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Natural Extinctions (not Human Influenced)
N Natural Extinctions (not Human Influenced) Christopher N Johnson, James Cook University, Townsville, QLD, Australia r 2001 Elsevier Inc. All rights reserved. This article is reproduced from the previous edition, volume 4, pp 305–315, r 2001, Elsevier Inc.
Glossary Conditions Physical features of the environment, such as substrate type, ambient temperature, or salinity, that affect the ability of organisms to survive, grow, and reproduce. Dispersal The movement of an individual organism away from its place of origin to the place where it breeds (also, movement by an adult from one breeding location to another). Pseudoextinction The disappearance of a species from the fossil record due not to the death of all its members but to an evolutionary change that results in it being classified as a new species.
Introduction Most species have durations that are very short relative to the history of life, and it is likely that 99% of all species that have ever lived are now extinct. Extinction, therefore, is very much a natural process that produces continuous turnover in the membership of biological assemblages as species are steadily lost by extinction and replaced by speciation. Natural extinctions may be divided into two kinds: those that happened during geologically brief periods of crisis when many taxa disappeared (the mass extinction events) and those during the long intervals of ‘‘background’’ time between mass extinctions. Mass extinctions have attracted a great deal of interest because they bit so deeply into standing biodiversity and because the biotas that reformed after mass extinctions were often quite different from those that existed before; they dramatically reshaped world patterns of biodiversity. However, 95% or more of the total number of extinctions have taken place outside mass extinctions (May et al., 1995). These background extinctions have been most important in producing turnover in species assemblages. Differences in the probability of extinction for different types of organisms interact with rates of origination of new lineages to shape patterns of biodiversity. To understand patterns of biodiversity it is therefore essential that the process of extinction be understood. In particular, we need to know whether extinction rates vary among different types of organisms and to identify the
Encyclopedia of Biodiversity, Volume 5
Quaternary The past 2 million years (approximately) of Earth history, including the Pleistocene and Holocene (or Recent) epochs, and characterized by the extreme fluctuations in global temperature that produce the ice ages. Resources Physical and biotic features of the environment, such as shelter sites or foods, that are required by organisms and are consumed such that use by one individual reduces their availability to others. Secondary extinction Extinction of a species resulting from the extinction of another species on which it relies.
characteristics of taxa that make them more or less vulnerable to extinction. Extinction can be studied at the level of higher taxaFgenera, families, and so onFbut this article is concerned primarily with extinctions of species.
Natural Causes of Extinction The causes of extinction can be divided into two types: changes in the environment and interactions with other species.
Changes in the Environment Populations of all species fluctuate in abundance. A large part of this variation is due to chance variation in environmental conditions, such as variations in weather or events such as cyclones, which can be regarded as environmental ‘‘accidents.’’ Species vary in their ability to resist accidents, but for any species there will eventually come an environmental event of sufficient magnitude to wipe it out, or an unlucky succession of smaller blows that drive its abundance down to zero, even when there is no trend in average conditions. Additionally, species may be driven extinct by directional changes in the environment, such as changes in temperature to levels outside their tolerance or the disappearance of
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key habitats. Species can respond to such changes in the environment by (i) acquiring adaptations to the changed conditions (‘‘evolving out of trouble’’), (ii) shifting their geographic ranges to remain within a set of suitable conditions (‘‘moving out of trouble’’), or (iii) going extinct. If the pace of environmental change is fast relative to the rate of evolution, the first of these responses is much less likely than the other two. The fossil record provides many examples of extinctions apparently driven by environmental changes of many different kinds, especially during mass extinctions events. Environmental changes have been much more extreme and rapid during some periods of Earth history than during others, but environmental conditions have never been truly static. Global temperatures have trended downwards for much of the past 50 million years, and at a finer temporal scale variations in the earth’s orbit produce fluctuations in climate with periodicities in the range of 10,000 to 400,000 years. These are called Milankovitch cycles, and during the past 2 million years they have produced the succession of ice ages, but they must have forced rapid swings in climate throughout Earth history (Bennett, 1997).
Interactions with Other Species The population growth rates of species are constrained by the species predators, parasites, and competitors. The abundance of a species will be reduced if its natural enemies become more abundant or evolve greater efficiency, or if its geographic range is invaded by a new enemy to which it has not evolved defenses. It is generally difficult to reconstruct such interactions in the fossil record, but some patterns may reflect the impact of predators on prey species. For example, the number of species of endobyssate bivalves gradually declined through the Mesozoic. These species were abundant, immobile, and lay partly exposed on the open seafloor. Their decline coincided with radiations of marine crabs, teleost fish, and carnivorous snails, groups that account for most predation on modern bivalves and to which the endobyssates must have been vulnerable (Stanley, 1979). The few present-day survivors of the group live in conditions with low predator pressure. Recent experience shows that prey species can be rapidly driven extinct by unfamiliar predators that invade their habitat. The carnivorous snail Euglandina rosea, for example, has caused the extinction of hundreds of species of endemic snails, including 600 of more than 1000 original species from the Hawaiian Islands, since its introduction to many Pacific islands in the 1970s. Such a rapid course of events would be unresolvable in the fossil record. Probably, the impacts of environmental changes and of other species interact in subtle ways to cause extinction. For example, a species might experience a slight environmental change that reduces its population without driving it extinct and to which it could readily adapt given sufficient time. However, the same change might favor a competitor or trigger a range expansion by an unfamiliar predator suited to the new conditions. Interactions of this kind could mean that quite small environmental changes could have dramatic consequences leading ultimately to extinction.
Lifetimes of Species Variation among Taxonomic Groups The oldest extant species known is the tadpole shrimp, Triops cancriformis, a small freshwater crustacean found in temporary pools in arid regions of Eurasia and north Africa that is indistinguishable from 180-million-year-old fossils bearing the same name. Most species do not live to this age, as shown in Table 1. The lifetime of a species begins with its origin in a speciation event and ends either when it dies out, leaving no descendants, or when its characteristics have been sufficiently changed by evolution that it is classified as a new species. The first type of disappearance of species is ‘‘real’’ extinction, and the second is referred to as pseudoextinction. This distinction is important but not easy to draw in practice. Our understanding of species life spans derives from study of the fossil record, and when a recognizable species disappears from the record it can be difficult to determine whether it has died out or evolved into something else. Information in Table 1 is based on real extinctions when the distinction can be made,
Table 1 Durations of species and extinction rates for major groups of organisms in the fossil record Taxon
Single-celled organisms Diatoms Dinoflagellates Planktonic foraminifera Benthic foraminifera Plants Early vascular plants Pteridophytes Gymnosperms Monocots Dicots All invertebrates Reef corals Mollusks: Marine gastropods Marine bivalves Mesozoic ammonites Upper Cambrian trilobites Marine ostracods Silurian graptolites Echinoderms Echinoids Crinoids Bryozoans Freshwater fish Birds Mammals Cenozoic mammals Horses Primates
Estimated mean species duration (millions of years)
Extinction rate (extinctions per million species years)
8 13 7–20
0.12 0.08 0.14–0.05
25
0.04
10–14 7–15 2–15 4 3 11 20
0.1–0.07 0.14–0.07 0.5–0.07 0.25 0.33 0.09 0.05
10 15 1 1.3
0.1 0.07 1 0.77
8 2
0.12 0.5
6 6.7 12 3 2.5 1.4 1–2 4 1
0.17 0.15 0.08 0.33 0.42 0.71 1–0.5 0.25 1
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but most estimates include an unknown combination of real and pseudoextinctions. There is considerable variation in species life spans among different groups of organisms. In general, it seems that species of unicellular organisms last longer than species of multicellular organisms, and invertebrates appear to last longer than vertebrates. The most long-lived animal groups tend to be marine rather than terrestrial, although too little is known about species durations of marine vertebrates or terrestrial invertebrates to judge differences between marine and terrestrial species independent of the difference between vertebrates and invertebrates. Some marine invertebrate groups that are now entirely extinct (the trilobites, ammonites, and graptolites) had short species durations, even though they were successful, abundant, and species rich for long periods of geological time. Among plants, species durations were longer in groups that appeared early in the evolutionary history of plants but have tended to shorten in recently evolved groups. The inverse of the typical duration of species in a given taxonomic group can be used as a measure of the probability of extinction per unit time for species belonging to that group: Long durations equate to low probabilities of extinction. In Table 1, probabilities of extinction have been expressed as the rates of extinction per million species years. Thus, marine gastropods typically last 10 million years, so a sample of 1 million marine gastropod species would be expected to experience 0.1 extinctions per year.
Variation within Taxonomic Groups The distributions of species lifetimes within higher taxa are typically right-skewed: Most species have short durations, but a small minority are long-lasting (Figure 1). There could be two causes for this pattern. First, only a few species might have characteristics that make them intrinsically resistant to extinction, whereas most are sensitive to extinction risk. Second, species might not vary in their susceptibility to extinction, but
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if many independent factors can cause extinction only a small minority of species will be lucky enough to avoid extinction for long. Probably both factors play a part in shaping distributions of species durations.
Risk of Extinction in Relation to Species Age Does the likelihood that a species will go extinct depend on its age? One might think that it should because the longer a species stays in existence the more adaptations to its environment it can accumulate; older species should therefore be better at avoiding extinction. This idea can be tested by examining species survivorship curves. A species survivorship curve shows the relationship between age and the proportion of species in a taxon surviving to each age. Such curves are typically log linear; that is, when the proportion surviving is plotted logarithmically its decline with age approximates a straight line. This shows that the proportion of species going extinct is approximately constant with respect to age. The constancy of extinction probability with species age can be explained by assuming that the environment of any species is continually changing so that even if the species continually adapts, its fitness lags behind the current condition of the environment. Thus, no matter how long a species lasts it can never reach a condition of optimal adaptation. There are two forms of this explanation. The first assumes that the probability of extinction for a species is determined primarily by its interactions with other species and that each species is under constant selection pressure to increase its fitness relative to these other species. However, adaptations in one species that increase abundance at the expense of other species will be met by counteradaptations from them so that, on average, no species improves its fitness with time. This is the Red Queen hypothesis, named after the character in Lewis Carroll’s Alice Through the Looking Glass in whose world ‘‘it takes all the running you can do, just to stay in one place.’’ The Red Queen hypothesis predicts that extinction rates will be
Figure 1 Species durations of Silurian graptolites of the British Isles. (Reproduced from Stanley SM (1979) Macroevolution: Patterns and Process. San Francisco: Freeman, with permission from W.H. Freeman and Company.)
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approximately constant with respect to absolute time. The second form of the explanation assumes that it is the abiotic environment that is continually changing. Changes in the abiotic environment will tend to be episodic and will therefore produce fluctuations in extinction rates with time, but their effects will still be independent of species age. It is not clear which form of the hypothesis is closer to the truth.
The Selectivity of Extinction Extinction may be largely a matter of the bad luck of environmental change, exacerbated perhaps by pressure from other species; however, the fact that species durations vary so widely among higher taxa suggests that biological characteristics of species influence their susceptibility to extinction. Three types of studies have helped to identify these characteristics. First, the attributes of species that have short versus long durations in the fossil record can be compared. A common variant of this technique compares species that persisted through mass extinction events with those that did not. Second, the living faunas of ‘‘land-bridge islands’’ can be compared with their presumed original faunas. A land-bridge island is an island formed as a result of isolation from the mainland by rising sea levels during the Pleistocene. Such islands typically have fewer species than do similar areas of mainland habitat to which they were once connected, reflecting extinctions caused by the pressure of reduced habitat area. Third, extinction of local populations can be observed directly in contemporary ecological studies. The second and third approaches focus on population rather than species extinctions, but the extinction of a species is the end point of a series of population extinctions, so such studies may still reveal traits that correlate with risk of extinction at the species level. The following traits consistently emerge from many studies of the selectivity of extinction: rarity, dispersal ability, body size, and specialization.
Rarity The commonness or rarity of a species is a function of two factors: its geographic range and its population density where it occurs. Both components of rarity influence extinction risk.
Geographic Range There is strong evidence from the fossil record (mainly for marine invertebrates) that species with large ranges have lower extinction rates (Jablonski, 1995; McKinney, 1997). There are probably two causes for this effect. First, at a given scale, a disturbance will affect a smaller proportion of the range of a widespread rather than of a geographically restricted species. In the extreme, a single catastrophic event may wipe out a localized species but have little impact on a widespread species. Second, even if an environmental change affects a very large area, it is likely that some populations of widespread species will persist in isolated refuges that provide some local protection from the change. Species that hang on in such refuges may reinvade their original ranges once conditions
improve. This is probably part of the explanation for the existence in the fossil record of ‘‘Lazarus species’’ that vanish during periods of environmental crisis and then reappear much later. The effect of range size on extinction risk tends to be strongest for background extinctions, and it may weaken or disappear in mass extinctions. This seems to have been the case for marine mollusks, for example (Jablonski, 1991), and is probably because mass extinctions were caused by events that affected such large areas and had such profound impacts that even widespread species were susceptible to them.
Local Abundance Population density is generally not well represented in the fossil record, but patterns of extinction of populations on land-bridge islands and in the present day show that local extinction is more likely for species with low population densities. For example, Foufopoulos and Ives (1999) found that reptile species with low population densities were more likely to go extinct from land-bridge islands in the Mediterranean Sea. The causes of extinction of small populations have been widely discussed in the literature on conservation. Briefly, small populations are more vulnerable than large populations because (i) they may go extinct more quickly when chance environmental variation causes fluctuations in abundance; (ii) they are affected by chance demographic fluctuations, such as occasional production of biased sex ratios of offspring, that would be averaged out in large populations; (iii) they may lose genetic variation and experience high levels of inbreeding and inbreeding depression; and (iv) they may be subject to Allee effectsFthat is, social or reproductive dysfunction as a direct result of low numbers.
The Relationship between Range and Abundance The components of rarityFgeographic range size and population densityFare generally positively related among species: Species with small geographic ranges also tend to have low population densities, and wide-ranging species have high population densities. This pattern has been found in many terrestrial plant and animal taxa, although it remains almost unstudied in marine organisms. Why there should be a positive relationship between range and abundance is not clear. Several ecological mechanisms have been proposed as its cause, but two ideas have been especially influential. First, Brown (1995) argued that niche breadth is positively correlated with both range size and population density because species with broad niches can exist under a wider range of conditions and use more types of resources than can species with narrow niches; variation among species in niche breadth therefore produces a positive relationship between range and density. Second, species that reach high local densities should be both more resistant to extinction on habitat patches because their populations are larger and produce more migrants that are able to recolonize habitat patches after local extinctions (Hanski, 1999). High local abundance therefore results in wide geographic distribution. To the extent that geographic range and local abundance affect extinction risk independently of one another, the correlation between them should exaggerate differences among species in extinction risk. Rare species face double jeopardy:
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Spatial Structure of Populations Another aspect of rarity is ubiquity or patchiness of distribution within the geographic range. The distributions of practically all species are discontinuous at some scale, but the degree of patchiness varies, reflecting specialization for habitats or resources that are themselves patchily distributed. In a species that has a patchy distribution, metapopulation dynamics are likely (Hanski, 1999). That is, the risk of extinction of populations on discrete patches of habitat may be high, but local populations are eventually reestablished by migrants from other populations. Recolonization will involve a time lag that depends on the distance between patches and the dispersal ability of the species. A general deterioration in the quality of habitat for a species is likely to cause contraction of larger habitat patches and the disappearance of smaller ones, causing local extinctions and simultaneously increasing the distance between surviving patches and thus reducing the probability of migration. Patchily distributed species should therefore be more likely to go extinct as a result of environmental change than should continuously distributed species. The sensitivity of patchy species to environmental change has been demonstrated for insects in Great Britain subject to human-caused changes (Webb and Thomas, 1994), but it is likely to be general to any form of shift in environmental conditions. Patchiness of distribution is loosely correlated with the other components of rarity so that widespread and locally abundant species tend to be continuously distributed within their ranges, whereas rare species are likely to be patchy.
Figure 2 Relationships between size of geographic range and population density for species of Australian marsupials: (a) all species other than those defined as ancient and (b) ancient species only. Ancient species are those that diverged from their closest living relative more than 4 million years ago and have therefore demonstrated resistance to extinction. The shaded triangle defines the region of distribution-abundance space from which species would need to have gone extinct to produce the pattern observed among ancient species. (Reproduced with permission from Johnson CN (1998) Species extinction and the relationship between distribution and abundance. Nature 394: 272–274.)
The vulnerability that comes from having a small range is compounded with the vulnerability due to low abundance. Common species, on the other hand, are likely to be highly resistant to extinction because they combine high abundance with large ranges. For example, Johnson (1998) showed that among Australian marsupials, ancient species (those that diverged from their closest relative more than 4 million years ago) are very unlikely to have both small ranges and low population densities, although this combination occurs frequently among young species (Figure 2). This suggests that species with low abundance and small ranges tend to be short lived. There are ancient marsupials with small ranges but they have unusually high densities, and conversely there are species with low densities but they have unusually large ranges, implying that a high density can compensate for the vulnerability that comes from having a small range and vice versa.
Dispersal Ability Dispersal ability is positively associated with species longevity for two reasons. First, species that disperse widely tend to have large geographic ranges, and their resistance to extinction can be a direct result of large range. Marine gastropod snails, for example, have two different forms of development. In some, the egg is released into surface waters and develops into a larval form that feeds in the plankton and drifts widely before settling and developing into an adult snail. This form of development promotes wide dispersal. Others have direct development in which eggs and young grow up close to the parent. Species with planktonic development have larger geographic ranges and longer durations in the fossil record than do species with direct development (Jablonski, 1995). Second, species that disperse widely are better able to recolonize after going extinct from part of the range, and they can more rapidly shift their ranges to track changes in the distribution of their preferred climates and habitats. During the Quartenary in the Northern Hemisphere, the distribution of habitats changed very rapidly as ice sheets repeatedly advanced and receded. These changes produced remarkably few extinctions among Northern Hemisphere beetles. Instead, species shifted their geographic ranges to keep pace with the changing distribution of habitats, an effect that was more dramatic in flighted than in flightless species (Coope, 1995). Probably, dispersal ability and local abundance interact to confer high resistance to extinction because high local abundance means that large numbers of dispersers are produced,
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resulting in the potential for rapid shifting of range boundaries as conditions change. This combination of characteristics might protect species that have specialized habitat requirements and small geographic ranges and would otherwise be vulnerable to extinction.
Body Size It often seems to be the case that large-bodied species are at higher risk of extinction than small-bodied species. Although there are exceptions, this pattern is reasonably consistent in the fossil record both for background extinctions and for mass extinctions (McKinney, 1997), and it also emerges in extinctions on land-bridge islands (Brown, 1995). There are several reasons why large-bodied species might be particularly vulnerable to extinction: 1. Potential rate of population increase declines with body size because large-bodied species generally have longer generation times and lower fecundity than do small-bodied species. This means that large-bodied species will generally recover more slowly from population declines, and because they produce fewer offspring they may be slower to track habitats than will small-bodied species. 2. Individuals of large-bodied species generally need larger areas, and large-bodied species are therefore strongly affected by declines in habitat area. 3. Population density tends to decline with body size so that large species are often naturally rare. This is partly compensated by a tendency for size of geographic range to increase with body size, but this relationship is often weak or absent so that total population size is usually much less for large than small species. The decline in population density with body size is clearest when species of very different size (e.g., mice and elephants) are compared, but in guilds of ecologically similar species it is often the case that density increases with body size, possibly because larger species are better competitors for resources (Cotgreave, 1993). At this finer scale of comparison, therefore, large-bodied species might be more resistant to extinction than small-bodied species.
Specialization Species can be classed as ‘‘specialists’’ or ‘‘generalists’’ on three criteria: the range of conditions that they are adapted to tolerate, the range of resources that they are able to use, and the degree of their evolved dependence on a small number of other species.
Conditions Species that are narrowly adapted to environmental conditions are likely to be the first to go extinct when the environment changes. This is difficult to demonstrate in the fossil record, however, because it is not possible to measure directly the environmental tolerances of fossil species. Instead, environmental tolerances are inferred from geographic distributions. Species with small geographic ranges will necessarily occupy a narrow range of climate zones and habitats, but it
does not follow from this that their environmental tolerances are narrow. Some species that could potentially be widely distributed have small ranges because of population history, geographic barriers to movement, or poor dispersal ability or because range expansion is prevented by interactions with other species (competitors, predators, and so on). Therefore, although there is abundant evidence from the fossil record that species with small geographic ranges are extinction-prone, there is much less evidence for the commonsense view that the breadth of tolerance of environmental conditions directly affects extinction risk.
Resources Species that depend on a narrow range of types of resources are likely to be more sensitive to changes in resource abundance than generalists that can easily switch resources. This vulnerability may be partly compensated by the fact that specialization on a particular resource may be more likely to evolve if that resource is abundant and widespread. For example, feeding on grasses by mammals requires extensive specialization of the teeth and digestive system, and increases in body size, to overcome the abrasiveness and poor nutritional quality of grasses. However, because of the abundance of grasses many mammals have evolved these adaptations, and grazing mammals typically have high local abundance and large geographic ranges. Nonetheless, grazing mammals in Africa have suffered higher extinction rates since the Miocene than mixed grazer/browsers, as the extent of grasslands has fluctuated during the Pliocene and Pleistocene (Vrba, 1987).
Interactions Specialization is taken a step further in species that have evolved a close dependence on one or a small number of other species. For example, many herbivorous insects feed on only one species of plant, and many predators attack only one or a small number among many possible species of prey. Of particular interest are mutualistic interactions, in which species provide benefits to one another. Figs, for example, rely on fig wasps for pollination, and fig wasps in turn lay their eggs only in the flowers of figs. This interaction tends to be highly species specific, with each species of fig visited by only one species of fig wasp and each partner in the interaction completely dependent on the other for reproduction. Such tight species specificity results from coevolution, in which each species in the interaction evolves special characteristics in response to evolutionary changes in the other to increase its benefit from the interaction. Specialization of this kind is classically regarded as an extinction trap because the specialist will inevitably go extinct if the species that it depends on goes extinct or becomes very rare. This view is probably an oversimplification. Careful study of some species-specific interactions has revealed more flexibility and greater potential for rapid evolutionary response to changes in the abundance of interacting species, including the ability to switch to new partners, than was previously assumed (Thompson, 1994). Also, mutualistic interactions have the general effect of increasing the geographic range and abundance, and stabilizing the population dynamics, of both partners in the interaction. These ecological benefits may at
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least partly compensate for the vulnerability caused by dependence on another species. Because interactions between species are not revealed in detail in the fossil record, there is little direct information on rates of secondary extinction. It is sometimes possible, however, to evaluate the risks of secondary extinction from study of living communities. Many plants cannot set seed without cross-pollination and rely on animals to transfer pollen. Such plants should be vulnerable to reproductive failure, and possibly extinction, if their pollinators decline, and species that have only one or a small number of pollinators are likely to be especially vulnerable. This vulnerability can be reduced by traits such as the ability to propagate vegetatively that reduce demographic dependence on seeds. Bond (1995) showed that in some plant communities there are no species that have both a high dependence on animal pollinators for seed set and a high demographic dependence on seeds, despite wide variation among species in both sets of characteristics (Figure 3). One explanation for this pattern is that such species are unusual because their high dependence on other species means that they are very likely to go extinct.
Reproductive and Life History Traits A wide variety of reproductive and life history traits may influence the likelihood of extinction in some circumstances. Perhaps the most important is sexual reproduction. Sexual lineages appear able to evolve more quickly than parthenogenetic ones because genetic recombination generates more variability among
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individuals on which natural selection can act. Sexual species may therefore be better able to adapt to changed environmental conditions or to meet new challenges from other species. The taxonomic distribution of parthenogenetic lineages suggests that they are short lived: With few exceptions, no higher taxa (genera, families, etc.) consists solely of parthenogens; almost all parthenogens have close sexual relatives and are likely to be recently derived from sexual species (Maynard Smith, 1978). Species with resting or resistant stages in their life cycle may be better able to pass through environmental catastrophes than species in which all life stages are vulnerable to environmental changes. In the islands of the Lesser Antilles, for example, butterflies are better able to persist on small islands than are birds or mammals, perhaps because they are able to pass through unfavorable seasons as diapausing eggs and pupae. Similarly, reptiles and amphibians are resistant to extinction, possibly by virtue of their ability to survive for long periods in protected micro environments without having to feed (Ricklefs and Lovette, 1999).
Geographic Patterns in Extinction Natural extinction rates vary along two major geographic axes: Extinction rates are lower for marine than terrestrial organisms, and extinction rates may be higher near the equator than at high latitudes. The low extinction rates of marine organisms are presumably due to their large geographic rangesFthe oceans are bigger and less subdivided than the continentsFand the high dispersal ability of many species that have larval life stages that drift in the plankton. The effects of latitude on extinction rates are less distinct, but where extinction rates have been shown to vary with latitude they tend to be higher in the tropics. Tropical species often have smaller geographic ranges and lower population densities than species at higher latitudes and may thus be more vulnerable to the effects of environmental change (Lawton, 1995). Also, some particularly species-rich tropical environments, such as the low-sediment, low-nutrient, shallow-water platforms that support reef and related communities, are easily disrupted by changes in climate and sea level (Jablonski, 1995).
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Figure 3 The relationship between an index of dependence on animal pollinators for seed set and dependence on seeds for regeneration for species of spring flowering herbs in a temperate deciduous forest. Any species that was both dependent on pollinators for seed set and dependent on seeds to regenerate would be considered at high risk of extinction due to pollinator failure. (Redrawn with permission from Bond WJ (1995) Assessing the risk of extinction due to pollinator and disperser failure. In: Lawton JH and May RM (eds.) Extinction Rates, pp. 131–147. Oxford: Oxford Univ. Press.)
The diversity of any lineage of organisms through time reflects the balance of the rates of loss of species by extinction and gains by speciation. Because extinction rates vary among lineages, extinction is an important factor shaping patterns of biodiversity. Much of the explanation for the very high diversity of insects is that, owing presumably to traits such as small size, high abundance, and high mobility, they have low extinction rates. Essentially no insect families have gone extinct during the past 50 million years, and some living genera and species with good fossil records are of Miocene age or older (Labandeira and Sepkoski, 1993). Species diversity of insects has therefore accumulated over long periods of time. Mammals, on the other hand, appear to evolve and speciate rapidly, but they are a minority taxon because their extinction rates are high.
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Insects and mammals provide an extreme example of contrasts in the balance of extinction and speciation rates, but in general extinction and speciation rates are positively correlated among different lineages (Figure 4). Such a relationship could arise if total species number in a lineage is held at equilibrium by competition between species so that a new species can only establish by occupying a niche left vacant by a species that has gone extinct. However, the relationship was first shown for groups of animals undergoing rapid increase in diversity (Stanley, 1979). There are three possible causes of the correlation between rates of speciation and extinction: 1. The effects of dispersal and gene flow: Dispersal rates should be correlated with resistance to extinction, but the gene flow resulting from high dispersal should also prevent genetic divergence of populations, thus impeding allopatric speciation. This explanation may apply to marine gastropods during the Late Cretaceous, when lineages with planktonic larvae and large ranges not only were less likely to go extinct but also were less likely to produce new species than those with direct development and restricted dispersal (Hansen, 1983). 2. The effects of niche breadth: Ecologically specialized species are likely to be vulnerable to environmental change, but they also tend to have patchy distributions, and this spatial subdivision should promote divergent evolution of local populations and the generation of many species. Generalists may be resistant to extinction, but their lack of spatial population structure also impedes divergent evolution among local populations.
Figure 4 The relationship between extinction rate and diversification rate for lineages of animals (J) and plants (K). Because diversification rate equals speciation rate minus extinction rate, the positive relationship shows that rates of extinction and speciation must be positively correlated (if not, the relationship on the graph would be negative). Extinction rates are measured per million species years and calculated as the reciprocal of species durations.
3. The effects of rarity: Species with small populations are prone to extinction. Somewhat controversially, it is believed that speciation may be enhanced by small or fluctuating population sizes (Futuyma, 1998). Because extinction is selective for particular characteristics of species, it can act as a filter through which certain types of species are more likely to pass. Selective extinction therefore shapes the composition of ecological assemblages of species. This filtering effect can be seen most clearly in mass extinctions, which typically leave in their wake ‘‘survival faunas’’ dominated by small numbers of wide-ranging and abundant generalist species of a few simple ecological types. The examples shown in Figures 2 and 3 illustrate some more subtle effects of the continuous operation of extinction filters, shaping respectively the patterns of distribution and abundance in living marsupials and the combinations of demographic characteristics of living plants. In some cases, directional trends in evolution and the development of communities can be opposed or curtailed by selective extinction. This effect can produce taxon cycles, which occur if derived species tend to evolve characteristics that make them vulnerable to extinction. For example, species that colonize islands are often generalists that are abundant and competitively dominant and quickly become widespread. Their descendants, however, tend to become more specialized and less mobile, occupy fewer habitats, lose their competitive ability, and sustain smaller and more subdivided populations. These trends eventually lead to extinction and the repetition of the cycle as sets of derived species are replaced by newly invading generalists (Ricklefs and Miller, 1999). Taxon cycles are most visible on island chains, where ecological communities are relatively simple and the patterns of distribution of related species on different islands provide clues to the direction of evolution. However, similar processes probably operate over larger areas on continents and in the oceans. What can the study of natural extinctions teach us about the coming wave of human-caused extinctions? There are at least two messages. First, species durations among different taxa in the fossil record are positively related to rates of endangerment of living species in the same taxa (McKinney, 1997). This suggests that the characteristics that have made species vulnerable to extinction under natural conditions also make them sensitive to human impacts on the environment, and in the absence of better information these characteristics could be used to identify species likely to be at risk in the near future. Second, the selectivity of extinction means that extinction rates will be higher in certain ecological types and taxonomic groups than in others, and if environmental pressures continue for a sufficient amount of time some groups may be removed entirely. The result will be a much greater impoverishment of biodiversity than would be the case if extinctions were randomly distributed among species.
See also: Extinction, Causes of. Extinction in the Fossil Record. Mammals (Late Quaternary), Extinctions of. Mammals (PreQuaternary), Extinctions of. Mass Extinctions, Concept of. Population Density. Species Interactions
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References Bennett KD (1997) Evolution and Ecology: The Pace of Life. Cambridge, UK: Cambridge Univ. Press. Bond WJ (1995) Assessing the risk of extinction due to pollinator and disperser failure. In: Lawton JH and May RM (eds.) Extinction Rates, pp. 131–147. Oxford: Oxford Univ. Press. Brown JH (1995) Macroecology. Chicago: Univ. of Chicago Press. Coope RG (1995) Insect faunas in ice age environments: Why so little extinction? In: Lawton JH and May RM (eds.) Extinction Rates, pp. 55–74. Oxford: Oxford Univ. Press. Cotgreave P (1993) The relationship between body size and population abundance in animals. Trends Ecol. Evol. 8: 244–248. Erwin DH (1998) The end and the beginning: Recoveries from mass extinctions. Trends Ecol. Evol. 13: 344–349. Foufopoulos J and Ives AR (1999) Reptile extinctions on land-bridge islands: Lifehistory attributes and vulnerability to extinction. Am. Nat. 153: 1–25. Futuyma DJ (1998) Evolutionary Biology. Sunderland, MA: Sinauer. Hansen TA (1983) Modes of larval development and rates of speciation in early Tertiary neogastropods. Science 220: 501–502. Hanski I (1999) Metapopulation Ecology. Oxford: Oxford Univ. Press. Jablonski D (1991) Extinction: A paleontological perspective. Science 253: 754–757. Jablonski D (1995) Extinction in the fossil record. In: Lawton JH and May RM (eds.) Extinction Rates, pp. 25–44. Oxford: Oxford Univ. Press. Johnson CN (1998) Species extinction and the relationship between distribution and abundance. Nature 394: 272–274.
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Labandeira CC and Sepkoski JJ (1993) Insect diversity in the fossil record. Science 261: 310–315. Lawton JH (1995) Population dynamic principles. In: Lawton JH and May RM (eds.) Extinction Rates, pp. 147–163. Oxford: Oxford Univ. Press. May RM, Lawton JH, and Stork NE (1995) Assessing extinction rates. In: Lawton JH and May RM (eds.) Extinction Rates, pp. 1–24. Oxford: Oxford Univ. Press. Maynard Smith J (1978) The Evolution of Sex. Cambridge, UK: Cambridge Univ. Press. McKinney ML (1997) Extinction vulnerability and selectivity: Combining ecological and paleontological views. Annu. Rev. Ecol. Syst. 28: 495–516. Niklas KJ, Tiffney BH, and Knoll AH (1983) Patterns in vascular land plant diversification. Nature 303: 614–616. Ricklefs RE and Lovette IJ (1999) The roles of island area per se and habitat diversity in the species–area relationships of four Lesser Antillean faunal groups. J. Anim. Ecol. 68: 1142–1160. Ricklefs RE and Miller GL (1999) Ecology, 4th ed. New York: Freeman. Stanley SM (1979) Macroevolution: Patterns and Process. San Francisco: Freeman. Thompson JN (1994) The Coevolutionary Process. Chicago: Univ. of Chicago Press. Vrba ES (1987) Ecology in relation to speciation rates: Some case histories of Miocene–Recent mammal clades. Evol. Ecol. 1: 283–300. Webb NR and Thomas JA (1994) Conserving insect habitats in heathland biotopes: A question of scale. In: Edwards PJ, May RM, and Webb NR (eds.) Large-scale Ecology and Conservation Biology, pp. 129–152. Oxford: Blackwell.
Glossary Conditions Physical features of the environment, such as substrate type, ambient temperature, or salinity, that affect the ability of organisms to survive, grow, and reproduce. Dispersal The movement of an individual organism away from its place of origin to the place where it breeds (also, movement by an adult from one breeding location to another). Pseudoextinction The disappearance of a species from the fossil record due not to the death of all its members but to an evolutionary change that results in it being classified as a new species.
Introduction Most species have durations that are very short relative to the history of life, and it is likely that 99% of all species that have ever lived are now extinct. Extinction, therefore, is very much a natural process that produces continuous turnover in the membership of biological assemblages as species are steadily lost by extinction and replaced by speciation. Natural extinctions may be divided into two kinds: those that happened during geologically brief periods of crisis when many taxa disappeared (the mass extinction events) and those during the long intervals of ‘‘background’’ time between mass extinctions. Mass extinctions have attracted a great deal of interest because they bit so deeply into standing biodiversity and because the biotas that reformed after mass extinctions were often quite different from those that existed before; they dramatically reshaped world patterns of biodiversity. However, 95% or more of the total number of extinctions have taken place outside mass extinctions (May et al., 1995). These background extinctions have been most important in producing turnover in species assemblages. Differences in the probability of extinction for different types of organisms interact with rates of origination of new lineages to shape patterns of biodiversity. To understand patterns of biodiversity it is therefore essential that the process of extinction be understood. In particular, we need to know whether extinction rates vary among different types of organisms and to identify the
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Quaternary The past 2 million years (approximately) of Earth history, including the Pleistocene and Holocene (or Recent) epochs, and characterized by the extreme fluctuations in global temperature that produce the ice ages. Resources Physical and biotic features of the environment, such as shelter sites or foods, that are required by organisms and are consumed such that use by one individual reduces their availability to others. Secondary extinction Extinction of a species resulting from the extinction of another species on which it relies.
characteristics of taxa that make them more or less vulnerable to extinction. Extinction can be studied at the level of higher taxaFgenera, families, and so onFbut this article is concerned primarily with extinctions of species.
Natural Causes of Extinction The causes of extinction can be divided into two types: changes in the environment and interactions with other species.
Changes in the Environment Populations of all species fluctuate in abundance. A large part of this variation is due to chance variation in environmental conditions, such as variations in weather or events such as cyclones, which can be regarded as environmental ‘‘accidents.’’ Species vary in their ability to resist accidents, but for any species there will eventually come an environmental event of sufficient magnitude to wipe it out, or an unlucky succession of smaller blows that drive its abundance down to zero, even when there is no trend in average conditions. Additionally, species may be driven extinct by directional changes in the environment, such as changes in temperature to levels outside their tolerance or the disappearance of
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key habitats. Species can respond to such changes in the environment by (i) acquiring adaptations to the changed conditions (‘‘evolving out of trouble’’), (ii) shifting their geographic ranges to remain within a set of suitable conditions (‘‘moving out of trouble’’), or (iii) going extinct. If the pace of environmental change is fast relative to the rate of evolution, the first of these responses is much less likely than the other two. The fossil record provides many examples of extinctions apparently driven by environmental changes of many different kinds, especially during mass extinctions events. Environmental changes have been much more extreme and rapid during some periods of Earth history than during others, but environmental conditions have never been truly static. Global temperatures have trended downwards for much of the past 50 million years, and at a finer temporal scale variations in the earth’s orbit produce fluctuations in climate with periodicities in the range of 10,000 to 400,000 years. These are called Milankovitch cycles, and during the past 2 million years they have produced the succession of ice ages, but they must have forced rapid swings in climate throughout Earth history (Bennett, 1997).
Interactions with Other Species The population growth rates of species are constrained by the species predators, parasites, and competitors. The abundance of a species will be reduced if its natural enemies become more abundant or evolve greater efficiency, or if its geographic range is invaded by a new enemy to which it has not evolved defenses. It is generally difficult to reconstruct such interactions in the fossil record, but some patterns may reflect the impact of predators on prey species. For example, the number of species of endobyssate bivalves gradually declined through the Mesozoic. These species were abundant, immobile, and lay partly exposed on the open seafloor. Their decline coincided with radiations of marine crabs, teleost fish, and carnivorous snails, groups that account for most predation on modern bivalves and to which the endobyssates must have been vulnerable (Stanley, 1979). The few present-day survivors of the group live in conditions with low predator pressure. Recent experience shows that prey species can be rapidly driven extinct by unfamiliar predators that invade their habitat. The carnivorous snail Euglandina rosea, for example, has caused the extinction of hundreds of species of endemic snails, including 600 of more than 1000 original species from the Hawaiian Islands, since its introduction to many Pacific islands in the 1970s. Such a rapid course of events would be unresolvable in the fossil record. Probably, the impacts of environmental changes and of other species interact in subtle ways to cause extinction. For example, a species might experience a slight environmental change that reduces its population without driving it extinct and to which it could readily adapt given sufficient time. However, the same change might favor a competitor or trigger a range expansion by an unfamiliar predator suited to the new conditions. Interactions of this kind could mean that quite small environmental changes could have dramatic consequences leading ultimately to extinction.
Lifetimes of Species Variation among Taxonomic Groups The oldest extant species known is the tadpole shrimp, Triops cancriformis, a small freshwater crustacean found in temporary pools in arid regions of Eurasia and north Africa that is indistinguishable from 180-million-year-old fossils bearing the same name. Most species do not live to this age, as shown in Table 1. The lifetime of a species begins with its origin in a speciation event and ends either when it dies out, leaving no descendants, or when its characteristics have been sufficiently changed by evolution that it is classified as a new species. The first type of disappearance of species is ‘‘real’’ extinction, and the second is referred to as pseudoextinction. This distinction is important but not easy to draw in practice. Our understanding of species life spans derives from study of the fossil record, and when a recognizable species disappears from the record it can be difficult to determine whether it has died out or evolved into something else. Information in Table 1 is based on real extinctions when the distinction can be made,
Table 1 Durations of species and extinction rates for major groups of organisms in the fossil record Taxon
Single-celled organisms Diatoms Dinoflagellates Planktonic foraminifera Benthic foraminifera Plants Early vascular plants Pteridophytes Gymnosperms Monocots Dicots All invertebrates Reef corals Mollusks: Marine gastropods Marine bivalves Mesozoic ammonites Upper Cambrian trilobites Marine ostracods Silurian graptolites Echinoderms Echinoids Crinoids Bryozoans Freshwater fish Birds Mammals Cenozoic mammals Horses Primates
Estimated mean species duration (millions of years)
Extinction rate (extinctions per million species years)
8 13 7–20
0.12 0.08 0.14–0.05
25
0.04
10–14 7–15 2–15 4 3 11 20
0.1–0.07 0.14–0.07 0.5–0.07 0.25 0.33 0.09 0.05
10 15 1 1.3
0.1 0.07 1 0.77
8 2
0.12 0.5
6 6.7 12 3 2.5 1.4 1–2 4 1
0.17 0.15 0.08 0.33 0.42 0.71 1–0.5 0.25 1
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but most estimates include an unknown combination of real and pseudoextinctions. There is considerable variation in species life spans among different groups of organisms. In general, it seems that species of unicellular organisms last longer than species of multicellular organisms, and invertebrates appear to last longer than vertebrates. The most long-lived animal groups tend to be marine rather than terrestrial, although too little is known about species durations of marine vertebrates or terrestrial invertebrates to judge differences between marine and terrestrial species independent of the difference between vertebrates and invertebrates. Some marine invertebrate groups that are now entirely extinct (the trilobites, ammonites, and graptolites) had short species durations, even though they were successful, abundant, and species rich for long periods of geological time. Among plants, species durations were longer in groups that appeared early in the evolutionary history of plants but have tended to shorten in recently evolved groups. The inverse of the typical duration of species in a given taxonomic group can be used as a measure of the probability of extinction per unit time for species belonging to that group: Long durations equate to low probabilities of extinction. In Table 1, probabilities of extinction have been expressed as the rates of extinction per million species years. Thus, marine gastropods typically last 10 million years, so a sample of 1 million marine gastropod species would be expected to experience 0.1 extinctions per year.
Variation within Taxonomic Groups The distributions of species lifetimes within higher taxa are typically right-skewed: Most species have short durations, but a small minority are long-lasting (Figure 1). There could be two causes for this pattern. First, only a few species might have characteristics that make them intrinsically resistant to extinction, whereas most are sensitive to extinction risk. Second, species might not vary in their susceptibility to extinction, but
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if many independent factors can cause extinction only a small minority of species will be lucky enough to avoid extinction for long. Probably both factors play a part in shaping distributions of species durations.
Risk of Extinction in Relation to Species Age Does the likelihood that a species will go extinct depend on its age? One might think that it should because the longer a species stays in existence the more adaptations to its environment it can accumulate; older species should therefore be better at avoiding extinction. This idea can be tested by examining species survivorship curves. A species survivorship curve shows the relationship between age and the proportion of species in a taxon surviving to each age. Such curves are typically log linear; that is, when the proportion surviving is plotted logarithmically its decline with age approximates a straight line. This shows that the proportion of species going extinct is approximately constant with respect to age. The constancy of extinction probability with species age can be explained by assuming that the environment of any species is continually changing so that even if the species continually adapts, its fitness lags behind the current condition of the environment. Thus, no matter how long a species lasts it can never reach a condition of optimal adaptation. There are two forms of this explanation. The first assumes that the probability of extinction for a species is determined primarily by its interactions with other species and that each species is under constant selection pressure to increase its fitness relative to these other species. However, adaptations in one species that increase abundance at the expense of other species will be met by counteradaptations from them so that, on average, no species improves its fitness with time. This is the Red Queen hypothesis, named after the character in Lewis Carroll’s Alice Through the Looking Glass in whose world ‘‘it takes all the running you can do, just to stay in one place.’’ The Red Queen hypothesis predicts that extinction rates will be
Figure 1 Species durations of Silurian graptolites of the British Isles. (Reproduced from Stanley SM (1979) Macroevolution: Patterns and Process. San Francisco: Freeman, with permission from W.H. Freeman and Company.)
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approximately constant with respect to absolute time. The second form of the explanation assumes that it is the abiotic environment that is continually changing. Changes in the abiotic environment will tend to be episodic and will therefore produce fluctuations in extinction rates with time, but their effects will still be independent of species age. It is not clear which form of the hypothesis is closer to the truth.
The Selectivity of Extinction Extinction may be largely a matter of the bad luck of environmental change, exacerbated perhaps by pressure from other species; however, the fact that species durations vary so widely among higher taxa suggests that biological characteristics of species influence their susceptibility to extinction. Three types of studies have helped to identify these characteristics. First, the attributes of species that have short versus long durations in the fossil record can be compared. A common variant of this technique compares species that persisted through mass extinction events with those that did not. Second, the living faunas of ‘‘land-bridge islands’’ can be compared with their presumed original faunas. A land-bridge island is an island formed as a result of isolation from the mainland by rising sea levels during the Pleistocene. Such islands typically have fewer species than do similar areas of mainland habitat to which they were once connected, reflecting extinctions caused by the pressure of reduced habitat area. Third, extinction of local populations can be observed directly in contemporary ecological studies. The second and third approaches focus on population rather than species extinctions, but the extinction of a species is the end point of a series of population extinctions, so such studies may still reveal traits that correlate with risk of extinction at the species level. The following traits consistently emerge from many studies of the selectivity of extinction: rarity, dispersal ability, body size, and specialization.
Rarity The commonness or rarity of a species is a function of two factors: its geographic range and its population density where it occurs. Both components of rarity influence extinction risk.
Geographic Range There is strong evidence from the fossil record (mainly for marine invertebrates) that species with large ranges have lower extinction rates (Jablonski, 1995; McKinney, 1997). There are probably two causes for this effect. First, at a given scale, a disturbance will affect a smaller proportion of the range of a widespread rather than of a geographically restricted species. In the extreme, a single catastrophic event may wipe out a localized species but have little impact on a widespread species. Second, even if an environmental change affects a very large area, it is likely that some populations of widespread species will persist in isolated refuges that provide some local protection from the change. Species that hang on in such refuges may reinvade their original ranges once conditions
improve. This is probably part of the explanation for the existence in the fossil record of ‘‘Lazarus species’’ that vanish during periods of environmental crisis and then reappear much later. The effect of range size on extinction risk tends to be strongest for background extinctions, and it may weaken or disappear in mass extinctions. This seems to have been the case for marine mollusks, for example (Jablonski, 1991), and is probably because mass extinctions were caused by events that affected such large areas and had such profound impacts that even widespread species were susceptible to them.
Local Abundance Population density is generally not well represented in the fossil record, but patterns of extinction of populations on land-bridge islands and in the present day show that local extinction is more likely for species with low population densities. For example, Foufopoulos and Ives (1999) found that reptile species with low population densities were more likely to go extinct from land-bridge islands in the Mediterranean Sea. The causes of extinction of small populations have been widely discussed in the literature on conservation. Briefly, small populations are more vulnerable than large populations because (i) they may go extinct more quickly when chance environmental variation causes fluctuations in abundance; (ii) they are affected by chance demographic fluctuations, such as occasional production of biased sex ratios of offspring, that would be averaged out in large populations; (iii) they may lose genetic variation and experience high levels of inbreeding and inbreeding depression; and (iv) they may be subject to Allee effectsFthat is, social or reproductive dysfunction as a direct result of low numbers.
The Relationship between Range and Abundance The components of rarityFgeographic range size and population densityFare generally positively related among species: Species with small geographic ranges also tend to have low population densities, and wide-ranging species have high population densities. This pattern has been found in many terrestrial plant and animal taxa, although it remains almost unstudied in marine organisms. Why there should be a positive relationship between range and abundance is not clear. Several ecological mechanisms have been proposed as its cause, but two ideas have been especially influential. First, Brown (1995) argued that niche breadth is positively correlated with both range size and population density because species with broad niches can exist under a wider range of conditions and use more types of resources than can species with narrow niches; variation among species in niche breadth therefore produces a positive relationship between range and density. Second, species that reach high local densities should be both more resistant to extinction on habitat patches because their populations are larger and produce more migrants that are able to recolonize habitat patches after local extinctions (Hanski, 1999). High local abundance therefore results in wide geographic distribution. To the extent that geographic range and local abundance affect extinction risk independently of one another, the correlation between them should exaggerate differences among species in extinction risk. Rare species face double jeopardy:
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Spatial Structure of Populations Another aspect of rarity is ubiquity or patchiness of distribution within the geographic range. The distributions of practically all species are discontinuous at some scale, but the degree of patchiness varies, reflecting specialization for habitats or resources that are themselves patchily distributed. In a species that has a patchy distribution, metapopulation dynamics are likely (Hanski, 1999). That is, the risk of extinction of populations on discrete patches of habitat may be high, but local populations are eventually reestablished by migrants from other populations. Recolonization will involve a time lag that depends on the distance between patches and the dispersal ability of the species. A general deterioration in the quality of habitat for a species is likely to cause contraction of larger habitat patches and the disappearance of smaller ones, causing local extinctions and simultaneously increasing the distance between surviving patches and thus reducing the probability of migration. Patchily distributed species should therefore be more likely to go extinct as a result of environmental change than should continuously distributed species. The sensitivity of patchy species to environmental change has been demonstrated for insects in Great Britain subject to human-caused changes (Webb and Thomas, 1994), but it is likely to be general to any form of shift in environmental conditions. Patchiness of distribution is loosely correlated with the other components of rarity so that widespread and locally abundant species tend to be continuously distributed within their ranges, whereas rare species are likely to be patchy.
Figure 2 Relationships between size of geographic range and population density for species of Australian marsupials: (a) all species other than those defined as ancient and (b) ancient species only. Ancient species are those that diverged from their closest living relative more than 4 million years ago and have therefore demonstrated resistance to extinction. The shaded triangle defines the region of distribution-abundance space from which species would need to have gone extinct to produce the pattern observed among ancient species. (Reproduced with permission from Johnson CN (1998) Species extinction and the relationship between distribution and abundance. Nature 394: 272–274.)
The vulnerability that comes from having a small range is compounded with the vulnerability due to low abundance. Common species, on the other hand, are likely to be highly resistant to extinction because they combine high abundance with large ranges. For example, Johnson (1998) showed that among Australian marsupials, ancient species (those that diverged from their closest relative more than 4 million years ago) are very unlikely to have both small ranges and low population densities, although this combination occurs frequently among young species (Figure 2). This suggests that species with low abundance and small ranges tend to be short lived. There are ancient marsupials with small ranges but they have unusually high densities, and conversely there are species with low densities but they have unusually large ranges, implying that a high density can compensate for the vulnerability that comes from having a small range and vice versa.
Dispersal Ability Dispersal ability is positively associated with species longevity for two reasons. First, species that disperse widely tend to have large geographic ranges, and their resistance to extinction can be a direct result of large range. Marine gastropod snails, for example, have two different forms of development. In some, the egg is released into surface waters and develops into a larval form that feeds in the plankton and drifts widely before settling and developing into an adult snail. This form of development promotes wide dispersal. Others have direct development in which eggs and young grow up close to the parent. Species with planktonic development have larger geographic ranges and longer durations in the fossil record than do species with direct development (Jablonski, 1995). Second, species that disperse widely are better able to recolonize after going extinct from part of the range, and they can more rapidly shift their ranges to track changes in the distribution of their preferred climates and habitats. During the Quartenary in the Northern Hemisphere, the distribution of habitats changed very rapidly as ice sheets repeatedly advanced and receded. These changes produced remarkably few extinctions among Northern Hemisphere beetles. Instead, species shifted their geographic ranges to keep pace with the changing distribution of habitats, an effect that was more dramatic in flighted than in flightless species (Coope, 1995). Probably, dispersal ability and local abundance interact to confer high resistance to extinction because high local abundance means that large numbers of dispersers are produced,
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resulting in the potential for rapid shifting of range boundaries as conditions change. This combination of characteristics might protect species that have specialized habitat requirements and small geographic ranges and would otherwise be vulnerable to extinction.
Body Size It often seems to be the case that large-bodied species are at higher risk of extinction than small-bodied species. Although there are exceptions, this pattern is reasonably consistent in the fossil record both for background extinctions and for mass extinctions (McKinney, 1997), and it also emerges in extinctions on land-bridge islands (Brown, 1995). There are several reasons why large-bodied species might be particularly vulnerable to extinction: 1. Potential rate of population increase declines with body size because large-bodied species generally have longer generation times and lower fecundity than do small-bodied species. This means that large-bodied species will generally recover more slowly from population declines, and because they produce fewer offspring they may be slower to track habitats than will small-bodied species. 2. Individuals of large-bodied species generally need larger areas, and large-bodied species are therefore strongly affected by declines in habitat area. 3. Population density tends to decline with body size so that large species are often naturally rare. This is partly compensated by a tendency for size of geographic range to increase with body size, but this relationship is often weak or absent so that total population size is usually much less for large than small species. The decline in population density with body size is clearest when species of very different size (e.g., mice and elephants) are compared, but in guilds of ecologically similar species it is often the case that density increases with body size, possibly because larger species are better competitors for resources (Cotgreave, 1993). At this finer scale of comparison, therefore, large-bodied species might be more resistant to extinction than small-bodied species.
Specialization Species can be classed as ‘‘specialists’’ or ‘‘generalists’’ on three criteria: the range of conditions that they are adapted to tolerate, the range of resources that they are able to use, and the degree of their evolved dependence on a small number of other species.
Conditions Species that are narrowly adapted to environmental conditions are likely to be the first to go extinct when the environment changes. This is difficult to demonstrate in the fossil record, however, because it is not possible to measure directly the environmental tolerances of fossil species. Instead, environmental tolerances are inferred from geographic distributions. Species with small geographic ranges will necessarily occupy a narrow range of climate zones and habitats, but it
does not follow from this that their environmental tolerances are narrow. Some species that could potentially be widely distributed have small ranges because of population history, geographic barriers to movement, or poor dispersal ability or because range expansion is prevented by interactions with other species (competitors, predators, and so on). Therefore, although there is abundant evidence from the fossil record that species with small geographic ranges are extinction-prone, there is much less evidence for the commonsense view that the breadth of tolerance of environmental conditions directly affects extinction risk.
Resources Species that depend on a narrow range of types of resources are likely to be more sensitive to changes in resource abundance than generalists that can easily switch resources. This vulnerability may be partly compensated by the fact that specialization on a particular resource may be more likely to evolve if that resource is abundant and widespread. For example, feeding on grasses by mammals requires extensive specialization of the teeth and digestive system, and increases in body size, to overcome the abrasiveness and poor nutritional quality of grasses. However, because of the abundance of grasses many mammals have evolved these adaptations, and grazing mammals typically have high local abundance and large geographic ranges. Nonetheless, grazing mammals in Africa have suffered higher extinction rates since the Miocene than mixed grazer/browsers, as the extent of grasslands has fluctuated during the Pliocene and Pleistocene (Vrba, 1987).
Interactions Specialization is taken a step further in species that have evolved a close dependence on one or a small number of other species. For example, many herbivorous insects feed on only one species of plant, and many predators attack only one or a small number among many possible species of prey. Of particular interest are mutualistic interactions, in which species provide benefits to one another. Figs, for example, rely on fig wasps for pollination, and fig wasps in turn lay their eggs only in the flowers of figs. This interaction tends to be highly species specific, with each species of fig visited by only one species of fig wasp and each partner in the interaction completely dependent on the other for reproduction. Such tight species specificity results from coevolution, in which each species in the interaction evolves special characteristics in response to evolutionary changes in the other to increase its benefit from the interaction. Specialization of this kind is classically regarded as an extinction trap because the specialist will inevitably go extinct if the species that it depends on goes extinct or becomes very rare. This view is probably an oversimplification. Careful study of some species-specific interactions has revealed more flexibility and greater potential for rapid evolutionary response to changes in the abundance of interacting species, including the ability to switch to new partners, than was previously assumed (Thompson, 1994). Also, mutualistic interactions have the general effect of increasing the geographic range and abundance, and stabilizing the population dynamics, of both partners in the interaction. These ecological benefits may at
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least partly compensate for the vulnerability caused by dependence on another species. Because interactions between species are not revealed in detail in the fossil record, there is little direct information on rates of secondary extinction. It is sometimes possible, however, to evaluate the risks of secondary extinction from study of living communities. Many plants cannot set seed without cross-pollination and rely on animals to transfer pollen. Such plants should be vulnerable to reproductive failure, and possibly extinction, if their pollinators decline, and species that have only one or a small number of pollinators are likely to be especially vulnerable. This vulnerability can be reduced by traits such as the ability to propagate vegetatively that reduce demographic dependence on seeds. Bond (1995) showed that in some plant communities there are no species that have both a high dependence on animal pollinators for seed set and a high demographic dependence on seeds, despite wide variation among species in both sets of characteristics (Figure 3). One explanation for this pattern is that such species are unusual because their high dependence on other species means that they are very likely to go extinct.
Reproductive and Life History Traits A wide variety of reproductive and life history traits may influence the likelihood of extinction in some circumstances. Perhaps the most important is sexual reproduction. Sexual lineages appear able to evolve more quickly than parthenogenetic ones because genetic recombination generates more variability among
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individuals on which natural selection can act. Sexual species may therefore be better able to adapt to changed environmental conditions or to meet new challenges from other species. The taxonomic distribution of parthenogenetic lineages suggests that they are short lived: With few exceptions, no higher taxa (genera, families, etc.) consists solely of parthenogens; almost all parthenogens have close sexual relatives and are likely to be recently derived from sexual species (Maynard Smith, 1978). Species with resting or resistant stages in their life cycle may be better able to pass through environmental catastrophes than species in which all life stages are vulnerable to environmental changes. In the islands of the Lesser Antilles, for example, butterflies are better able to persist on small islands than are birds or mammals, perhaps because they are able to pass through unfavorable seasons as diapausing eggs and pupae. Similarly, reptiles and amphibians are resistant to extinction, possibly by virtue of their ability to survive for long periods in protected micro environments without having to feed (Ricklefs and Lovette, 1999).
Geographic Patterns in Extinction Natural extinction rates vary along two major geographic axes: Extinction rates are lower for marine than terrestrial organisms, and extinction rates may be higher near the equator than at high latitudes. The low extinction rates of marine organisms are presumably due to their large geographic rangesFthe oceans are bigger and less subdivided than the continentsFand the high dispersal ability of many species that have larval life stages that drift in the plankton. The effects of latitude on extinction rates are less distinct, but where extinction rates have been shown to vary with latitude they tend to be higher in the tropics. Tropical species often have smaller geographic ranges and lower population densities than species at higher latitudes and may thus be more vulnerable to the effects of environmental change (Lawton, 1995). Also, some particularly species-rich tropical environments, such as the low-sediment, low-nutrient, shallow-water platforms that support reef and related communities, are easily disrupted by changes in climate and sea level (Jablonski, 1995).
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Figure 3 The relationship between an index of dependence on animal pollinators for seed set and dependence on seeds for regeneration for species of spring flowering herbs in a temperate deciduous forest. Any species that was both dependent on pollinators for seed set and dependent on seeds to regenerate would be considered at high risk of extinction due to pollinator failure. (Redrawn with permission from Bond WJ (1995) Assessing the risk of extinction due to pollinator and disperser failure. In: Lawton JH and May RM (eds.) Extinction Rates, pp. 131–147. Oxford: Oxford Univ. Press.)
The diversity of any lineage of organisms through time reflects the balance of the rates of loss of species by extinction and gains by speciation. Because extinction rates vary among lineages, extinction is an important factor shaping patterns of biodiversity. Much of the explanation for the very high diversity of insects is that, owing presumably to traits such as small size, high abundance, and high mobility, they have low extinction rates. Essentially no insect families have gone extinct during the past 50 million years, and some living genera and species with good fossil records are of Miocene age or older (Labandeira and Sepkoski, 1993). Species diversity of insects has therefore accumulated over long periods of time. Mammals, on the other hand, appear to evolve and speciate rapidly, but they are a minority taxon because their extinction rates are high.
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Insects and mammals provide an extreme example of contrasts in the balance of extinction and speciation rates, but in general extinction and speciation rates are positively correlated among different lineages (Figure 4). Such a relationship could arise if total species number in a lineage is held at equilibrium by competition between species so that a new species can only establish by occupying a niche left vacant by a species that has gone extinct. However, the relationship was first shown for groups of animals undergoing rapid increase in diversity (Stanley, 1979). There are three possible causes of the correlation between rates of speciation and extinction: 1. The effects of dispersal and gene flow: Dispersal rates should be correlated with resistance to extinction, but the gene flow resulting from high dispersal should also prevent genetic divergence of populations, thus impeding allopatric speciation. This explanation may apply to marine gastropods during the Late Cretaceous, when lineages with planktonic larvae and large ranges not only were less likely to go extinct but also were less likely to produce new species than those with direct development and restricted dispersal (Hansen, 1983). 2. The effects of niche breadth: Ecologically specialized species are likely to be vulnerable to environmental change, but they also tend to have patchy distributions, and this spatial subdivision should promote divergent evolution of local populations and the generation of many species. Generalists may be resistant to extinction, but their lack of spatial population structure also impedes divergent evolution among local populations.
Figure 4 The relationship between extinction rate and diversification rate for lineages of animals (J) and plants (K). Because diversification rate equals speciation rate minus extinction rate, the positive relationship shows that rates of extinction and speciation must be positively correlated (if not, the relationship on the graph would be negative). Extinction rates are measured per million species years and calculated as the reciprocal of species durations.
3. The effects of rarity: Species with small populations are prone to extinction. Somewhat controversially, it is believed that speciation may be enhanced by small or fluctuating population sizes (Futuyma, 1998). Because extinction is selective for particular characteristics of species, it can act as a filter through which certain types of species are more likely to pass. Selective extinction therefore shapes the composition of ecological assemblages of species. This filtering effect can be seen most clearly in mass extinctions, which typically leave in their wake ‘‘survival faunas’’ dominated by small numbers of wide-ranging and abundant generalist species of a few simple ecological types. The examples shown in Figures 2 and 3 illustrate some more subtle effects of the continuous operation of extinction filters, shaping respectively the patterns of distribution and abundance in living marsupials and the combinations of demographic characteristics of living plants. In some cases, directional trends in evolution and the development of communities can be opposed or curtailed by selective extinction. This effect can produce taxon cycles, which occur if derived species tend to evolve characteristics that make them vulnerable to extinction. For example, species that colonize islands are often generalists that are abundant and competitively dominant and quickly become widespread. Their descendants, however, tend to become more specialized and less mobile, occupy fewer habitats, lose their competitive ability, and sustain smaller and more subdivided populations. These trends eventually lead to extinction and the repetition of the cycle as sets of derived species are replaced by newly invading generalists (Ricklefs and Miller, 1999). Taxon cycles are most visible on island chains, where ecological communities are relatively simple and the patterns of distribution of related species on different islands provide clues to the direction of evolution. However, similar processes probably operate over larger areas on continents and in the oceans. What can the study of natural extinctions teach us about the coming wave of human-caused extinctions? There are at least two messages. First, species durations among different taxa in the fossil record are positively related to rates of endangerment of living species in the same taxa (McKinney, 1997). This suggests that the characteristics that have made species vulnerable to extinction under natural conditions also make them sensitive to human impacts on the environment, and in the absence of better information these characteristics could be used to identify species likely to be at risk in the near future. Second, the selectivity of extinction means that extinction rates will be higher in certain ecological types and taxonomic groups than in others, and if environmental pressures continue for a sufficient amount of time some groups may be removed entirely. The result will be a much greater impoverishment of biodiversity than would be the case if extinctions were randomly distributed among species.
See also: Extinction, Causes of. Extinction in the Fossil Record. Mammals (Late Quaternary), Extinctions of. Mammals (PreQuaternary), Extinctions of. Mass Extinctions, Concept of. Population Density. Species Interactions
Natural Extinctions (not Human Influenced)
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