevations in the Middle East, now sur- vive in only a few isolated groves. A particularly telling example of overharvesting of a so- called commercial species is the commercial harvesting of fish in the North Atlantic. Fishing fleets continued to har- vest large amounts of cod off Newfoundland during the 1980s, even as the population numbers declined precipi- tously. By 1992 the cod population had dropped to less than 1% of their original numbers. The American and Canadian governments have closed the fishery, but no one can predict if the fish populations will recover. The At- lantic bluefin tuna has experienced a 90% population de- cline in the last 10 years. The swordfish has declined even further. In both cases, the drop has led to even more in- tense fishing of the remaining populations. A variety of factors can make a species particularly vulnerable to extinction. 632 Part VIII The Global Environment Factors Responsible For Extinction Because a species is rare does not necessarily mean that it is in danger of extinction. The habitat it utilizes may simply be in short supply, preventing population numbers from growing. In a similar way, shortage of some other resource may be limiting the size of populations. Secondary carni- vores, for example, are usually rare because so little energy is available to support their populations. Nor are vulnerable species such as those categories discussed in the previous section always threatened with extinction. Many local en- demics are quite stable and not at all threatened. If it’s not just size or vulnerability, what factors are re- sponsible for extinction? Studying a wide array of recorded extinctions and many species currently threatened with ex- tinction, conservation biologists have identified a few fac- tors that seem to play a key role in many extinctions: over- exploitation, introduced species, disruption of ecological relationships, loss of genetic variability, and habitat loss and fragmentation (figure 31.8 and table 31.3). Most recorded extinctions can be attributed to one of five causes: overexploitation, introduced species, ecodisruption, loss of genetic variability, and habitat loss and fragmentation. Chapter 31 Conservation Biology 633 31.3 Causes of endangerment usually reflect human activities. Habitat loss Overexploitation Introduced species Other Percent of species af fected 0 10 20 30 40 50 60 70 80 90 100 FIGURE 31.8 Factors responsible for animal extinction. These data represent known extinctions of mammals in Australasia and the Americas. Table 31.3 Causes of Extinctions Percentage of Species Influenced by the Given Factor* Habitat Species Group Loss Overexploitation Introduction Predators Other Unknown EXTINCTIONS Mammals 19 23 20 1 1 36 Birds 20 11 22 0 2 37 Reptiles 5 32 42 0 0 21 Fish 35 4 30 0 4 48 THREATENED EXTINCTIONS Mammals 68 54 6 8 12 — Birds 58 30 28 1 1 — Reptiles 53 63 17 3 6 — Amphibians 77 29 14 — 3 — Fish 78 12 28 — 2 — *Some species may be influenced by more than one factor; thus, some rows may exceed 100%. Source: Reid and Miller, 1989. Habitat Loss As figure 31.8 and table 31.3 indicate, habitat loss is the single most important cause of extinction. Given the tremendous amounts of ongoing destruction of all types of habitat, from rain forest to ocean floor, this should come as no surprise. Natural habitats may be adversely affected by human influences in four ways: (1) destruction, (2) pollu- tion, (3) human disruption, and (4) habitat fragmentation. Destruction A proportion of the habitat available to a particular species may simply be destroyed. This is a common occurrence in the “clear-cut” harvesting of timber, in the burning of trop- ical forest to produce grazing land, and in urban and indus- trial development. Forest clearance has been, and is, by far the most pervasive form of habitat disruption (figure 31.9). Many tropical forests are being cut or burned at a rate of 1% or more per year. Biologists often use the well-established observation that larger areas support more species (see figure 29.24) to esti- mate the effect of reductions in habitat available to a species. As we saw in chapter 30, a relationship usually ex- ists between the size of an area and the number of species it contains. Although this relationship varies according to ge- ographic area, type of organism, and type of area (for ex- ample, oceanic islands, patches of habitat on the mainland), a general result is that a tenfold increase in area usually leads to approximately a doubling in number of species. This relationship suggests, conversely, that if the area of a habitat is reduced by 90%, so that only 10% remains, then half of all species will be lost. Evidence for this theory comes from a study of extinction rates of birds on habitat islands (that is, islands of a particular type of habitat sur- rounded by unsuitable habitat) in Finland where the extinc- tion rate was found to be inversely proportional to island size (figure 31.10). Pollution Habitat may be degraded by pollution to the extent that some species can no longer survive there. Degradation oc- curs as a result of many forms of pollution, from acid rain to pesticides. Aquatic environments are particularly vulner- able; many northern lakes in both Europe and North America, for example, have been essentially sterilized by acid rain. Human Disruption Habitat may be so disturbed by human activities as to make it untenable for some species. For example, visitors to caves in Alabama and Tennessee produced significant population declines in bats over an eight-year period, some as great as 100%. When visits were fewer than one 634 Part VIII The Global Environment Before human colonization 1950 Africa 1985 FIGURE 31.9 Extinction and habitat destruction. The rain forest covering the eastern coast of Madagascar, an island off the coast of East Africa, has been progressively destroyed as the island’s human population has grown. Ninety percent of the original forest cover is now gone. Many species have become extinct, and many others are threatened, including 16 of Madagascar’s 31 primate species. Extinction rate (per year) 0.5 0.4 0.3 0.2 0.1 0.0 10 -2 110 2 Area (km 2 ) FIGURE 31.10 Extinction and the species-area relationship. The data present percent extinction rates as a function of habitat area for birds on a series of Finnish islands. Smaller islands experience far greater local extinction rates. per month, less than 20% of bats were lost, but caves with more than four visits per month suffered population de- clines of between 86 and 95%. Habitat Fragmentation Loss of habitat by a species frequently results not only in a lowering of population numbers, but also in fragmentation of the population into unconnected patches (figure 31.11). A habitat may become fragmented in unobvious ways, such as when roads and habitation intrude into forest. The effect is to carve up the populations living in the habitat into a series of smaller populations, often with disastrous consequences. Although detailed data are not available, fragmentation of wildlife habitat in developed temperate areas is thought to be very substantial. As habitats become fragmented and shrink in size, the relative proportion of the habitat that occurs on the bound- ary, or edge, increases. Edge effects can significantly de- grade a population’s chances of survival. Changes in micro- climate (temperature, wind, humidity, etc.) near the edge may reduce appropriate habitat for many species more than the physical fragmentation suggests. In isolated fragments of rain forest, for example, trees on the edge are exposed to direct sunlight and, consequently, hotter and drier condi- tions than they are accustomed to in the cool, moist forest interior. As a result, within 100 meters of the forest edge, tree biomass decreased by 36% in the first 17 years after fragment isolation in one study. Also, increasing habitat edges opens up opportunities for parasites and predators, both more effective at edges. As fragments decrease in size, the proportion of habitat that is distant from any edge decreases and, consequently, more and more of the habitat is within the range of these preda- tors. Habitat fragmentation is thought to have been re- sponsible for local extinctions in a wide range of species. The impact of habitat fragmentation can be seen clearly in a major study done in Manaus, Brazil, as the rain forest was commercially logged. Landowners agreed to preserve patches of rain forest of various sizes, and censuses of these patches were taken before the logging started, while they were still part of a continuous forest. After logging, species began to disappear from the now-isolated patches (figure 31.12). First to go were the monkeys, which have large home ranges. Birds that prey on ant colonies followed, dis- appearing from patches too small to maintain enough ant colonies to support them. Because some species like monkeys require large patches, this means that large fragments are indispensable if we wish to preserve high levels of biodiversity. The take- home lesson is that preservation programs will need to pro- vide suitably large habitat fragments to avoid this impact. Habitat loss is probably the greatest cause of extinction. As habitats are destroyed, remaining habitat becomes fragmented, increasing the threat to many species. Chapter 31 Conservation Biology 635 1831 1882 1902 1950 FIGURE 31.11 Fragmentation of woodland habitat. From the time of settlement of Cadiz Township, Wisconsin, the forest has been progressively reduced from a nearly continuous cover to isolated woodlots covering less than 1% of the original area. FIGURE 31.12 A study of habitat fragmentation. Biodiversity was monitored in the isolated patches of rain forest in Manaus, Brazil, before and after logging. Fragmentation led to significant species loss within patches. Case Study: Overexploitation— Whales Whales, the largest living animals, are rare in the world’s oceans today, their numbers driven down by commercial whaling. Commercial whaling began in the sixteenth cen- tury, and reached its apex in the nineteenth and early twentieth centuries. Before the advent of cheap high- grade oils manufactured from petroleum in the early twentieth century, oil made from whale blubber was an important commercial product in the worldwide market- place. In addition, the fine lattice-like structure used by baleen whales to filter-feed plankton from seawater (termed “baleen,” but sometimes called “whalebone” even though it is actually made of keratin, like finger- nails) was used in undergarments. Because a whale is such a large animal, each individual captured is of significant commercial value. Right whales were the first to bear the brunt of commer- cial whaling. They were called right whales because they were slow, easy to capture, and provided up to 150 barrels of blubber oil and abundant whalebone, making them the “right” whale for a commercial whaler to hunt. As the right whale declined in the eighteenth century, whalers turned to other species, the gray, humpback (figure 31.13), and bowhead. As their numbers declined, whalers turned to the blue, largest of all whales, and when they were decimated, to smaller whales: the fin, then the Sei, then the sperm whales. As each species of whale became the focus of commercial whaling, its numbers inevitably began a steep decline (figure 31.14). Hunting of right whales was made illegal in 1935. By then, all three species had been driven to the brink of ex- tinction, their numbers less than 5% of what they used to be. Protected since, their numbers have not recovered in either the North Atlantic or North Pacific. By 1946 sev- eral other species faced imminent extinction, and whaling nations formed the International Whaling Commission (IWC) to regulate commercial whale hunting. Like hav- ing the fox guard the hen house, the IWC for decades did little to limit whale harvests, and whale numbers contin- ued a steep decline. Finally, in 1974, when numbers of all but the small minke whales had been driven down, the IWC banned hunting of blue, gray, and humpback whales, and instituted partial bans on other species. The rule was violated so often, however, that the IWC in 1986 instituted a worldwide moratorium on all commercial killing of whales. While some commercial whaling con- tinues, often under the guise of harvesting for scientific studies, annual whale harvests have dropped dramatically in the last 15 years. Some species appear to be recovering, while others do not. Humpback numbers have more than doubled since the early 1960s, increasing nearly 10% annually, and Pacific gray whales have fully recovered to their previous numbers of about 20,000 animals after being hunted to less than 1000. Right, sperm, fin, and blue whales have not recov- ered, and no one knows whether they will. Commercial whaling, by overharvesting, has driven most large whale species to the brink of extinction. Stopping the harvest has allowed recovery of some but not all species. 636 Part VIII The Global Environment FIGURE 31.13 A humpback whale. Only 5000 to 10,000 humpback whales remain, out of a world population estimated to have been 100,000. 1910 1920 1930 1940 1950 1960 1970 1980 1990 0 5 10 15 20 25 30 Number of whales (in thousands) Fin Sperm Blue Minke Sei Humpback Year FIGURE 31.14 A history of commercial whaling. These data show the world catch of whales in the twentieth century. Each species in turn is hunted until its numbers fall so low that hunting it becomes commercially unprofitable. Case Study: Introduced Species— Lake Victoria Cichlids Lake Victoria, an immense shallow freshwater sea about the size of Switzerland in the heart of equatorial East Africa, had until 1954 been home to an incredibly diverse collection of over 300 species of cichlid fishes (figure 31.15). These small, perchlike fishes range from 2 to 10 inches in length, with males coming in endless varieties of colors. Today, all of these cichlid species are threatened, endangered, or extinct. What happened to bring about the abrupt loss of so many endemic cichlid species? In 1954, the Nile perch, Lates niloticus, a commercial fish with a voracious ap- petite, was introduced on the Ugandan shore of Lake Victoria. Nile perch, which grow to over 4 feet in length, were to form the basis of a new fishing industry (figure 31.16). For decades, these perch did not seem to have a significant impact—over 30 years later, in 1978, Nile perch still made up less than 2% of the fish harvested from the lake. Then something happened to cause the Nile perch to explode and to spread rapidly through the lake, eating their way through the cichlids. By 1986, Nile perch constituted nearly 80% of the total catch of fish from the lake, and the endemic cichlid species were virtually gone. Over 70% of cichlid species disappeared, including all open-water species. So what happened to kick-start the mass extinction of the cichlids? The trigger seems to have been eutrophica- tion. Before 1978, Lake Victoria had high oxygen levels at all depths, down to the bottom layers exceeding 60 meters depth. However, by 1989 high inputs of nutrients from agricultural runoff and sewage from towns and villages had led to algal blooms that severely depleted oxygen levels in deeper parts of the lake. Cichlids feed on algae, and initially their population numbers are thought to have risen in re- sponse to this increase in their food supply, but unlike simi- lar algal blooms of the past, the Nile perch was now pre- sent to take advantage of the situation. With a sudden increase in its food supply (cichlids), the numbers of Nile perch exploded, and the greater numbers of them simply ate all available cichlids. Since 1990 the situation has been compounded by a sec- ond factor, the introduction into Lake Victoria of a floating water weed from South America, the water hyacinth Eichor- nia crassipes. Extremely fecund under eutrophic conditions, thick mats of water hyacinth soon covered entire bays and inlets, choking off the coastal habitats of non-open-water cichlids. Lake Victoria’s diverse collection of cichlid species is being driven to extinction by an introduced species, the Nile perch. A normal increase in cichlid numbers due to algal blooms led to an explosive increase in perch, which then ate their way through the cichlids. Chapter 31 Conservation Biology 637 FIGURE 31.15 Lake Victoria cichlids. Cichlid fishes are extremely diverse and occupy different niches. Some species feed on arthropods, others on dense stands of plants; there are fish-eaters, and still other species feed on fish eggs and larvae. FIGURE 31.16 Victor and vanquished. The Nile perch (larger fishes in foreground), a commercial fish introduced into Lake Victoria as a potential food source, is responsible for the virtual extinction of hundreds of species of cichlid fishes (smaller fishes in tub). Case Study: Disruption of Ecological Relationships—Black- Footed Ferrets The black-footed ferret (Mustela nigripes) is one of the most attractive weasels of North America. A highly specialized predator, black-footed ferrets prey on prairie dogs, which live in large underground colonies connected by a maze of tunnels. These ferrets have experienced a dramatic decline in their North American range during this century, as agri- cultural development has destroyed their prairie habitat, and particularly the prairie dogs on which they feed (figure 31.17). Prairie dogs once roamed freely over 100 million acres of the Great Plains states, but are now confined to under 700,000 acres (table 31.4). Their ecological niche devastated, populations of the black-footed ferret collapsed. Increasingly rare in the second half of the century, the black-footed ferret was thought to have gone extinct in the late 1970s, when the only known wild population—a small colony in South Dakota—died out. In 1981, a colony of 128 animals was located in Mee- teese, Wyoming. Left undisturbed for four years, the num- ber of ferrets dropped by 50%, and the entire population seemed in immediate danger of extinction. A decision was made to capture some animals for a captive breeding pro- gram. The first six black-footed ferrets captured died of ca- nine distemper, a disease present in the colony and proba- bly responsible for its rapid decline. At this point, drastic measures seemed called for. In the next year, a concerted effort was made to capture all the remaining ferrets in the Meeteese colony. A captive popu- lation of 18 individuals was established before the Mee- teese colony died out. The breeding program proved a great success, the population jumping to 311 individuals by 1991. In 1991, biologists began to attempt to reintroduce black-footed ferrets to the wild, releasing 49 animals in Wyoming. An additional 159 were released over the next two years. Six litters were born that year in the wild, and the reintroduction seemed a success. However, the re- leased animals then underwent a drastic decline, and only ten individuals were still alive in the wild five years later in 1998. The reason for the decline is not completely under- stood, but predators such as coyotes appear to have played a large role. Current attempts at reintroduction involve killing the local coyotes. It is important that these attempts succeed, as numbers of offspring in the captive breeding colony are declining, probably as a result of the intensive inbreeding. The black-footed ferret still teeters at the brink of extinction. Loss of its natural prey has eliminated black-footed ferrets from the wild; attempts to reintroduce them have not yet proven successful. 638 Part VIII The Global Environment Table 31.4 Acres of Prairie Dog Habitat State 1899-1990 1998 Arizona unknown extinct Colorado 7,000,000 44,000 Kansas 2,500,000 36,000 Montana 6,000,000 65,000 Nebraska 6,000,000 60,000 New Mexico 12,000,000 15,000 North Dakota 2,000,000 20,400 Oklahoma 950,000 9,500* South Dakota 1,757,000 244,500 Texas 56,833,000 22,650 Wyoming 16,000,000 70,000–180,000 U.S. Total 111,000,000 700,000 Source: National Wildlife Federation and U.S. Fish and Wildlife Report, 1998. *1990. FIGURE 31.17 Teetering on the brink. The black-footed ferret is a predator of prairie dogs, and loss of prairie dog habitat as agriculture came to dominate the plains states in this century has led to a drastic decline in prairie dogs, and an even more drastic decline in the black-footed ferrets that feed on them. Attempts are now being made to reestablish natural populations of these ferrets, which have been extinct in the wild since 1986. Case Study: Loss of Genetic Variation—Prairie Chickens The greater prairie chicken (Tympanuchus cupido pinnatus) is a showy 2-pound wild bird renowned for its flamboyant mating rituals (figure 31.18). Abundant in many midwest- ern states, the prairie chickens in Illinois have in the last six decades undergone a population collapse. Once, enormous numbers of birds covered the state, but with the introduc- tion of the steel plow in 1837, the first that could slice through the deep dense root systems of prairie grasses, the Illinois prairie began to be replaced by farmland, and by the turn of the century the prairie had vanished. By 1931, the subspecies known as the heath hen (Tympanuchus cupido cupido) became extinct in Illinois. The greater prairie chicken fared little better in Illinois, its numbers falling to 25,000 statewide in 1933, then to 2000 in 1962. In sur- rounding states with less intensive agriculture, it continued to prosper. In 1962, a sanctuary was established in an attempt to preserve the prairie chicken, and another in 1967. But pri- vately owned grasslands kept disappearing, with their prairie chickens, and by the 1980s the birds were extinct in Illinois except for the two preserves. And there they were not doing well. Their numbers kept falling. By 1990, the egg hatching rate, which had averaged between 91 and 100%, had dropped to an extremely low 38%. By the mid- 1990s, the count of males dropped to as low as six in each sanctuary. What was wrong with the sanctuary populations? One reasonable suggestion was that because of very small popu- lation sizes and a mating ritual where one male may domi- nate a flock, the Illinois prairie chickens had lost so much genetic variability as to create serious inbreeding problems. To test this idea, biologists at the University of Illinois compared DNA from frozen tissue samples of birds that died in Illinois between 1974 and 1993 and found that in recent years, Illinois birds had indeed become genetically less diverse. Extracting DNA from tissue in the roots of feathers from stuffed birds collected in the 1930s from the same population, the researchers found little genetic differ- ence between the Illinois birds of the 1930s and present- day prairie chickens of other states. However, present-day Illinois birds had lost fully one-third of the genetic diver- sity of birds living in the same place before the population collapse of the 1970s. Now the stage was set to halt the Illinois prairie chick- en’s race toward extinction. Wildlife managers began to transplant birds from genetically diverse populations of Minnesota, Kansas, and Nebraska to Illinois. Between 1992 and 1996, a total of 518 out-of-state prairie chick- ens were brought in to interbreed with the Illinois birds, and hatching rates were back up to 94% by 1998. It looks like the Illinois prairie chickens have been saved from extinction. The key lesson to be learned is the importance of not al- lowing things to go too far, not to drop down to a single isolated population (figure 31.19). Without the outlying genetically different populations, the prairie chickens in Illinois could not have been saved. The black-footed ferrets discussed on the previous page are particularly endangered because they exist as a single isolated population. When their numbers fell, Illinois prairie chickens lost much of their genetic variability, resulting in reproductive failure and the threat of immediate extinction. Breeding with genetically more variable birds appears to have reversed the decline. Chapter 31 Conservation Biology 639 FIGURE 31.18 A male prairie chicken performing a mating ritual. He inflates bright orange air sacs, part of his esophagus, into balloons on each side of his head. As air is drawn into the sacs, it creates a three- syllable “boom-boom-boom” that can be heard for miles. Polymorphism (%) Population size (log) 1 2 3456 0 10 20 30 40 ?? ? ? ?? ? ? ? ?? ? ? ? ? ? FIGURE 31.19 Small populations lose much of their genetic variability. The percentage of polymorphic genes in isolated populations of the tree Halocarpus bidwilliin the mountains of New Zealand is a sensitive function of population size. Case Study: Habitat Loss and Fragmentation—Songbirds Every year since 1966, the U.S. Fish and Wildlife Service has organized thousands of amateur ornithologists and bird watchers in an annual bird count called the Breeding Bird Survey. In recent years, a shocking trend has emerged. While year-round residents that prosper around humans, like robins, starlings, and blackbirds, have increased their numbers and distribution over the last 30 years, forest songbirds have declined severely. The decline has been greatest among long-distance migrants such as thrushes, orioles, tanagers, catbirds, vireos, buntings, and warblers. These birds nest in northern forests in the summer, but spend their winters in South or Central America or the Caribbean Islands. In many areas of the eastern United States, more than three-quarters of the neotropical migrant bird species have declined significantly. Rock Creek Park in Washington, D.C., for example, has lost 90 percent of its long distance migrants in the last 20 years. Nationwide, American red- starts declined about 50% in the single decade of the 1970s. Studies of radar images from National Weather Service stations in Texas and Louisiana indicate that only about half as many birds fly over the Gulf of Mexico each spring compared to numbers in the 1960s. This suggests a loss of about half a billion birds in total, a devastating loss. The culprit responsible for this widespread decline ap- pears to be habitat fragmentation and loss. Fragmentation of breeding habitat and nesting failures in the summer nesting grounds of the United States and Canada have had a major negative impact on the breeding of woodland song- birds. Many of the most threatened species are adapted to deep woods and need an area of 25 acres or more per pair to breed and raise their young. As woodlands are broken up by roads and developments, it is becoming increasingly dif- ficult to find enough contiguous woods to nest successfully. A second and perhaps even more important factor seems to be the availability of critical winter habitat in Central and South America. Living in densely crowded limited areas, the availability of high-quality food is critical. Studies of the American redstart clearly indicate that birds with better winter habitat have a superior chance of successfully migrating back to their breeding grounds in the spring. Peter Marra and Richard Holmes of Dartmouth College and Keith Hobson of the Canadian Wildlife Service cap- tured birds, took blood samples, and measured the levels of the stable carbon isotope 13 C. Plants growing in the best overwintering habitats in Jamaica and Honduras (man- groves and wetland forests) have low levels of 13 C, and so do the redstarts that feed on them. Sixty-five percent of the wet forest birds maintained or gained weight over the win- ter. Plants growing in substandard dry scrub, by contrast, have high levels of 13 C, and so do the redstarts that feed on them. Scrub-dwelling birds lost up to 11% of their body mass over the winter. Now here’s the key: birds that winter in the substandard scrub leave later in the spring on the long flight to northern breeding grounds, arrive at their summer homes, and have fewer young. You can see this clearly in the redstart study (figure 31.20): the proportion of 13 C carbon in birds arriving in New Hampshire breeding grounds increases as spring wears on and scrub-overwinter- ing stragglers belatedly arrive. Thus, loss of mangrove habitat in the neotropics is having a real negative impact. As the best habitat disappears, overwintering birds fare poorly, and this leads to population declines. Unfortu- nately, the Caribbean lost about 10% of its mangroves in the 1980s, and continues to lose about 1% a year. This loss of key habitat appears to be a driving force in the looming extinction of songbirds. Fragmentation of summer breeding grounds and loss of high-quality overwintering habitat seem both to be contributing to a marked decline in migratory songbird species. 640 Part VIII The Global Environment Stable carbon isotope values ( 13 C) Males Females May 12 May 17 May 22 May 27 June 1 -22.5 -23.5 -23.0 -24.0 -24.5 -25.0 FIGURE 31.20 The American redstart, a migratory songbird whose numbers are in serious decline. The graph presents data on the level of 13 C in redstarts arriving at summer breeding grounds. Early arrivals, with the best shot at reproductive success, have lower levels of 13 C, indicating they wintered in more favorable mangrove-wetland forest habitats. Many Approaches Exist for Preserving Endangered Species Once you understand the reasons why a particular species is endangered, it becomes possible to think of designing a recovery plan. If the cause is commercial overharvesting, regulations can be designed to lessen the impact and pro- tect the threatened species. If the cause is habitat loss, plans can be instituted to restore lost habitat. Loss of ge- netic variability in isolated subpopulations can be coun- tered by transplanting individuals from genetically differ- ent populations. Populations in immediate danger of extinction can be captured, introduced into a captive breeding program, and later reintroduced to other suit- able habitat. Of course, all of these solutions are extremely expensive. As Bruce Babbitt, Interior Secretary in the Clinton admin- istration, noted, it is much more economical to prevent such “environmental trainwrecks” from occurring than it is to clean them up afterwards. Preserving ecosystems and monitoring species before they are threatened is the most effective means of protecting the environment and prevent- ing extinctions. Habitat Restoration Conservation biology typically concerns itself with preserv- ing populations and species in danger of decline or extinc- tion. Conservation, however, requires that there be some- thing left to preserve, while in many situations, conservation is no longer an option. Species, and in some cases whole communities, have disappeared or have been irretrievably modified. The clear-cutting of the temperate forests of Washington State leaves little behind to con- serve; nor does converting a piece of land into a wheat field or an asphalt parking lot. Redeeming these situations re- quires restoration rather than conservation. Three quite different sorts of habitat restoration pro- grams might be undertaken, depending very much on the cause of the habitat loss. Pristine Restoration. In situations where all species have been effectively removed, one might attempt to restore the plants and animals that are believed to be the natural in- habitants of the area, when such information is available. When abandoned farmland is to be restored to prairie (fig- ure 31.21), how do you know what to plant? Although it is in principle possible to reestablish each of the original species in their original proportions, rebuilding a commu- nity requires that you know the identity of all of the origi- nal inhabitants, and the ecologies of each of the species. We rarely ever have this much information, so no restora- tion is truly pristine. Removing Introduced Species. Sometimes the habitat of a species has been destroyed by a single introduced species. In such a case, habitat restoration involves re- moval of the introduced species. Restoration of the once- diverse cichlid fishes to Lake Victoria will require more than breeding and restocking the endangered species. Eu- trophication will have to be reversed, and the introduced water hyacinth and Nile perch populations brought under control or removed. It is important to act quickly if an introduced species is to be removed. When aggressive African bees (the so-called “killer bees”) were inadvertently released in Brazil, they re- mained in the local area only one season. Now they occupy much of the Western hemisphere. Cleanup and Rehabilitation. Habitats seriously de- graded by chemical pollution cannot be restored until the pollution is cleaned up. The successful restoration of the Nashua River in New England, discussed in chapter 30, is one example of how a concerted effort can succeed in restoring a heavily polluted habitat to a relatively pristine condition. Chapter 31 Conservation Biology 641 31.4 Successful recovery plans will need to be multidimensional. (a) (b) FIGURE 31.21 The University of Wisconsin-Madison Arboretum has pioneered restoration ecology. (a) The restoration of the prairie was at an early stage in November, 1935. (b) The prairie as it looks today. This picture was taken at approximately the same location as the 1935 photograph. Captive Propagation Recovery programs, particularly those focused on one or a few species, often must involve direct intervention in nat- ural populations to avoid an immediate threat of extinction. Earlier we learned how introducing wild-caught individuals into captive breeding programs is being used in an attempt to save ferret and prairie chicken populations in immediate danger of disappearing. Several other such captive propaga- tion programs have had significant success. Case History: The Peregrine Falcon. American popu- lations of birds of prey such as the peregrine falcon (Falco peregrinus) began an abrupt decline shortly after World War II. Of the approximately 350 breeding pairs east of the Mississippi River in 1942, all had disappeared by 1960. The culprit proved to be the chemical pesticide DDT (dichlorodiphenyltrichloroethane) and related organochlo- rine pesticides. Birds of prey are particularly vulnerable to DDT because they feed at the top of the food chain, where DDT becomes concentrated. DDT interferes with the de- position of calcium in the bird’s eggshells, causing most of the eggs to break before they hatch. The use of DDT was banned by federal law in 1972, causing levels in the eastern United States to fall quickly. There were no peregrine falcons left in the eastern United States to reestablish a natural population, however. Falcons from other parts of the country were used to establish a captive breeding program at Cornell University in 1970, with the intent of reestablishing the peregrine falcon in the eastern United States by releasing offspring of these birds By the end of 1986, over 850 birds had been released in 13 eastern states, producing an astonishingly strong recovery (figure 31.22). Case History: The California Condor. Numbers of the California condor (Gymnogyps californianus), a large vulturelike bird with a wingspan of nearly 3 meters, have been declining gradually for the last 200 years. By 1985 condor numbers had dropped so low the bird was on the verge of extinction. Six of the remaining 15 wild birds disappeared that year alone. The entire breeding popula- tion of the species consisted of the 6 birds remaining in the wild, and an additional 21 birds in captivity. In a last- ditch attempt to save the condor from extinction, the re- maining birds were captured and placed in a captive breeding population. The breeding program was set up in zoos, with the goal of releasing offspring on a large 5300-ha ranch in prime condor habitat. Birds were iso- lated from human contact as much as possible, and closely related individuals were prevented from breeding. By the end of 1999 the captive population of California condors had reached over 110 individuals. Twenty-nine captive-reared condors have been released successfully in California at two sites in the mountains north of Los An- geles, after extensive prerelease training to avoid power poles and people, all of the released birds seem to be doing well. Twenty additional birds released into the Grand Canyon have adapted well. Biologists are waiting to see if the released condors will breed in the wild and successfully raise a new generation of wild condors. Case History: Yellowstone Wolves. The ultimate goal of captive breeding programs is not simply to pre- serve interesting species, but rather to restore ecosystems to a balanced functional state. Yellowstone Park has been an ecosystem out of balance, due in large part to the sys- tematic extermination of the gray wolf (Canis lupus) in the park early in this century. Without these predators to keep their numbers in check, herds of elk and deer ex- panded rapidly, damaging vegetation so that the elk themselves starve in times of scarcity. In an attempt to restore the park’s natural balance, two complete wolf packs from Canada were released into the park in 1995 and 1996. The wolves adapted well, breeding so success- fully that by 1998 the park contained nine free-ranging packs, a total of 90 wolves. While ranchers near the park have been unhappy about the return of the wolves, little damage to livestock has been noted, and the ecological equilibrium of Yellowstone Park seems well on the way to recovery. Elk are congregating in larger herds, and their populations are not growing as rapidly as in years past. Importantly, wolves are killing coy- otes and their pups, driving them out of some areas. Coy- otes, the top predators in the absence of wolves, are known to attack cattle on surrounding ranches, so reintroduction of wolves to the park may actually benefit the cattle ranch- ers that are opposed to it. 642 Part VIII The Global Environment 1980 0 20 40 60 80 100 1982 1984 Year Number of pairs of peregrines 1986 1988 1990 Pairs observed Pairs nesting Pairs producing offspring FIGURE 31.22 Captive propagation. The peregrine falcon has been reestablished in the eastern United States by releasing captive- bred birds over a period of 10 years. Sustaining Genetic Diversity One of the chief obstacles to a successful species recovery program is that a species is generally in serious trouble by the time a recovery program is instituted. When popula- tions become very small, much of their genetic diversity is lost (see figure 31.19), as we have seen clearly in our exami- nation of the case histories of prairie chickens and black- footed ferrets. If a program is to have any chance of suc- cess, every effort must be made to sustain as much genetic diversity as possible. Case History: The Black Rhino. All five species of rhinoceros are critically endangered. The three Asian species live in forest habitat that is rapidly being de- stroyed, while the two African species are illegally killed for their horns. Fewer than 11,000 individuals of all five species survive today. The problem is intensified by the fact that many of the remaining animals live in very small, isolated populations. The 2400 wild-living individuals of the black rhino, Diceros bicornis, live in approximately 75 small widely separated groups (figure 31.23) consisting of six subspecies adapted to local conditions throughout the species’ range. All of these subspecies appear to have low genetic variability; in three of the subspecies, only a few dozen animals remain. Analysis of mitochondrial DNA suggests that in these populations most individuals are genetically very similar. This lack of genetic variability represents the greatest challenge to the future of the species. Much of the range of the black rhino is still open and not yet subject to human encroachment. To have any significant chance of success, a species recovery program will have to find a way to sustain the genetic diversity that remains in this species. Heterozygosity could be best maintained by bringing all black rhinos together in a single breeding population, but this is not a practical possibility. A more feasible solution would be to move individuals between populations. Man- aging the black rhino populations for genetic diversity could fully restore the species to its original numbers and much of its range. Placing black rhinos from a number of different loca- tions together in a sanctuary to increase genetic diversity raises a potential problem: local subspecies may be adapted in different ways to their immediate habitats—what if these local adaptations are crucial to their survival? Homogeniz- ing the black rhino populations by pooling their genes risks destroying such local adaptations, if they exist, perhaps at great cost to survival. Chapter 31 Conservation Biology 643 (a) Black African Rhino Present distribution Equator Former distribution (b) FIGURE 31.23 Sustaining genetic diversity. The black rhino (a) is highly endangered, living in 75 small, widely separated populations (b). Only about 2400 individuals survive in the wild. Preserving Keystone Species Keystone species are species that exert a particularly strong influence on the structure and functioning of a particu- lar ecosystem. The sea otters of figure 31.7 are a keystone species of the kelp forest ecosystem, and their removal can have disastrous consequences. There is no hard-and-fast line that allows us to clearly identify keystone species. It is rather a qualitative concept, a state- ment that a species plays a particularly important role in its community. Key- stone species are usually characterized by measuring the strength of their im- pact on their community. Community importance measures the change in some quantitative aspect of the ecosys- tem (species richness, productivity, nu- trient cycling) per unit of change in the abundance of a species. Case History: Flying Foxes. The severe decline of many species of pteropodid bats, or “flying foxes,” in the Old World tropics is an example of how the loss of a keystone species can have dramatic effects on the other species living within an ecosystem, sometimes even leading to a cascade of further extinctions (figure 31.24). These bats have very close relationships with important plant species on the islands of the Pacific and Indian Oceans. The family Pteropodidae contains nearly 200 species, approximately a quarter of them in the genus Ptero- pus, and is widespread on the islands of the South Pacific, where they are the most important—and often the only— pollinators and seed dispersers. A study in Samoa found that 80 to 100% of the seeds landing on the ground during the dry season were deposited by flying foxes. Many species are entirely dependent on these bats for pollination. Some have evolved features like night-blooming flowers that pre- vent any other potential pollinators from taking over the role of the fruit bats. In Guam, where the two local species of flying fox have recently been driven extinct or nearly so, the impact on the ecosystem appears to be substantial. Botanists have found some plant species are not fruiting, or are doing so only marginally, with fewer fruits than normal. Fruits are not being dispersed away from parent plants, so offspring shoots are being crowded out by the adults. Flying foxes are being driven to extinction by human hunting. They are hunted for food, for sport, and by or- chard farmers, who consider them pests. Flying foxes are particularly vulnerable because they live in large, easily seen groups of up to a million individuals. Because they move in regular and predictable patterns and can be easily tracked to their home roost, hunters can easily bag thou- sands at a time. Species preservation programs aimed at preserving par- ticular species of flying foxes are only just beginning. One particularly successful example is the program to save the Rodrigues fruit bat, Pteropus rodricensis, which occurs only on Rodrigues Island in the Indian Ocean near Madagascar. The population dropped from about 1000 individuals in 1955 to fewer than 100 by 1974, the drop reflecting largely the loss of the fruit bat’s forest habitat to farming. Since 1974 the species has been legally protected, and the forest area of the island is being increased through a tree-planting program. Eleven captive breeding colonies have been es- tablished, and the bat population is now increasing rapidly. The combination of legal protection, habitat restoration, and captive breeding has in this instance produced a very effective preservation program. Recovery programs at the species level must deal with habitat loss and fragmentation, and often with a marked reduction in genetic diversity. Captive breeding programs that stabilize genetic diversity and pay careful attention to habitat preservation and restoration are typically involved in successful recoveries. 644 Part VIII The Global Environment FIGURE 31.24 Preserving keystone species. The flying fox is a keystone species in many Old World tropical islands. It pollinates many of the plants, and is a key disperser of seeds. Its elimination by hunting and habitat loss is having a devastating effect on the ecosystems of many South Pacific islands. Conservation of Ecosystems Habitat fragmentation is one of the most pervasive enemies of biodiversity conservation efforts. As we have seen, some species simply require large patches of habitat to thrive, and conservation efforts that cannot provide suitable habi- tat of such a size are doomed to failure. As it has become clear that isolated patches of habitat lose species far more rapidly than large preserves do, conservation biologists have promoted the creation, particularly in the tropics, of so-called megareserves, large areas of land containing a core of one or more undisturbed habitats (figure 31.25). The key to devoting such large tracts of land to reserves successfully over a long period of time is to operate the re- serve in a way compatible with local land use. Thus, while no economic activity is allowed in the core regions of the megareserve, the remainder of the reserve may be used for nondestructive harvesting of resources. Linking preserved areas to carefully managed land zones creates a much larger total “patch” of habitat than would otherwise be economi- cally practical, and thus addresses the key problem created by habitat fragmentation. Pioneering these efforts, a series of eight such megareserves have been created in Costa Rica (figure 31.26) to jointly manage biodiversity and economic activity. In addition to this focus on maintaining large enough reserves, in recent years, conservation biologists also have recognized that the best way to preserve biodiversity is to focus on preserving intact ecosystems, rather than focusing on particular species. For this reason, attention in many cases is turning to identifying those ecosystems most in need of preservation and devising the means to protect not only the species within the ecosystem, but the function- ing of the ecosystem itself. Efforts are being undertaken worldwide to preserve biodiversity in megareserves designed to counter the influences of habitat fragmentation. Focusing on the health of entire ecosystems, rather than of particular species, can often be a more effective means of preserving biodiversity. Chapter 31 Conservation Biology 645 x x x x x x x x x x x x x x x x x x x x xx xx xx x x x x x x x x x x x x x xx x x x x x x x x x x x x xx x x x xx x ER ER ER TA TA RA RA TU TU R E E T T M Core (Conservation and Monitoring) Buffer (Research, Education, Tourism) Experimental Research Traditional Use Rehabilitation Transition Area Human Settlements Facilities for Research (R), Education (E), Tourism (T), Monitoring (M) x xx x x x R FIGURE 31.25 Design of a megareserve. A megareserve, or biosphere reserve, recognizes the need for people to have access to resources. Critical ecosystems are preserved in the core zone. Research and tourism is allowed in the buffer zone. Sustainable resource harvesting and permanent habitation is allowed in the multiple-use areas surrounding the buffer. NICARAGUA Caribbean Sea PANAMA Pacific Ocean Isla Bola?os N.W.R. Santa Rosa-Guanacaste N.P. Rincón de la Vieja N.P. Ca?o Negro N.W.R. Lake Arenal Monteverde Cloud Forest Preserve Lomas Barbudal Biological Reserve Palo Verde N.P. Barra Honda N.P. Ostional N.W.R. Cabo Blanco AbsoluteBiological Reserve Curú N.W.R. Nicoya Islands Biological Reserve Carara Biological Reserve Volcán Poás N.P. San José Volcán Irazú N.P. Tapantí N.W.R. Manuel Antonio N.P. Chirripó N.P. Guayabo N.M. Braulio Carrillo N.P. Barra del Colorado N.W.R. Tortuguero N.P. La Amistad N.P. Cahuita N.P. Isla del Ca?o Biological Reserve Golfito N.W.R. Corcovado N.P. Isla del Coco N.P. Hitoy-Cerere Biological Reserve La Selva Biological Station FIGURE 31.26 Biopreserves in Costa Rica. Costa Rica has placed about 12% of its land into national parks and eight megareserves. 646 Part VIII The Global Environment Chapter 31 Summary Questions Media Resources 31.1 The new science of conservation biology is focusing on conserving biodiversity. ? Early humans caused many extinctions when they appeared in new areas, but rates of extinction have increased in modern times. ? Some areas are particularly rich in species diversity and particularly merit conservation attention. 1.Are some areas particularly important for conserving biodiversity? 2.Describe some of the indirect economic values of biodiversity. ? Interdependence among species in an ecosystem leads to the possibility of cascading extinctions if removal of one species has major effects throughout the food web. ? Species are particularly vulnerable when they have localized distributions, are declining in population size, lack genetic variability, or are harvested or hunted by humans. 3.What factors contribute to the extinction rate on a particular piece of land? 4.How does a low genetic variability contribute to a species’ greater risk of extinction? 31.2 Vulnerable species are more likely to become extinct. ? Habitat loss is the single most important cause of species extinction. ? As suggested by the species-area relationship, a reduced habitat will support fewer numbers of species. ? This reduction in habitat can occur in four different ways: a habitat can be completely removed or destroyed, a habitat can become fragmented and disjunct, a habitat can be degraded or altered, or a habitat can become too frequently used by humans so as to disturb the species there. 5.How can problems resulting from lack of genetic diversity within a population be solved? 6.How can extinction of a keystone species be particularly disruptive to an ecosystem? 31.3 Causes of endangerment usually reflect human activities. ? Pristine restoration of a habitat may be attempted, but removing introduced species, rehabilitating the habitat, and cleaning up the habitat may be more feasible. ? Captive propagation, sustaining genetic variability, and preserving keystone species have been effective in preserving biodiversity. ? Megareserves have been successfully designed in many parts of the world to contain core areas of undisturbed habitat surrounded by managed land. 7.Why is maintaining large preserves particularly important? 8.Is captive propagation always an answer to species vulnerability? 9.Why is it important to attempt to eradicate introduced species soon after they appear? 31.4 Successful recovery plans will need to be multidimensional. www.mhhe.com/raven6e www.biocourse.com ? Biodiversity ? Species ? Extinction ? Wetlands ? Deoxygenation of Lakes ? On Science Article:What’s Killing the Frogs? ? Book Review: The End of the Gameby Beard ? Book Review: West with the Night by Markham ? Activity: Biomagnification ? On Science Article:Biodiversity Behind Bars ? Extinction