Causes of extinction in island birds

Oceanic island bird assemblages have suffered a major extinction episode following human arrival (Steadman, 1995, 2006). Some of our recent work has been aimed at understanding why bird assemblages that have persisted relatively unchanged for long periods suddenly lost a large proportion of their species following human settlement, why those extinctions have been concentrated in certain groups (e.g. species that are more highly endemic to islands have a disproportionately higher rate of extinction) and why some islands have lost more species than others. Our results, and the results of other studies, implicate human hunting and the introduction of exotic mammalian predators as a primary cause of avian extinctions on islands (Atkinson, 1985, 1989; Milberg & Tyrberg, 1993; Paulay, 1994; Holdaway, 1999; Duncan, Blackburn & Worthy, 2002; Roff & Roff, 2003; Blackburn et al., 2004, 2005; Duncan & Blackburn, 2004). Human hunting, coupled with the introduction of different suites of predators during different episodes of human settlement, can account for temporal patterns in the loss of avian species, can explain why losses are concentrated in certain groups (in particular why more highly endemic island species are more prone to extinction) and can account for variation in the proportion of species that have been lost from different islands. Jamieson (2007) identifies an apparent opposition between the conclusions of our studies and those of population geneticists (notably Richard Frankham and colleagues). These workers emphasize the role of inbreeding and other genetic effects as important contributors to extinction in island species (e.g. Frankham, 1998, 2005; O'Grady et al., 2006), while we have ignored it. We agree with Jamieson that these approaches are different, although we do not view our work as being in opposition to that of population geneticists. Ecologists have long recognized a distinction between the processes that drive a species to low numbers (ultimate causes, or the declining population paradigm) and those that deliver the coup de grâce to those small populations (proximate causes or the small population paradigm) (Simberloff, 1986; Caughley, 1994; Lawton, 1995). As Jamieson highlights, we have been primarily interested in the former, whereas inbreeding and other genetic effects that may contribute to small population failure are especially relevant to the latter. We argue that such genetic effects cannot be implicated as the ultimate cause of island bird population declines because island bird assemblages had very low rates of extinction before human arrival (Steadman, 1995, 2006; Worthy & Holdaway, 2002) regardless of how inbred they were. In this respect, our view coincides with the recent position taken by population geneticists. Spielman, Brook & Frankham (2004), arguing for the importance of genetic factors in species extinctions, began by stating that 'species population sizes are reduced by habitat loss, overexploitation, impact of introduced species, and pollution until they reach a point where stochastic factors [including the genetic effects they are interested in] further elevate extinction risk'. Here, the ultimate (habitat loss, overexploitation, impact of introduced species, pollution) and proximate (stochastic factors) causes of extinction need not be competing paradigms. Each provides complementary insights into the causes of extinction, albeit within a different context and framework of processes (Hedrick et al., 1996). That said, there are two patterns to island extinctions where genetic factors could be argued to play a wider role. The first is that extinction rates tend to be higher on smaller islands, a pattern that holds for birds having accounted for the influence of predator introductions (Blackburn et al., 2004). Smaller islands will tend to support smaller populations that are more prone to inbreeding, and such inbred populations may be more susceptible to impacts such as predation or habitat loss, leading to the elevated extinction rates observed on smaller islands. The difficulty here is that several other effects are predicted to elevate extinction rates in small populations on small islands, including demographic stochasticity, Allee effects and the likelihood that predators will be able to find and remove every individual. Second, Frankham (1998) argues that species endemic to islands should be more inbred than non-endemic species, and hence may suffer a higher extinction risk as a result. In common with other studies (McDowall, 1969; Temple, 1986), we have found higher extinction rates in endemic relative to non-endemic island bird species (Blackburn et al., 2004), and that, for New Zealand, extinction rate is positively correlated with the taxonomic level at which a bird species is endemic (Duncan & Blackburn, 2004). Again, however, factors other than the level of inbreeding correlate with level of endemism and can account for these extinction patterns. In New Zealand, more highly endemic species tend to possess traits that increase their susceptibility to human hunting (larger body mass) and the impact of exotic predators (lack of mammalian predator escape responses including loss of flight and predator naivety). For prehistoric bird extinctions in New Zealand, we can clearly demonstrate a link between elevated extinction rates in more highly endemic clades and the pattern of human hunting. Analysis of sub-fossil deposits from Marfells Beach, South Island, shows that humans preferentially hunted larger-bodied species (which characterize more highly endemic clades; Duncan & Blackburn, 2004) and that these species were in turn more likely to become extinct (Duncan et al., 2002). Our explanations for the above patterns have focused on the importance of hunting and predator introductions because of their primary role in causing island bird extinctions, and because, in some cases, we have strong evidence linking the patterns to these processes. This does not exclude the possibility that other factors, including habitat loss, disease, demographic stochasticity, genetic and Allee effects, may have played contributing roles and could have compounded the effects of predators (see Holdaway & Jacomb, 2000; Duncan et al., 2002), or that different factors may be important in driving extinctions in other taxa. We agree with Jamieson, however, that the impacts of human settlement and predator introductions on island birds probably occurred quite rapidly and were sufficiently large to overwhelm any differences among populations arising from inbreeding effects. Such effects may nevertheless become important in small isolated populations that, by good luck or heroic conservation efforts, have persisted by being isolated from the ultimate drivers of extinction, often on islands that are predator free (e.g. Hale & Briskie, 2007). Thanks are due to Guy Cowlishaw for inviting us to write this commentary, and Phill Cassey for comments.