The ecology of extinction: population fluctuation and decline in amphibians

Abstract

Even among widespread species with high reproductive potentials and significant dispersal abilities, the probability of extinctions should be correlated both with population size variance and with the extent of population isolation. To address how variation in demographic characteristics and habitat requirements may reflect on the comparative risk of species decline, I examined 617 time series of population census data derived from 89 amphibian species using the normalized estimate of the realized rate of increase, ΔN, and its variance. Amphibians are demonstrably in general decline and exhibit a great range of dispersal abilities, demographic characteristics, and population sizes. I compared species according to life-history characteristics and habitat use. Among the populations examined, census declines outnumbered increases yet the average magnitudes for both declines and increases were not demonstrably different, substantiating findings of amphibian decline. This gives no support for the idea that amphibian population sizes are dictated by regimes featuring relatively rare years of high recruitment offset by intervening years of gradual decline such that declines may outnumber increases without negative effect. For any given population size, those populations living in large streams or in ponds had significantly higher variance than did populations of completely terrestrial or other stream-dwelling amphibians. This could not be related to life-history complexity as all the stream-breeding species examined have larvae and all of the wholly terrestrial species have direct development without a larval stage. Variance in ΔN was highest amongst the smallest populations in each comparison group. Estimated local extinction rates averaged 3.1% among pond-breeding frogs, 2.2% for pond-breeding salamanders, and negligible for both stream-breeding and terrestrial direct-developing species. Recoveries slightly exceeded extinctions among European pond-breeding frogs but not among North American pond-breeding frogs. Less common species had greater negative disparities between extinctions and recoveries. Species with highly fluctuating populations and high frequencies of local extinctions living in changeable environments, such pond- and torrent-breeding amphibians, may be especially susceptible to curtailment of dispersal and restriction of habitat.

Introduction

Population decline leading to local or complete extinction of species is explicitly or implicitly the focus of conservation initiatives and conservation research. Population decline can be considered a downward trend in numbers of individuals (Vial and Saylor, 1993) but confirming this in any species with even moderate population fluctuations is problematic. Populations of species with high potentials for increase (r) tend to show fluctuations and should therefore have increased risk of chance extinction at low population sizes (Belovsky, 1987). But, in some cases, fluctuating population sizes are not necessarily tightly coupled with the chance of extinction (Blaustein et al., 1994a, Schoener & Spiller, 1992) and thus it is the interplay of the demographic characteristics of populations with changes in their particular environments, coupled with the interconnectivity of populations over landscapes, that determines how populations will behave and survive (Bolger et al., 1991, Opdam et al., 1993, Hanski, 1998, Marsh & Trenham, 2001). The probability of local extinctions should be correlated both with high variance in population size and with habitat alterations that have severed or attenuated dispersal between local populations (Thrall et al., 2000). Although these effects have been shown in particular cases (Gibbs, 1998, Cooper & Walters, 2002), their generality has not been thoroughly examined.

There is real concern over broad scale declines, for instance, in numbers of amphibians (Houlahan et al., 2000, Alford & Richards, 1999). Investigations into the plight of amphibian populations have been directed towards discerning decreases in numbers of individuals within populations and by documenting possible proximate causes (Blaustein et al., 1994a, Corn, 2000, Kiesecker et al., 2001). Emerging infectious diseases (Cunningham et al., 1996, Lips, 1999, Morell, 1999), parasitic infections (Sessions & Ruth, 1990, Johnsone et al., 1999), ultra-violet radiation (Blaustein et al., 1994b), chemical pollutants (Berrill et al., 1997, Bonin et al., 1997, Harte & Hoffman, 1989), introduced predators (Liss & Larson, 1991, Bradford & Graber, 1993, Morgan & Buttemer, 1996), habitat destruction (Blaustein et al., 1994a, Green, 1997a, Corn, 2000), and climate change (Pounds et al., 1999, Kiesecker et al., 2001) have all been touted as explanations for declines in amphibian populations. Each is plausible, all are likely, but none is mutually exclusive nor apt to be the single underlying cause.

The condundrum is that amphibian declines occur neither everywhere nor among all species. In some amphibians, declines have not been detected (Hairston and Wiley, 1993) and in others, trends cannot be detected at all (Pechmann et al., 1991). Some have argued (Pechmann & Wilbur, 1996, Alford et al., 2001) that declines in amphibian abundances may be more apparent than real. Alford and Richards (1999) proposed a model whereby fluctuating amphibian populations are dictated by the occasional year of high recruitment offset by intervening years in which reproducive success is low. Therefore, population declines could outnumber population increases without indicating overall decline in the population's status. The corollary to this is that the average magnitude of the declines should be less than the average magnitude of the increases. But this particular model may not be general (Houlahan et al., 2001) and, as stated by Alford et al. (2001), more detailed analysis is required.

Understanding the causes of population declines in any group of organisms is likely to be hampered if the ecology of the organisms themselves is insufficiently considered. Amphibians are often depicted as particularly susceptible to the adverse effects of habitat alteration. They are routinely stereotyped as small and damp, and possessing only limited powers of dispersal. It is true that most of the nearly 5000 species of amphibians are small and damp yet they also are abundant, adaptable, and resilient. Amphibians exhibit a great range of dispersing abilities (Marsh and Trenham, 2001) and demographic characteristics (Stebbins and Cohen, 1995). Their populations cannot all be presumed to behave in a similar fashion when confronted with environmental dangers.

Because of the stochasiticity entailed in extinction events, the variance in population change must be accounted for in order to predict susceptibility to decline and population loss. For example, it may be predicted that pond-breeding frogs which disperse widely should have better capacity for maintaining cohesion within metapopulations but, on the other hand, may have more need to do so because they have greatly fluctuating populations. Populations of species with limited dispersal abilities may or may not be more at risk of decline and/or extinction than similarly-sized populations of highly fecund, dispersing species. Is population size variance dependent upon the relative stability of habitats, particularly breeding habitats, or is it correlated with recruitment or fecundity? To address how variation in demographic characteristics and habitat requirements may reflect on the comparative risk of decline in amphibians, and to comprehend the relative degrees of variance among changes in amphibian population sizes, I examined 617 time series of population census data derived from 89 amphibian species, largely from North America and Europe. I considered if species with expected high intrinsic rates of increase, notably those pond-breeding amphibian species with biphasic life-histories and the highest fecundities, have more highly fluctuating populations and higher rates of local extinctions. Specifically I predicted that populations of direct-developing species in stable terrestrial habitats would exhibit decreased population variance relative to pond-breeding amphibians subject to greater demographic and environmental stochasticity.