followed human colonization (Diamond 1984a,b; Milberg and Tyrberg, 1993; Pimm et al.,. 1994). The wave of colonists spread eastwards from the east Indies, ...
Biodiversity and Conservation 5, 1059-1067 (1996)
Lessons from a kill STUART L. PIMM Department of Ecology and Evolutionary Biology, The University of Tennessee, Knoxville, TN 37996, USA Received 1 August 1995; revised and accepted 20 March 1996
During their colonization by Polynesians and later by Europeans, the Hawaiian islands suffered a massive loss of species. All the extinctions are indirectly attributable to human impact. Nonetheless, it has proved extremely difficult to specify which of several possible mechanisms caused each particular extinction. This seems to admit defeat in the battle to understand past extinctions. Such understanding could guide our efforts to protect species that are now threatened with extinction. Will it be easier to understand the causes of future extinctions? Surveys of future extinctions stress habitat destruction as the simple and dominant mechanism. This contrasts to its secondary (and generally confused) role in past extinctions. I argue that this contrast between the complexity of the past and the apparent simplicity of the future arises because extinction mechanisms are inherently synergistic. Once extensive species losses begin, it may be impossible to separate the mechanisms and thus manage an individual species as if its decline had a single cause. Keywords: extinction; Hawai'i; synergisms.
Introduction For most managers of biodiversity, the massive loss of species is a future nightmare they hope to avoid by inspired decisions. Yet for those working on Pacific islands, massive losses are both recent history and today's news. The Hawaiian islands have lost > 90% of their bird species, and all well-known taxa have suffered large losses. Many species that do survive persist in only very small numbers. What general lessons can we learn about the probable features of massive extinction elsewhere from this case history? I first review the ecological history of the Hawaiian islands and the consequences of their discovery by Polynesians and Europeans. Massive species loss followed both colonizations, and they continue to this day. It is difficult to ascribe particular mechanisms to these human-caused extinctions, yet we must understand them if we are to prevent future extinctions. Understanding current mechanisms of endangerment is also difficult. I will interpret these difficulties as a result of the unexpected discontinuities and synergisms that are the topic of this special issue.
The Hawaiian islands: a history of ecological disaster The Pacific islands faunas and floras are well-known for the high extinction rates that followed human colonization (Diamond 1984a,b; Milberg and Tyrberg, 1993; Pimm et al., 1994). The wave of colonists spread eastwards from the east Indies, reaching Melanesia and Micronesia about 4000 years ago, Fiji and Samoa 3500 years ago, the Marquesas 2000 years ago, and the outliers of Hawai'i, Easter Island, and New Zealand within the last 2000 years (Kirch, 1994). European exploration started with Magellan and Mendafia in the 16th century and was all but complete when Cook died at Kealakekua, Hawai'i, in 1779. The 0960-3115 © 1996 Chapman & Hall
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first missionaries arrived in the Hawaiian islands in 1820; over 100 whaling ships were off Lahaina, Maul, by 1824 (Daws, 1968). Across the Pacific, the bones of many bird species persist into, but not through, archaeological zones showing human presence. No species disappeared in the longer intervals before first contact (Steadman, 1995). The larger Hawaiian Islands (Kaua'i, O'ahu, Moloka'i, Maui, Lana'i and Hawai'i) are young, shield volcanoes in various stages of erosion. The remains of birds in caves in lava tubes (and other such places) provide an unusually detailed record of the islands' faunas (Olson and James, 1982, 1991; James and Olson, 1991). We know 43 species only from their bones. Yet bird bones are fragile and easily destroyed. We may never find bones of all the now-extinct species, so how many are missing? The bone record would be complete only if all the recent species - those collected or seen in the last two centuries - were also found as bones. Simply, the proportion of recent species also found as bones estimates how complete is the sample of species found only as bones. Across the Hawaiian islands, we estimate that there are about 40 species missing from the record (Pimm et al., 1994). Add this number to the 43 known extinctions and the body count rises to 83. The Hawaiian islands were not alone in their fate. As they spread across the Pacific, the Polynesians, using only Stone-age technology, eliminated - 1 5 % of the planet's bird species (Steadman, 1995). This fact is a compelling rejoinder to those who doubt our species' ability to cause future mass extinctions (Pimm et al., 1995). Our only records of another 18 species of birds are the specimens collected by 19th century naturalists. We know they missed some species. On Moloka'i, for example, early naturalists heard a rail but never collected it. We will never know whether it was the same species as one known only from bones. The body count rises to at least 101. What remains today? A dozen species are so rare that there is little hope of saving them. A further dozen we can find, but in numbers so small that their future survival is uncertain. Of an estimated 136 species, only 11 survive in numbers that suggest a confident future (Pimm et al., 1994). How Hawai'i acquired an introduced avifauna larger than any other area is a story we have told before (Moulton and Lockwood, 1992; Moulton and Pimm, 1985, 1987). Originally, all the passerine birds were endemic. Currently, only about one-third of the passerine birds are endemic. Almost all the birds (species and individuals) seen below 1000 m are now alien. We do not know the islands' other plants and animals as well as birds, but they appear to share a similar fate. Of 980 native Hawaiian plants, 84 are extinct and 133 have wild populations of < 100 individuals (Sohmer, 1994). Across the Hawaiian islands, a predatory snail, EugIandina rosea, introduced to control another introduced snail, Achatinafulica, ate to extinction hundreds of taxa of native Achatinella land snails (Hadfield, 1986; World Conservation Monitoring Centre, 1992). (I use the term 'taxa' to include recognized geographically distinct populations. Taxonomic uncertainties often raise and sink their specific status. For those that are now extinct we may never resolve the issue.) Birds, plants, and land snails are eminently collectable; for this reason alone, we have known their fate from the time of European colonization. We have much less knowledge about groups not so favoured by Victorian naturalists, and, of course, only birds have left us such convenient fossils.
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What caused the extinctions? What were the precise mechanisms behind these extinctions? I will consider three periods of extinction: the many Polynesian extinctions, an extinction a century ago, and a species that only just survives. Polynesian extinctions Habitat destruction is a leading candidate, but it is not easy to determine how extensive it was. The Hawaiian population seems to have been at least 300 000 spread across a total island area of - 1 7 000 km 2 (Kirch, 1994, p. 346.) Not all this area is vegetated: large amounts of the islands of Maui and Hawai'i are sparsely-vegetated, recent lava flows. Elsewhere, pondfield irrigation for taro cultivation was restricted to the few areas of lowlands and the short valleys close to the ocean. Intensive dryland fields were more extensive inland on the islands of Maui and Hawai'i (Kirch, 1994, p. 252). In more modern times, < 10% of the land area has been cultivated for sugar cane (Moulton and Pimm, 1985), and many areas above 1000 m are cold, very wet and rugged places that do not support agriculture. Even today, large forest reserves remain on Kaua'i, Mani, Moloka'i and Hawai'i (Scott et aI., 1986). I have not found it easy to combine these observations into an estimate of how much of the islands' forests were left intact. Nonetheless, I think that a safe estimate is that at least half the islands' native habitats remained. Should the destruction of half the islands' habitat been sufficient to cause all the extinctions? The relationship that equates a habitat's size, A, to the number of species, S, it houses is S = cA z, where c and z are constants. This relationship suggests that, following habitat loss, the proportional loss of species should equal the proportional loss of area raised to the power z. The observed values of z are small ( < 1), meaning that with decreasing habitat area one loses species more slowly. With a widely accepted value of z = 0.25, a 50% loss of habitat would suggest only a 15% loss of species - an estimate calibrated by the historical loss of bird species in eastern North America (Pimm and Askins, 1995). Even choosing a high value of z = 0.6, following a 50% loss of habitat, the Hawaiian islands should not have lost only 35% of their species. The figure for Polynesian extinctions alone, (83/136 = 61%), is nearly twice that. One can explain the discrepancy by supposing that many of the now-extinct species were restricted to lowland or dry forests, habitats that may have been totally cleared. I think it is more likely that there were many causes of extinction other than the loss of habitat. The Polynesians brought pigs and rats with them. The latter may have eaten groundnesting birds to extinction. The former may have eaten vulnerable plants to extinction, species on which some birds depended for food. Many of the extinct birds were flightless and would have been perfect accompaniments to poi - the staple made from taro root. Other species were hunted for their feathers (see below). The Galapagos islands are well known for their tame birds: the islands are exceptional in not having been discovered by the Polynesians. Had the Hawaiian birds been tame they would have been easy victims of both the Polynesians and their introduced predators. It is easy to imagine how extinctions could have happened but impossible to separate the mechanisms.
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The Kona finch
Grant (1995) has commemorated the centenary of the loss of Kona finch in - 1895 with a detailed discussion of the possible causes. The species was not known to the native Hawaiians (it has no Hawaiian name) and so was not hunted by them, and it probably did not occur at low elevations where it would have been familiar. Grant first discusses habitat loss. Against this explanation is the observation that the species, and others in its upland forest habitat, declined very rapidly, perhaps more rapidly than the loss of habitat. Another explanation is the inbreeding and the demographic risks unavoidable in small populations. The difficulty here is that the explanation begs the question of why the species became rare in the first place. The cause could have been diseases such as pox, brought in with poultry, and avian malaria. However, the latter probably arrived too late to be a factor for this species. Finally, there are introduced predators, including cats, rats and mongooses. No single cause emerges as a clear favourite for the species' rapid decline to extinction. The 'alala
Even more recently, the National Research Council assembled a committee to consider the decline of the 'alala and ways to reverse it (National Research Council, 1992). Unlike the demise of other species, we know the final stages of this decline in some detail. Exactly the same set of factors were considered as those mentioned for the Kona finch with exactly the same result. This forest crow declined continuously for several decades despite what appeared to be extensive upland habitat. In the later stages of decline, nesting success was typical of other species of crows, the survivorship until breeding was excellent, but breeding-age birds died in unusual numbers. A probable explanation was the persecution of nesting birds on all but the one small area where the birds survived. The NRC committee thought such persecution an unlikely explanation for the initial decline towards extreme rarity. Even with modern data and the ability to study its current predicament, the NRC committee did not provide clear answers as to why the species declined in the first place. SINGLE FACTOR OR MULTI-FACTOR EXPLANATIONS? There are two hypotheses for the multiplicity of explanations for these declines. The first is that each decline had a single cause, but without adequate data we cannot discern it. There is one excellent example of this possibility: the extinction of the land birds on Guam, an island in the western Pacific. We now accept that the cause of these extinctions was the introduction of a bird predator, the brown tree snake. Julie Savidge's efforts to make this case and defend it against rival explanations makes a fascinating story that Jaffe (1994) has told well. Only with hindsight, and only because Savidge caught the snake in the act of causing so many extinctions, do we see this story as a clear and simple one. It was not so to ecologists at the time. The second hypothesis is that the declines were the consequence of several factors that operated synergistically. Under this hypothesis, no single-factor explanation would emerge as the explanation of choice. How plausible is this hypothesis? THE INTERACTION BETWEEN HABITAT LOSS AND INTRODUCED SPECIES An interaction between habitat loss and losses from introduced species accepts that such species do harm, then posits that habitat loss inevitably increases their opportunities to do
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so. There are two parts to the argument. First, forest clearing created fragmented communities surrounded by highly modified and often species-poor communities that will be readily invaded by introduced species as a consequence. In the Hawaiian islands, the lowland areas where such introductions are the only species present were easy to invade when few species were present. As the communities gained more species through introductions, the chance that a new introduction would succeed declined progressively (Moulton and Pimm, 1985). The detailed patterns of which species succeeded and which failed strongly implicates interspecific competition as the mechanism behind this (Moulton and Pimm, 1987). The other part of the argument is that once a diverse community of introduced species surrounds the fragments of native habitat it will contain species with the potential to harm the native species within. There are at least two ways in which this might happen. The first is the well-known edge effects, of which the work of Robinson et al. (1995) on cowbirds in eastern North America is a well-documented example. Predators (or brood parasites like cowbirds) forage in open habitats but stray some distance into the forest. Individuals near edges (or in such small fragments that entire native habitat is near an edge) will suffer high mortality. Deforestation often produces fragments of high fractal dimension, that is, where most of the remaining forest is near an edge (Skole and Tucker, 1993). The other part of the argument involves the extent to which introduced species make their home within the native habitat (as opposed to the 'just-visiting' argument of the previous paragraph). Some introduced predators, such as rats and mongooses, occur throughout the Hawaiian forests. So, too, do the introduced birds that may act as competitors, vectors of diseases, or even predators. Within each island, the native forests are the doughnut holes in a surround of lower, disturbed habitats where introduced species totally dominate. Since these volcanic islands are conical in shape, the inner forests are also higher. The proportion of individual native birds encountered increases continuously as one moves inland (and so upwards) from the lowland communities (Scott et al., 1986). Other things being equal, the more native species there are in a given forest, the greater the percentage of native individuals one encounters in that forest. (Those 'other things' are elevation, island and forest type.) Whether the presence of more native species is the cause of fewer introduced individuals or the result of them is impossible to decide, of course. Whatever the precise mechanisms, habitat clearing has allowed native and introduced faunas to mix. This allows the latter to harm the former in the various hard-to-determine ways already mentioned. DECLINES AND THE INCREASE IN HUNTING PRESSURE The extermination of large, flightless, good-to-eat birds is understandable, but even small, mobile species may have been hunted to extinction. The feather capes of the Hawaiian nobility and the kalihi - ceremonial feather maces - contain many thousands of bird feathers (Rose et al., 1993). Some of these species, such as the 'o'u and the four species of 'o'o, are now extinct. The impact of hunting on these species may be hard to judge. I have long pondered the sheer number of feathers in these cultural artefacts as I have waited patiently beside my mist-nets. This 20th century bird-catching technology rarely produces better than one individual per hour per net in the islands' upland forests. Collecting feathers must have been a very time-consuming task; it is not surprising that these artefacts were of considerable value.
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Perhaps the native hunters knew the location of bird roosts: birds would be much easier to catch in numbers there. I have seen thousands of i'iwi on their way to such places; this species supplies the orange-red feathers of the capes. Roosts would be easy but vulnerable targets, simply because the birds are so concentrated. Moreover, individual roosts would be increasingly vulnerable as habitat losses concentrated the birds into a small number of them. The ecologist's intuition that predation declines when prey become scarce need not apply when economic considerations are at stake. As a species became rarer, the increased value of the feathers may have stepped up the pressure to hunt it even more zealously. The reduction in numbers from habitat loss or introduced species may have made the species more likely to succumb from hunting. SECONDARY EXTINCTIONS Once one species becomes extinct, there may be an avalanche of other extinctions. Food web theory suggests that the patterns of secondary extinction may be quite complicated and thus difficult to demonstrate (Pimm, 1991). The most easily recognizable secondary extinctions should be seen in species that depend closely upon each other. In the Hawaiian islands, anecdotal evidence for secondary extinctions comes from considering nectarfeeding birds. There are three nectar-feeding honeycreepers (Drepanidids) - the mamo, black mamo and i'iwi - with long, de-curved beaks, the kind adapted to inserting into appropriately long, de-curved flowers (Smith et al., 1995). The first two birds are extinct, the third has become extinct on two islands, is very rare on a third, and has declined on others. These extinctions may have followed the destruction of important, nectar-producing plants by introduced goats and pigs. Many of the native lobeliods (such as the genera Trematolobellia and Clermontia) have clearly evolved to be pollinated by the three Drepanidids, and the plants were once important components of the forest's understory. The extinction rate of lobeliods (25%; Wagner et al., 1990) clearly exceeds those for the rest of the flora, perhaps because they were so vulnerable to introduced mammalian herbivores. I am not certain whether the plants went first and their bird pollinators followed, or vice versa. Stories of secondary extinctions are nearly always such unsatisfactory anecdotes. The stories are sufficiently plausible for us to pay particular attention to the future consequences of contemporary extinctions.
Consequences Nearly two decades of experience of working with Hawaiian birds - and with excellent teams who study and manage them - suggest that there are no clear stories of cause and effect for the declines of the Hawaiian birds, past or present. The mish-mash of confusing, inter-related factors is operationally frustrating. Yet it is exactly what one would expect if the extinctions were the result of synergistic interactions between multiple factors. One cannot disentangle habitat loss, hunting, introduced species and secondary extinction; they are linked too intricately. Habitat loss is a direct cause of species extinction, but, plausibly, may also facilitate the invasion of alien species that, in turn, cause further extinctions. Rarity, however caused, need be no protection against hunting. In the case of culturally
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valuable artefacts, rarity might increase the pressure to hunt. Extinctions, whatever their cause, may also cause secondary extinctions. Two consequences follow if my interpretation of Hawaiian extinctions is correct. The first is strategic: we are making a serious error when we predict the future rates of extinction from those already threatened (Pimm et al., 1995). Assume that the threatened species of today will be tomorrow's extinctions. Then the predicted nature of future extinctions - overwhelmingly caused by habitat loss - is strikingly different from recent extinctions brought about by a complex set of factors of which habitat loss is not the leading candidate. For birds - the one group for which we have detailed lists of the causes of the threats to their survival - limited habitat is the most frequently cited factor, implicated in - 7 5 % of the - 1 1 0 0 threatened species (Collar et al., 1994). Interestingly, accidentally or deliberately introduced species are blamed for only 6% of currently threatened birds (Collar et al., 1994). This predominance of habitat loss as a cause of future extinction is not consistent with the experience of the Hawaiian past. Islands have contributed the most to recent extinctions, and islands floras and faunas may be unusually vulnerable to the complex set of factors that I have discussed. Islands may not be the best models of future extinctions, predicted to be mostly continental. I disagree with this statement. It is concentrations of restricted-range species ('endemics') that best predict patterns of extinction and endangerment (Pimm et al., 1995). Islands have such concentrations, but so do many continental areas (Myers, 1988, 1990). Case histories of continental extinction 'black spots' - as diverse as plants in the fynbos of South Africa, mussels and clams in the Mississippi drainage, and mammals in the arid interior of Australia - contain the same list of inter-related causes as Hawai'i (Pimm et aI., 1995). To the extent that any one cause of extinction predominates in the literature on recent extinction, the cause is that of introduced species and not habitat destruction (Nott et al., 1995). Simply, the causes of future extinctions are thought to differ from those of past extinctions. I see no reason why they should. Consider this thought experiment. Suppose that, by 2050, we have managed to preserve 5% of the world's tropical forests. Are not the species that remain in these small habitat islands likely to suffer the fate of those in the Hawaiian islands and for the same reasons? The consequences of synergisms is that once the rot begins, extinctions should be fast, furious, multifactorial, and in greater numbers than predicted from habitat destruction alone. The tactical consequence of these arguments is that those who work with the endangered species in the habit fragments that remain 50 years from now may have no more luck in disentangling the causes of particular extinctions than our generation has. Yet if we cannot identify simple causes of a species' decline, how can we prevent it?
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