Patterns of biological extinction
Patterns of biological extinction Introduction When I give a talk about extinction, there are usually two questions I am asked: • Isn’t extinction a natural process? • What makes us think we’re so smart that we can manage species to prevent they’re extinction? I’ll deal with the first question in a bit later, but let’s ponder the second one for now. The data I just finished presenting shows pretty convincingly, I think, that human beings have an enormous impact on the earth and its inhabitants. Thus, we may or may not be smart enough to manage well, but one thing’s for sure. We will have an impact. We cannot avoid having an impact. We can only choose what kind of impact we’ll have. This observation is related to my earlier point that conservation biologists have to make decisions in the face of incomplete data. We don’t have any choice about whether or not to make a decision, and we don’t have any choice about whether we’re going to manage. We can only choose to manage in a way that we hope will produce the outcome we want (compare [14]).1 In some cases that may amount to “letting nature take its course.” In others it will involve more active, hands-on managing. So what about the first question? Isn’t extinction a natural process? There are two components to my answer: 1. Contemporary rates of extinction are vastly greater than they are typical of the geological past, and they are projected to get worse. 2. The pattern of extinction is non-random, and the species that survive may not be those that make the world an appealing place to live. 1
Or we can choose not to (consciously) manage and hope that things turn out the way we want them to.
c 2003–2009 Kent E. Holsinger
Figure 1: Past, present, and projected extinction rates [1]. To start, let’s take a look at what the Millenium Ecosystem Report has to say about extinction rates (Figure 1). Notice the scale on the vertical axis. It’s a logarithmic scale. So our best guess about the current extinction rate is that it’s 100-1000 times higher than the background extinction rate in the fossil record, and the projected future extinction rate 10-100 times greater than the current rate. Numbers like that are why you often hear it said that we are living through the sixth great mass extinction in the history of life.
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Background extinction It is the fate of most living things eventually to go extinct. The species diversity now is almost certainly greater than it ever has been in the past, but paleontologists tell us that more than 99% of the species that have ever lived are now extinct. Some take comfort that we seem to have recovered from the great extinctions of the past • Ordovician (440mya) — 50% of animal families • Devonian (360mya) — 30% of animal families • Permian (250mya) — 50% of animal families, including 95% of marine species • Triassic (210mya) — 35% of animal families • Cretaceous (65mya) — 60% of animal species We’re still here, these people would argue, and the world doesn’t look so bad. Until recently I argued that the fossil record showed that recovery from these extinctions took a long time.2 But reanalysis of the record of Phanerozoic diversity for marine invertebrates [7, 8] suggests that the apparent delay in recovery is an artifact of the incompleteness of the fossil record. The recovery of biodiversity may, in fact, be geologically instantaneous, i.e., on the order of 5 million years or less. So the optimist in me says that we are very unlikely to destroy life on this planet and that the diversity of life will recover fairly quickly once we are gone. The pessimist in me points out that I don’t want to live in a world that has substantially less diversity than the one I live in now, and that even if life’s diversity recovers instantaneously from the perspective of deep geological time, it’s not like to happen on a time scale of any interest to human beings.3 To me, that means we want to do what we can to reduce the rate of extinction, ideally to a rate 10-100 times lower than it is now.
The causes of extinction The causes of extinction are (mostly) fairly obvious, and we touched on one of the largest ones all ready — habitat destruction and conversion. But let’s spend a little time reminding ourselves what the causes of extinction are, because knowing those causes helps us better to understand their consequences. 2
Ordovician — 25 million years; Devonian — 30 million years; Permian/Triassic — 100 million years; Cretaceous — 20 million years 3 “Humans” didn’t even exist 5 million years ago, if by “human” we mean a member of the genus Homo.
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• Overexploitation Whales – A record three year cruise in the 19th century killed fewer than one hundred whales. – In 1933 almost 30,000 whales were killed, yielding 2.5 million barrels of whale oil. – By 1967 60,000 were killed, but they yielded only 1.5 million barrels of oil — because the larger species, e.g., Blues and Fins, had been hunted virtually to extinction. – Analyses of genetic diversity suggest pre-exploitation population sizes 6-20 times greater than current estimates [13].4 Atlantic cod Wildlife trade, orchids and succulents Predator control — until 1952 the Bald Eagle had a price on its head • Development — urbanization, agriculture, & mining Cape flora – 6,000 species of native vascular plants; 1,200 threatened; 36 are extinct – More than 60% of the area previously occupied by the Cape flora has been replaced by farms, plantations, roads, dams, towns, etc. – More than 80% of the $4 million earned in the cut-flower industry is extracted directly from the wild flora Dams: Pacific northwest salmon fishery has declined dramatically in the last 50 years. Many runs are now listed (or proposed for listing) under the Endangered Species Act. Nearly 30% of the ca. 1400 historical populations are extinct (14% of populations from coastal regions, 55% from interior regions) [4]. Deforestation (Table 1) is just one aspect of habitat conversion, although it is probably among the most extreme. 4 This estimate is very sensitive to estimates of the rate of nucleotide substitution in mitochondria. Roman and Palumbi use estimates of 1.5-2.0 ×10−8 per base pair per year. If the rate were higher, say, 1.5-2.0 ×10−7 per base pair per year, the pre-exploration population sizes would be estimated at 0.6-2 times greater than current estimates.
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Country/Region % of old growth forest USA 15 Washington & Oregon 13 Canada 52 British Columbia 40 Europe Western Europe 1 Scotland 1 Sweden 1 Finland 2 Norway 3 Oceania New Zealand 25 Australia 5–21 Asia China 1 Table 1: Proportion of old-growth forest remaining in selected temperate forest countries (from Table 11.2-6 [16]). • Invasive exotics Zebra mussel Chestnut blight Wilcove, Rothstein, Dubow, Phillips, and Losos [19] surveyed recovery plans for species listed under the United States Endangered Species Act and categorized the threats they identified into one of five categories: habitat degradation/loss, alien species, pollution, overexploitation, and disease. Table 2 shows the percentage of listed species for which each of these five factors was mentioned as a cause contributing to endangerment.5 In short, many species are going extinct for reasons very different from those that caused their extinction in the past. Those causes make it clear that we are responsible for the elevated rates of extinction, but they don’t tell us how many species are going extinct. 5
The numbers add to more than 100% because each species may face threats in more than one category.
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Cause Habitat degradation Alien species Pollution Overexploitation Disease
All Vertebrates (n = 1880) (n = 494) 85% 92% 49% 47% 24% 46% 17% 27% 3% 11%
Invertebrates (n = 331) 87% 27% 45% 23% 0%
Plants (n = 1055) 81% 57% 7% 10% 1%
Table 2: Causes of endangerment mentioned in species recovery plans [19]. Conservation status Secure/apparently secure Vulnerable Imperiled Critically imperiled Presumed/possibly extinct
Percent of taxa 67% 16% 8% 7% 1%
Table 3: Percentage of species in taxonomically well-characterized taxa falling into different endangerment categories in the United States.
Rates of extinction Rates of extinction are very difficult to estimate, because we don’t even know within an order of magnitude how many species there are. Nonetheless, we can be quite sure that a large proportion of taxa are threatened with extinction. A little less than 10 years ago, The Nature Conservancy [9] assessed the status of 20,892 species in groups that are taxonomically well-characterized in the United States (freshwater mussels, crayfishes, vertebrates, vascular plants, tiger beetles, butterflies/butterflies, and dragonflies/damselflies; Table 3). These statistics don’t tell us how many extinctions are happening. And depending on whether you’re an optimist or a pessimist you can take this as good news or as bad news. Two out of three species in the United States are apparently secure. That’s the good news. One out of three species in the United States is vulnerable or imperiled. That’s the bad news. But how do these numbers compare with what might have characterized the biota of the U.S. prior to the arrival of humans? Do they, in fact, tell us that extinction rates are elevated, or are they simply characteristic of what we would have found at any time in the 6
geological past? Are a large fraction of species on the edge of extinction during most of geological history? Two different approaches have been employed to try to compare current rates of extinction with those inferred from the fossil record.
Species-area relationships Statistics on the rates of extinction have mostly been inferred from a species-area relationship and projections of habitat destruction. S = CAz If we’re only interested in the proportion of species remaining after some portion of the habitat has been destroyed CA0z S0 = S CAz! z A0 = A
(1) (2)
z is generally between 0.15 and 0.35. So for example, if we’re interested in projecting the fraction of species that will be lost from tropical rainforests as a result of deforestation, we can make the following back of the envelope calculation. If current rates of tropical deforestation continue for another 30 years half of the remaining rain forest will be gone. If we then prevent all further deforestation, between 0.50.35 = 0.78 and 0.50.15 = 0.90 of the species presently there will remain, i.e., 10%–20% will go extinct. More sophisticated approaches use an exponential decay model, recognizing that the predictions of the above approach apply only after the remaining forest fragments have reach an immigration-extinction equilibrium. Notice, however, that these calculations only reflect the effects of lost habitat, not increased exposure to disease, competition with invasive exotics, overxploitation, or habitat degradation.
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Rates from known extinctions It may come as a surprise to you to learn that we can also get reasonable estimates of current extinction rates from examining documented extinctions in groups that are reasonably wellstudied. In the United States alone, for example, 45 vertebrates (over half of which are birds), 347 invertebrates, and 147 plants are either presumed or possibly extinct [9].6 By calculating the fraction of known species that have gone extinct in historical times, we get a direct estimate of extinction rates. The calculations that follow are based on the data and the approach described in [10, 15]. • 100 documented extinctions of birds and mammals worldwide in the last century out of ≈ 14, 000 total. That’s a rate of 7 × 10−3 yr−1 . • The average life span of bird and mammal species in the fossil record is about 1 × 106 years. This is equivalent to an extinction rate of about 1 × 10−6 y−1 . • So the recent historical rate of vertebrate extinctions is a little over 7,000 times greater than the background rate of extinction. The rates calculated by these very different approaches are reasonably comparable, given the great uncertainties involved. They suggest that contemporary rates of extinction are 100 to 1,000 (and possibley 10,000) times higher than at any time in the last 65 million years. The figures in Table 4 show how many documented extinctions have occurred in the last 400 years, along with an estimate of the corresponding median lifetime of taxa in each group (derived from [15]).
Critiques of these estimates Critics of estimates based on species-area relationships have pointed out that > 95% of the eastern forests in North America were cut while only 4 bird species went extinct7 . How can we account for this apparent discrepancy [12]? • The region was not simultaneously deforested. As agriculture moved westward, forest reclaimed abandoned fields. Forests always covered > 50% of the land area. 0.50.25 = 0.84 16% or 25-26 out of ≈160 forest species should have gone extinct. 6
We should probably change the vertebrate extinction number to 44, given the apparent rediscovery of the ivory-billed woodpecker [3]. 7 And maybe only 3, if the ivory-billed woodpecker is still extant.
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Animals
Plants
Molluscs Crustaceans Insects Vertebrates Fishes Amphibians Reptiles Birds Mammals Total Gymnosperms Dicotyledons Monocotyledons Palms Total
Extinct Threatened Extant Time to 50% extinction 191 354 105 60,000 4 126 4 × 103 — 6 61 873 10 — 4 229 2,212 4.7 × 10 600 29 452 2.4 × 104 900 3 2 59 3 × 10 3,000 23 167 6 × 103 2,000 3 116 1,029 9.5 × 10 350 3 59 505 4.5 × 10 250 15,000 485 3,565 1.4 × 106 2 242 758 — 5 120 17,474 1.9 × 10 1,000 462 4,421 5.2 × 104 1,700 4 925 2820 70 584 22,137 2.4 × 105 1,100
Table 4: Extinction in major taxa since 1600. • May not have been enough time for extinction. Species-area relationship is an equilibrium expectation. Committed to extinction versus actually extinct • Only 28 of the 160 species are restricted to eastern forests. The rest are widely distributed elsewhere and would have persisted there. They could have later moved back into eastern forests. (0.50.25 )(28) = 23.5
,
i.e., 23-24 of the 28 species should have persisted. Only 4-5 should have gone extinct, which is about what we saw. • We lost few bird species from eastern North American forests because we had few endemics to lose.
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Population deletions We tend to focus on extinction as a species-level phenomenon, but doing so substantially understates the impact we are having. So long as a single population of a species is extant the species is not extinct, even if 99.9% of its populations have been eliminated. Species may be eliminated from most of their former range and persist only in small refuge areas. Over a decade ago, population declines in amphibians began to receive world-wide attention. Hobbs and Mooney [5] cite several similar examples:8 • Yellow-legged frog (Rana muscosa) — 1989 survey found in only 1 of 27 sites where it had been found 10 years before. • Owens pupfish (Cyprinodon radiosus) — Originally widespread in Owens Valley. Once thought extinct. A single population was rediscovered in 1956. • 26 six species of west Australian mammals occur only as remnant populations occupying less than 20% of their original range. 42% of mammals originally found in the wheatbelt region are no longer found there, although only 14% of those are extinct in the entire state. • Half of the bird species in the agricultural part western Australia have declined in distribution and abundance since 1900.
Biological consequences of human-caused extinctions We have now seen that rate at which human-caused extinctions are occurring is different from the rate at which extinction occurred before we became so dominant.9 What are the immediate consequences of such extinctions? Geerat Vermeij [17] suggested three questions to be answered to understand the implications of extinction for human welfare. 1. Which kinds of species are susceptible to extinction, and which are not? 2. How will the extinction of species affect the communities in which these species lived and alter the evolutionary environment of surviving life forms? 3. Can new species evolve on a human-dominated planet to replace the species that have disappeared and, if so, what will they look like? 8
And don’t forget the example of Pacific northwest salmon populations cited earlier [4]. We’ll return to this topic again when we talk about landscape change in a couple of months. There is substantial evidence that human occupation of the Americas and of Australia led to many extinctions among large mammals. 9
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Group Proportion threatened1 Freshwater mussels 69% Crayfishes 51% Stoneflies 43% Freshwater fishes 37% Amphibians 36% Flowering plants 33% Gymnosperms 24% Pteridophytes 22% Tiger beetles 19% Butterflies 19% Reptiles 18% Odanates 18% Mammals 16% Birds 14% 1 Presumed/possibly extinct, critically imperiled, imperiled, or vulnerable Table 5: The taxonomic distribution of endangerment in the United States.
Selectivity of extinctions Vanished species are unlikely to be a random subset of the biota. • Karr (Barro Colorado) — ground-dwelling birds suffered higher rate of extinction than canopy dwellers [6]. • The proportion of species threatened differs dramatically among taxonomic groups in the United States (Table 5; [9]).
Consequences of extinctions If these speculations are correct, human caused extinctions have two properties: 1. They are depleting biological diversity at a rate greater than at any time in the last 65 million years. 2. The species that are going extinct are predominantly those adapted to special conditions of life in localized habitats. 11
The result is a more homogeneous biotic environment, one in which many of the same plants and animals are found worldwide — English sparrows, starlings, dandelions, wild oats. Most of the grasses you see on the hills of California are native to the Mediterranean. Native Californian grasslands are largely confined to serpentine outcrops. Nearly all of the vegetation in lowland areas of Hawaii is introduced from other areas in the tropics. Of the roughly 1,700 plants native to Hawaii, almost half are introduced (see [11] for a more careful analysis of this issue). Whether it is a good thing for the character of our natural world to be changed in this way is something we must decide on non-biological grounds. Life will continue on this planet whatever we decide, but what we decide will have an enormous impact on what kind of life does survive.
U. S. Endangered Species Act A U.S.-based course in conservation biology wouldn’t be complete without a brief introduction to the Endangered Species Act. We won’t go into all of its details, but there are a few important features that anyone finishing this course should be aware of. The Endangered Species Act of 1973 requires the U. S. Fish & Wildife Service (or the National Marine Fisheries Service, for certain marine species) to identify species of wildlife and plants that are endangered or threatened, based on the best available scientific and commercial data. §3(6) The term “endangered species” means any species which is in danger of extinction throughout all or a significant portion of its range other than a species of the Class Insecta determined by the Secretary to constitute a pest whose protection under the provisions of this Act would present an overwhelming and overriding risk to man. §3(19) The term “threatened species” means any species which is likely to become an endangered species within the foreseeable future throughout all or a significant portion of its range. §3(15) The term “species” includes any subspecies of fish or wildlife or plants, and any distinct population segment of any species of vertebrate fisho or wildlife which interbreeds when mature. The act recognizes five factors permitting listing: 1. Present or threatened destruction of habitat, 2. Overutilization for commercial, recreational, scientific, or educational purposes, 3. Losses due to disease or predation, 12
4. Inadequacy of existing laws and regulations to protect the organism in question, and 5. Other natural or man-made factors affecting its continued existence. Notice that rarity and endangerment are not the same thing. “Rarity” means uncommon. “Endangerment” means likely to go extinct. Wilcove, McMilan, and Winston [18] point out that animal species proposed for listing between 1985 and 1991 had a median number of 1000 individuals and 2-3 populations when listed. Plants had a median number of 120 individuals and 4 populations. 39 species of plant had 10 or fewer individuals. This suggests that we are trying to save many endangered species when their populations are already drastically reduced. As of 31 August 2009 (http://ecos.fws.gov/tess_public/TESSBoxscore) • 1320 species in the United States are listed as threatened or endangered, 31 fewer than 2 years ago when I last taught this course. • 89 species are proposed for listing. Only 3 species (all animals: polar bear, coho salmon, gray wolf – distinct population segment) were proposed for listing 2 years ago. • 247 species are candidates for listing, 31 fewer than 2 years ago.10 Of the 1351 species listed as threatened or endangered • Critical habitat has been designated for 544 (58 more than two years ago). • 1135 have approved recovery plans. There are 592 distinct recovery plans, because many recovery plans cover more than one species. It seems intuitively obvious that there are some problems here, but before we can say much about how populations of endangered species should be managed, we need to spend some time discussion the problems of life in small populations, which is what we’ll be doing for the next three weeks, or so. 10
Candidate species – Plants and animals that have been studied and the Service has concluded that they should be proposed for addition to the Federal endangered and threatened species list. These species have formerly been referred to as category 1 candidate species. From the February 28, 1996 Federal Register, page http://endangered.fws.gov/96cnorwt.html: “those species for which the Service has on file sufficient information on biological vulnerability and threat(s) to support issuance of a proposed rule to list but issuance of the proposed rule is precluded.”
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Allocation of benefits to endangered species Before getting to the biology of small populations, though, I wouldn’t be providing the proper perspective on endangered species protection in the United States unless I spent a little more time talking about how the ESA is implemented. Look back at the five factors permitting listing. You’ll see that there’s a lot of room for discretion in interpreting whether or not particular criteria have been fulfilled, especially “inadequacy of existing laws and regulations” and “other natural or man-made factors affecting its continued existence.” Moreover, once a species is on the list, decisions have to be made about how much money to devote to its recovery. It shouldn’t come as a surprise that some species receive much more attention than others. Czech et al. [2] surveyed 2500 people in the United States (receiving 643 responses) and asked them to rank the importance of various broad groups of taxa in importance on a scale of 1-100. They tabulated total state and federal expenditure on endangered or threatened taxa in 1993, and tabulated conservation organizations that were focused on particular taxa (e.g., the New England Wildflower Society or the Connecticut Audubon Society). Surprisingly, the importance that people place on taxa is only loosely related to expenditures on their protection (Figure 2). The explanation is relatively straigthforward: Some taxa are associated with politically motivated and influential human constituencies, e.g., birds, mammals, and fish. They argue that “the consistency with which the eight types of species accrue benefits from the Endangered Species Act as predicted by the socialconstruction/political-power matrix is remarkable” (p. 1111). They present a matrix that describes these two axes of explanation (Figure 3) and argue that “a holistic perspective that accounts for public preference and political reality will be more productive in the policy arena and thus for species conservation” (p. 1109).
References [1] Millenium Ecosystem Assessment. Ecosystems and Human Well-being: Synthesis. Island Press, Washington, DC, 2005. [2] B. Czech, P. R. Krausman, and R. Borkhataria. Social construction, political power, and the allocation of benefits to endangered species. Conservation Biology, 12:1103–1112, 1998. [3] J. W. Fitzpatrick, M. Lammertink, Jr. Luneau, M. D., T. W. Gallagher, B. R. Harrison, G. M. Sparling, K. V. Rosenberg, R. W. Rohrbaugh, E. C. H. Swarthout, P. H. Wrege, S. Barker Swarthout, M. S. Dantzker, R. A. Charif, T. R. Barksdale, Jr. Remsen, J. V., 14
Figure 2: Total federal and state expenditures for endangered or threatened species in eight broad taxonomic groups (from [2].)
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Figure 3: The social-construcion/political-power matrix suggested by Czech et. al [2] as a tool for understanding expenditures on endangered species protection. S. D. Simon, and D. Zollner. Ivory-billed woodpecker (Campephilus principalis) persists in continental north america. Science, 308(5727):1460–1462, 2005. [4] Richard G. Gustafson, Robin S. Waples, James M. Myers, Laurie A. Weitkamp, Gregory J. Bryant, Orlay W. Johnson, and Jeffrey J. Hard. Pacific salmon extinctions: Quantifying lost and remaining diversity. Conservation Biology, 21(4):1009–1020, 2007. [5] R. J. Hobbs and H. A. Mooney. Broadening the extinction debate: population deletions and additions in California and western Australia. Conservation Biology, 12:271–283, 1998. [6] J. R. Karr. Avian extinction on Barro Colorado Island, Panama: a reasssessment. American Naturalist, 119:220–239, 1982. [7] Richard A. Kerr. Paleobiology: Revised numbers quicken the pace of rebound from mass extinctions. Science, 311(5763):931a–, 2006. [8] Peter J. Lu, Motohiro Yogo, and Charles R. Marshall. Phanerozoic marine biodiversity dynamics in light of the incompleteness of the fossil record. Proceedings of the National Academy of Sciences, 103(8):2736–2739, 2006. 10.1073/pnas.0511083103. [9] L. L. Master, B. A. Stein, L. S. Kutner, and G. A. Hammerson. Vanishing assets: conservation status of U.S. species. In Bruce A. Stein, Lynn S. Kutner, and Jonathan S. 16
Adams, editors, Precious Heritage: The Status of Biodiversity in the United States, pages 93–118. Oxford University Press, New York, NY, 2000. [10] Robert M. May, John H. Lawton, and Nigel E. Stork. Assessing extinction rates. In John H. Lawton and Robert M. May, editors, Extinction Rates, pages 1–24. Oxford University Press, New York, NY, 1995. [11] M. L. McKinney and J. L. Lockwood. Biotic homogenizations: a few winners replacing many losers in the next mass extinction. Trends in Ecology & Evolution, 14(11):450–453, 1999. [12] S. J. Pimm and R. A. Askins. Forest losses predict bird extinctions in eastern North America. Proceedings of the National Academy of Sciences USA, 92:9343–9347, 1995. [13] Joe Roman and S. R. Palumbi. Whales before whaling in the north atlantic. Science, 301:508–510, 2003. [14] E. W. Sanderson, M. Jaiteh, M. A. Levy, K. H. Redford, A. V. Wannebo, and G. Woolmer. The human footprint and the last of the wild. BioScience, 52(10):891–904, 2002. [15] Fraser D. M. Smith, Robert M. May, Robin Pellew, Timothy H. Johnson, and Kerry S. Walter. Estimating extinction rates. Nature, 364:494–496, 1993. [16] UNEP. Global Biodiversity Assessment. Cambridge University Press, Cambridge, 1995. [17] G. Vermeij. The biology of human-caused extinction. In Bryan G. Norton, editor, The Preservation of Species: The Value of Biological Diversity, pages 28–49. Princeton University Press, Princeton, NJ, 1986. [18] D. S. Wilcove, M. McMillan, and K. C. Winston. What exactly is an endangered species? an analysis of the u.s. endangered species list: 1985-1991. Conservation Biology, 7(1):87– 93, 1993. [19] D. S. Wilcove, D. Rothstein, J. Dubow, A. Phillips, and E. Losos. Quantifying threats to imperiled species in the United States. BioScience, 48(8):607–616, 1998.
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Or we can choose not to (consciously) manage and hope that things turn out the way we want them to.
c 2003–2009 Kent E. Holsinger
Figure 1: Past, present, and projected extinction rates [1]. To start, let’s take a look at what the Millenium Ecosystem Report has to say about extinction rates (Figure 1). Notice the scale on the vertical axis. It’s a logarithmic scale. So our best guess about the current extinction rate is that it’s 100-1000 times higher than the background extinction rate in the fossil record, and the projected future extinction rate 10-100 times greater than the current rate. Numbers like that are why you often hear it said that we are living through the sixth great mass extinction in the history of life.
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Background extinction It is the fate of most living things eventually to go extinct. The species diversity now is almost certainly greater than it ever has been in the past, but paleontologists tell us that more than 99% of the species that have ever lived are now extinct. Some take comfort that we seem to have recovered from the great extinctions of the past • Ordovician (440mya) — 50% of animal families • Devonian (360mya) — 30% of animal families • Permian (250mya) — 50% of animal families, including 95% of marine species • Triassic (210mya) — 35% of animal families • Cretaceous (65mya) — 60% of animal species We’re still here, these people would argue, and the world doesn’t look so bad. Until recently I argued that the fossil record showed that recovery from these extinctions took a long time.2 But reanalysis of the record of Phanerozoic diversity for marine invertebrates [7, 8] suggests that the apparent delay in recovery is an artifact of the incompleteness of the fossil record. The recovery of biodiversity may, in fact, be geologically instantaneous, i.e., on the order of 5 million years or less. So the optimist in me says that we are very unlikely to destroy life on this planet and that the diversity of life will recover fairly quickly once we are gone. The pessimist in me points out that I don’t want to live in a world that has substantially less diversity than the one I live in now, and that even if life’s diversity recovers instantaneously from the perspective of deep geological time, it’s not like to happen on a time scale of any interest to human beings.3 To me, that means we want to do what we can to reduce the rate of extinction, ideally to a rate 10-100 times lower than it is now.
The causes of extinction The causes of extinction are (mostly) fairly obvious, and we touched on one of the largest ones all ready — habitat destruction and conversion. But let’s spend a little time reminding ourselves what the causes of extinction are, because knowing those causes helps us better to understand their consequences. 2
Ordovician — 25 million years; Devonian — 30 million years; Permian/Triassic — 100 million years; Cretaceous — 20 million years 3 “Humans” didn’t even exist 5 million years ago, if by “human” we mean a member of the genus Homo.
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• Overexploitation Whales – A record three year cruise in the 19th century killed fewer than one hundred whales. – In 1933 almost 30,000 whales were killed, yielding 2.5 million barrels of whale oil. – By 1967 60,000 were killed, but they yielded only 1.5 million barrels of oil — because the larger species, e.g., Blues and Fins, had been hunted virtually to extinction. – Analyses of genetic diversity suggest pre-exploitation population sizes 6-20 times greater than current estimates [13].4 Atlantic cod Wildlife trade, orchids and succulents Predator control — until 1952 the Bald Eagle had a price on its head • Development — urbanization, agriculture, & mining Cape flora – 6,000 species of native vascular plants; 1,200 threatened; 36 are extinct – More than 60% of the area previously occupied by the Cape flora has been replaced by farms, plantations, roads, dams, towns, etc. – More than 80% of the $4 million earned in the cut-flower industry is extracted directly from the wild flora Dams: Pacific northwest salmon fishery has declined dramatically in the last 50 years. Many runs are now listed (or proposed for listing) under the Endangered Species Act. Nearly 30% of the ca. 1400 historical populations are extinct (14% of populations from coastal regions, 55% from interior regions) [4]. Deforestation (Table 1) is just one aspect of habitat conversion, although it is probably among the most extreme. 4 This estimate is very sensitive to estimates of the rate of nucleotide substitution in mitochondria. Roman and Palumbi use estimates of 1.5-2.0 ×10−8 per base pair per year. If the rate were higher, say, 1.5-2.0 ×10−7 per base pair per year, the pre-exploration population sizes would be estimated at 0.6-2 times greater than current estimates.
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Country/Region % of old growth forest USA 15 Washington & Oregon 13 Canada 52 British Columbia 40 Europe Western Europe 1 Scotland 1 Sweden 1 Finland 2 Norway 3 Oceania New Zealand 25 Australia 5–21 Asia China 1 Table 1: Proportion of old-growth forest remaining in selected temperate forest countries (from Table 11.2-6 [16]). • Invasive exotics Zebra mussel Chestnut blight Wilcove, Rothstein, Dubow, Phillips, and Losos [19] surveyed recovery plans for species listed under the United States Endangered Species Act and categorized the threats they identified into one of five categories: habitat degradation/loss, alien species, pollution, overexploitation, and disease. Table 2 shows the percentage of listed species for which each of these five factors was mentioned as a cause contributing to endangerment.5 In short, many species are going extinct for reasons very different from those that caused their extinction in the past. Those causes make it clear that we are responsible for the elevated rates of extinction, but they don’t tell us how many species are going extinct. 5
The numbers add to more than 100% because each species may face threats in more than one category.
5
Cause Habitat degradation Alien species Pollution Overexploitation Disease
All Vertebrates (n = 1880) (n = 494) 85% 92% 49% 47% 24% 46% 17% 27% 3% 11%
Invertebrates (n = 331) 87% 27% 45% 23% 0%
Plants (n = 1055) 81% 57% 7% 10% 1%
Table 2: Causes of endangerment mentioned in species recovery plans [19]. Conservation status Secure/apparently secure Vulnerable Imperiled Critically imperiled Presumed/possibly extinct
Percent of taxa 67% 16% 8% 7% 1%
Table 3: Percentage of species in taxonomically well-characterized taxa falling into different endangerment categories in the United States.
Rates of extinction Rates of extinction are very difficult to estimate, because we don’t even know within an order of magnitude how many species there are. Nonetheless, we can be quite sure that a large proportion of taxa are threatened with extinction. A little less than 10 years ago, The Nature Conservancy [9] assessed the status of 20,892 species in groups that are taxonomically well-characterized in the United States (freshwater mussels, crayfishes, vertebrates, vascular plants, tiger beetles, butterflies/butterflies, and dragonflies/damselflies; Table 3). These statistics don’t tell us how many extinctions are happening. And depending on whether you’re an optimist or a pessimist you can take this as good news or as bad news. Two out of three species in the United States are apparently secure. That’s the good news. One out of three species in the United States is vulnerable or imperiled. That’s the bad news. But how do these numbers compare with what might have characterized the biota of the U.S. prior to the arrival of humans? Do they, in fact, tell us that extinction rates are elevated, or are they simply characteristic of what we would have found at any time in the 6
geological past? Are a large fraction of species on the edge of extinction during most of geological history? Two different approaches have been employed to try to compare current rates of extinction with those inferred from the fossil record.
Species-area relationships Statistics on the rates of extinction have mostly been inferred from a species-area relationship and projections of habitat destruction. S = CAz If we’re only interested in the proportion of species remaining after some portion of the habitat has been destroyed CA0z S0 = S CAz! z A0 = A
(1) (2)
z is generally between 0.15 and 0.35. So for example, if we’re interested in projecting the fraction of species that will be lost from tropical rainforests as a result of deforestation, we can make the following back of the envelope calculation. If current rates of tropical deforestation continue for another 30 years half of the remaining rain forest will be gone. If we then prevent all further deforestation, between 0.50.35 = 0.78 and 0.50.15 = 0.90 of the species presently there will remain, i.e., 10%–20% will go extinct. More sophisticated approaches use an exponential decay model, recognizing that the predictions of the above approach apply only after the remaining forest fragments have reach an immigration-extinction equilibrium. Notice, however, that these calculations only reflect the effects of lost habitat, not increased exposure to disease, competition with invasive exotics, overxploitation, or habitat degradation.
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Rates from known extinctions It may come as a surprise to you to learn that we can also get reasonable estimates of current extinction rates from examining documented extinctions in groups that are reasonably wellstudied. In the United States alone, for example, 45 vertebrates (over half of which are birds), 347 invertebrates, and 147 plants are either presumed or possibly extinct [9].6 By calculating the fraction of known species that have gone extinct in historical times, we get a direct estimate of extinction rates. The calculations that follow are based on the data and the approach described in [10, 15]. • 100 documented extinctions of birds and mammals worldwide in the last century out of ≈ 14, 000 total. That’s a rate of 7 × 10−3 yr−1 . • The average life span of bird and mammal species in the fossil record is about 1 × 106 years. This is equivalent to an extinction rate of about 1 × 10−6 y−1 . • So the recent historical rate of vertebrate extinctions is a little over 7,000 times greater than the background rate of extinction. The rates calculated by these very different approaches are reasonably comparable, given the great uncertainties involved. They suggest that contemporary rates of extinction are 100 to 1,000 (and possibley 10,000) times higher than at any time in the last 65 million years. The figures in Table 4 show how many documented extinctions have occurred in the last 400 years, along with an estimate of the corresponding median lifetime of taxa in each group (derived from [15]).
Critiques of these estimates Critics of estimates based on species-area relationships have pointed out that > 95% of the eastern forests in North America were cut while only 4 bird species went extinct7 . How can we account for this apparent discrepancy [12]? • The region was not simultaneously deforested. As agriculture moved westward, forest reclaimed abandoned fields. Forests always covered > 50% of the land area. 0.50.25 = 0.84 16% or 25-26 out of ≈160 forest species should have gone extinct. 6
We should probably change the vertebrate extinction number to 44, given the apparent rediscovery of the ivory-billed woodpecker [3]. 7 And maybe only 3, if the ivory-billed woodpecker is still extant.
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Animals
Plants
Molluscs Crustaceans Insects Vertebrates Fishes Amphibians Reptiles Birds Mammals Total Gymnosperms Dicotyledons Monocotyledons Palms Total
Extinct Threatened Extant Time to 50% extinction 191 354 105 60,000 4 126 4 × 103 — 6 61 873 10 — 4 229 2,212 4.7 × 10 600 29 452 2.4 × 104 900 3 2 59 3 × 10 3,000 23 167 6 × 103 2,000 3 116 1,029 9.5 × 10 350 3 59 505 4.5 × 10 250 15,000 485 3,565 1.4 × 106 2 242 758 — 5 120 17,474 1.9 × 10 1,000 462 4,421 5.2 × 104 1,700 4 925 2820 70 584 22,137 2.4 × 105 1,100
Table 4: Extinction in major taxa since 1600. • May not have been enough time for extinction. Species-area relationship is an equilibrium expectation. Committed to extinction versus actually extinct • Only 28 of the 160 species are restricted to eastern forests. The rest are widely distributed elsewhere and would have persisted there. They could have later moved back into eastern forests. (0.50.25 )(28) = 23.5
,
i.e., 23-24 of the 28 species should have persisted. Only 4-5 should have gone extinct, which is about what we saw. • We lost few bird species from eastern North American forests because we had few endemics to lose.
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Population deletions We tend to focus on extinction as a species-level phenomenon, but doing so substantially understates the impact we are having. So long as a single population of a species is extant the species is not extinct, even if 99.9% of its populations have been eliminated. Species may be eliminated from most of their former range and persist only in small refuge areas. Over a decade ago, population declines in amphibians began to receive world-wide attention. Hobbs and Mooney [5] cite several similar examples:8 • Yellow-legged frog (Rana muscosa) — 1989 survey found in only 1 of 27 sites where it had been found 10 years before. • Owens pupfish (Cyprinodon radiosus) — Originally widespread in Owens Valley. Once thought extinct. A single population was rediscovered in 1956. • 26 six species of west Australian mammals occur only as remnant populations occupying less than 20% of their original range. 42% of mammals originally found in the wheatbelt region are no longer found there, although only 14% of those are extinct in the entire state. • Half of the bird species in the agricultural part western Australia have declined in distribution and abundance since 1900.
Biological consequences of human-caused extinctions We have now seen that rate at which human-caused extinctions are occurring is different from the rate at which extinction occurred before we became so dominant.9 What are the immediate consequences of such extinctions? Geerat Vermeij [17] suggested three questions to be answered to understand the implications of extinction for human welfare. 1. Which kinds of species are susceptible to extinction, and which are not? 2. How will the extinction of species affect the communities in which these species lived and alter the evolutionary environment of surviving life forms? 3. Can new species evolve on a human-dominated planet to replace the species that have disappeared and, if so, what will they look like? 8
And don’t forget the example of Pacific northwest salmon populations cited earlier [4]. We’ll return to this topic again when we talk about landscape change in a couple of months. There is substantial evidence that human occupation of the Americas and of Australia led to many extinctions among large mammals. 9
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Group Proportion threatened1 Freshwater mussels 69% Crayfishes 51% Stoneflies 43% Freshwater fishes 37% Amphibians 36% Flowering plants 33% Gymnosperms 24% Pteridophytes 22% Tiger beetles 19% Butterflies 19% Reptiles 18% Odanates 18% Mammals 16% Birds 14% 1 Presumed/possibly extinct, critically imperiled, imperiled, or vulnerable Table 5: The taxonomic distribution of endangerment in the United States.
Selectivity of extinctions Vanished species are unlikely to be a random subset of the biota. • Karr (Barro Colorado) — ground-dwelling birds suffered higher rate of extinction than canopy dwellers [6]. • The proportion of species threatened differs dramatically among taxonomic groups in the United States (Table 5; [9]).
Consequences of extinctions If these speculations are correct, human caused extinctions have two properties: 1. They are depleting biological diversity at a rate greater than at any time in the last 65 million years. 2. The species that are going extinct are predominantly those adapted to special conditions of life in localized habitats. 11
The result is a more homogeneous biotic environment, one in which many of the same plants and animals are found worldwide — English sparrows, starlings, dandelions, wild oats. Most of the grasses you see on the hills of California are native to the Mediterranean. Native Californian grasslands are largely confined to serpentine outcrops. Nearly all of the vegetation in lowland areas of Hawaii is introduced from other areas in the tropics. Of the roughly 1,700 plants native to Hawaii, almost half are introduced (see [11] for a more careful analysis of this issue). Whether it is a good thing for the character of our natural world to be changed in this way is something we must decide on non-biological grounds. Life will continue on this planet whatever we decide, but what we decide will have an enormous impact on what kind of life does survive.
U. S. Endangered Species Act A U.S.-based course in conservation biology wouldn’t be complete without a brief introduction to the Endangered Species Act. We won’t go into all of its details, but there are a few important features that anyone finishing this course should be aware of. The Endangered Species Act of 1973 requires the U. S. Fish & Wildife Service (or the National Marine Fisheries Service, for certain marine species) to identify species of wildlife and plants that are endangered or threatened, based on the best available scientific and commercial data. §3(6) The term “endangered species” means any species which is in danger of extinction throughout all or a significant portion of its range other than a species of the Class Insecta determined by the Secretary to constitute a pest whose protection under the provisions of this Act would present an overwhelming and overriding risk to man. §3(19) The term “threatened species” means any species which is likely to become an endangered species within the foreseeable future throughout all or a significant portion of its range. §3(15) The term “species” includes any subspecies of fish or wildlife or plants, and any distinct population segment of any species of vertebrate fisho or wildlife which interbreeds when mature. The act recognizes five factors permitting listing: 1. Present or threatened destruction of habitat, 2. Overutilization for commercial, recreational, scientific, or educational purposes, 3. Losses due to disease or predation, 12
4. Inadequacy of existing laws and regulations to protect the organism in question, and 5. Other natural or man-made factors affecting its continued existence. Notice that rarity and endangerment are not the same thing. “Rarity” means uncommon. “Endangerment” means likely to go extinct. Wilcove, McMilan, and Winston [18] point out that animal species proposed for listing between 1985 and 1991 had a median number of 1000 individuals and 2-3 populations when listed. Plants had a median number of 120 individuals and 4 populations. 39 species of plant had 10 or fewer individuals. This suggests that we are trying to save many endangered species when their populations are already drastically reduced. As of 31 August 2009 (http://ecos.fws.gov/tess_public/TESSBoxscore) • 1320 species in the United States are listed as threatened or endangered, 31 fewer than 2 years ago when I last taught this course. • 89 species are proposed for listing. Only 3 species (all animals: polar bear, coho salmon, gray wolf – distinct population segment) were proposed for listing 2 years ago. • 247 species are candidates for listing, 31 fewer than 2 years ago.10 Of the 1351 species listed as threatened or endangered • Critical habitat has been designated for 544 (58 more than two years ago). • 1135 have approved recovery plans. There are 592 distinct recovery plans, because many recovery plans cover more than one species. It seems intuitively obvious that there are some problems here, but before we can say much about how populations of endangered species should be managed, we need to spend some time discussion the problems of life in small populations, which is what we’ll be doing for the next three weeks, or so. 10
Candidate species – Plants and animals that have been studied and the Service has concluded that they should be proposed for addition to the Federal endangered and threatened species list. These species have formerly been referred to as category 1 candidate species. From the February 28, 1996 Federal Register, page http://endangered.fws.gov/96cnorwt.html: “those species for which the Service has on file sufficient information on biological vulnerability and threat(s) to support issuance of a proposed rule to list but issuance of the proposed rule is precluded.”
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Allocation of benefits to endangered species Before getting to the biology of small populations, though, I wouldn’t be providing the proper perspective on endangered species protection in the United States unless I spent a little more time talking about how the ESA is implemented. Look back at the five factors permitting listing. You’ll see that there’s a lot of room for discretion in interpreting whether or not particular criteria have been fulfilled, especially “inadequacy of existing laws and regulations” and “other natural or man-made factors affecting its continued existence.” Moreover, once a species is on the list, decisions have to be made about how much money to devote to its recovery. It shouldn’t come as a surprise that some species receive much more attention than others. Czech et al. [2] surveyed 2500 people in the United States (receiving 643 responses) and asked them to rank the importance of various broad groups of taxa in importance on a scale of 1-100. They tabulated total state and federal expenditure on endangered or threatened taxa in 1993, and tabulated conservation organizations that were focused on particular taxa (e.g., the New England Wildflower Society or the Connecticut Audubon Society). Surprisingly, the importance that people place on taxa is only loosely related to expenditures on their protection (Figure 2). The explanation is relatively straigthforward: Some taxa are associated with politically motivated and influential human constituencies, e.g., birds, mammals, and fish. They argue that “the consistency with which the eight types of species accrue benefits from the Endangered Species Act as predicted by the socialconstruction/political-power matrix is remarkable” (p. 1111). They present a matrix that describes these two axes of explanation (Figure 3) and argue that “a holistic perspective that accounts for public preference and political reality will be more productive in the policy arena and thus for species conservation” (p. 1109).
References [1] Millenium Ecosystem Assessment. Ecosystems and Human Well-being: Synthesis. Island Press, Washington, DC, 2005. [2] B. Czech, P. R. Krausman, and R. Borkhataria. Social construction, political power, and the allocation of benefits to endangered species. Conservation Biology, 12:1103–1112, 1998. [3] J. W. Fitzpatrick, M. Lammertink, Jr. Luneau, M. D., T. W. Gallagher, B. R. Harrison, G. M. Sparling, K. V. Rosenberg, R. W. Rohrbaugh, E. C. H. Swarthout, P. H. Wrege, S. Barker Swarthout, M. S. Dantzker, R. A. Charif, T. R. Barksdale, Jr. Remsen, J. V., 14
Figure 2: Total federal and state expenditures for endangered or threatened species in eight broad taxonomic groups (from [2].)
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Figure 3: The social-construcion/political-power matrix suggested by Czech et. al [2] as a tool for understanding expenditures on endangered species protection. S. D. Simon, and D. Zollner. Ivory-billed woodpecker (Campephilus principalis) persists in continental north america. Science, 308(5727):1460–1462, 2005. [4] Richard G. Gustafson, Robin S. Waples, James M. Myers, Laurie A. Weitkamp, Gregory J. Bryant, Orlay W. Johnson, and Jeffrey J. Hard. Pacific salmon extinctions: Quantifying lost and remaining diversity. Conservation Biology, 21(4):1009–1020, 2007. [5] R. J. Hobbs and H. A. Mooney. Broadening the extinction debate: population deletions and additions in California and western Australia. Conservation Biology, 12:271–283, 1998. [6] J. R. Karr. Avian extinction on Barro Colorado Island, Panama: a reasssessment. American Naturalist, 119:220–239, 1982. [7] Richard A. Kerr. Paleobiology: Revised numbers quicken the pace of rebound from mass extinctions. Science, 311(5763):931a–, 2006. [8] Peter J. Lu, Motohiro Yogo, and Charles R. Marshall. Phanerozoic marine biodiversity dynamics in light of the incompleteness of the fossil record. Proceedings of the National Academy of Sciences, 103(8):2736–2739, 2006. 10.1073/pnas.0511083103. [9] L. L. Master, B. A. Stein, L. S. Kutner, and G. A. Hammerson. Vanishing assets: conservation status of U.S. species. In Bruce A. Stein, Lynn S. Kutner, and Jonathan S. 16
Adams, editors, Precious Heritage: The Status of Biodiversity in the United States, pages 93–118. Oxford University Press, New York, NY, 2000. [10] Robert M. May, John H. Lawton, and Nigel E. Stork. Assessing extinction rates. In John H. Lawton and Robert M. May, editors, Extinction Rates, pages 1–24. Oxford University Press, New York, NY, 1995. [11] M. L. McKinney and J. L. Lockwood. Biotic homogenizations: a few winners replacing many losers in the next mass extinction. Trends in Ecology & Evolution, 14(11):450–453, 1999. [12] S. J. Pimm and R. A. Askins. Forest losses predict bird extinctions in eastern North America. Proceedings of the National Academy of Sciences USA, 92:9343–9347, 1995. [13] Joe Roman and S. R. Palumbi. Whales before whaling in the north atlantic. Science, 301:508–510, 2003. [14] E. W. Sanderson, M. Jaiteh, M. A. Levy, K. H. Redford, A. V. Wannebo, and G. Woolmer. The human footprint and the last of the wild. BioScience, 52(10):891–904, 2002. [15] Fraser D. M. Smith, Robert M. May, Robin Pellew, Timothy H. Johnson, and Kerry S. Walter. Estimating extinction rates. Nature, 364:494–496, 1993. [16] UNEP. Global Biodiversity Assessment. Cambridge University Press, Cambridge, 1995. [17] G. Vermeij. The biology of human-caused extinction. In Bryan G. Norton, editor, The Preservation of Species: The Value of Biological Diversity, pages 28–49. Princeton University Press, Princeton, NJ, 1986. [18] D. S. Wilcove, M. McMillan, and K. C. Winston. What exactly is an endangered species? an analysis of the u.s. endangered species list: 1985-1991. Conservation Biology, 7(1):87– 93, 1993. [19] D. S. Wilcove, D. Rothstein, J. Dubow, A. Phillips, and E. Losos. Quantifying threats to imperiled species in the United States. BioScience, 48(8):607–616, 1998.
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