The ecology of extinction: population fluctuation and decline in amphibians
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.
Section snippets
Data sets
The data were amassed from published sources as listed in the North American Amphibian Monitoring Program (NAAMP) database and the dataset used by Houlahan et al. (2000), as well as unpublished sources as used also by Houlahan et al. (2000). I only looked at time series of 5 years or greater duration. In cases where the census values were given as densities rather than as counts or estimates of actual animal numbers, I multiplied the density values by the sizes of the areas studied, where
Changes in population size
Among the 617 time-series, there were 4482 census intervals in total. Declines (50.6% of changes) overall outnumbered increases (45.1%), in accordance with the general downward trend detected by Houlahan et al. (2000), however this result is greatly influenced by the preponderance of pond-breeding frogs in the data set. Both the terrestrial direct developers and stream-breeding species exhibited more increases than decreases; their populations increased 48.0 and 49.7% of the time, respectively,
Discussion: population variance and population persistence
Contrary to the expectations of Alford and Richards (1999), the distribution of ΔN values was not consistent with any particular pattern of population rises and declines within populations. Although populations rarely remained precisely the same size, most of the time they changed little from one census to the next. Large increases and large decreases were both rare. Alford and Richards (1999) had predicted that amphibian populations are dominated by few, but large positive ΔN values amidst
Acknowledgements
I am grateful to J. Houlahan for use of the data he and his colleagues have amassed and to B. Schmidt, T.R. Halliday, J. Irwin, J. Houlahan, M. Lannoo, H.B. Shaffer, W. Gibbons, and M.A. Smith for discussions on the topic and/or comments on the manuscript. This work was supported by an NSERC Canada research grant.
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