Human-induced habitat loss and fragmentation continue at an alarming pace and threaten the survival of wildlife species world-wide and particularly in tropical regions (Wade et al. 2003). Identifying which species traits are advantageous in the face of habitat alterations, and why, is an important prerequisite for the development of effective conservation strategies to minimize future biodiversity losses (Laurance 1991; Kotiaho et al. 2005) and hence has become a pressing need for conservation biologists. Extinction proneness depends on the spatial and temporal scale of the study (Henle et al. 2004) and varies widely among taxa (Davies, Margules & Lawrence 2000; Purvis et al. 2000; Jones, Purvis & Gittleman 2003). Moreover, empirical evidence suggests differential sensitivities of species to habitat fragmentation (Laurance 1991; Swihart et al. 2003b; dos Anjos 2006).
Even though a wealth of factors has been linked to increased vulnerability to extinction on theoretical grounds, a recent review by Henle et al. (2004) suggests that only a limited suite of traits including small population size, high population fluctuations, rarity in the form of low abundance and a high degree of habitat specialization have good empirical support as strong general predictors of species’ sensitivity. Other traits that are hypothesized commonly to increase a species’ susceptibility to fragmentation are large body size, low mobility, high trophic level and low matrix tolerance (e.g. Laurance 1991; Purvis et al. 2000; Tscharntke et al. 2002; Ewers & Didham 2006). However, the relative importance of these traits is much less clear, as analyses are often confounded by a high degree of collinearity or synergistic interactions among traits (Davies, Margules & Lawrence 2004; Henle et al. 2004).
Bats are well-suited for evaluating sensitivity to habitat fragmentation, as they are mobile animals with the potential to readily move over extensive areas of fragmented landscapes. At the same time, they are ecologically highly diverse, suggesting differential vulnerability contingent upon species-specific ecological traits (Medellín, Equihua & Amin 2000). Because of their diversity and high abundance, bats are important components of tropical faunas where they fulfil crucial roles as pollinators, seed dispersers and arthropod predators (Kalko 1998; Patterson, Willig & Stevens 2003).
Analyses of correlates of extinction risk in bats have been restricted largely to large spatial scales (global, continental) and, to our knowledge, no study has examined in detail differential vulnerability of bats in the context of habitat fragmentation. Jones et al. (2003) identified small geographical ranges and low wing aspect ratio as significant global correlates of extinction proneness in bats. Safi & Kerth (2004), focusing on temperate-zone bats, found similarly that wing morphology as a measure of habitat specialization in bats is correlated with extinction risk, whereas dietary specialization was unrelated to extinction vulnerability. While these studies provide important insights into elucidating general endangering traits, they may be too broad in scope to be of practical use for species conservation (Fisher & Owens 2004). Here we present a quantitative assessment of trait-mediated differences in species responses of Neotropical bats to small-scale habitat fragmentation and discuss how determinants of extinction vulnerability compare to those identified by Jones et al. (2003) and Safi & Kerth (2004).
We used data on species prevalence and abundance collected in a 2-year study on 23 species of bats in a fragmented landscape of small land-bridge islands in Gatún Lake, Panama. We selected a priori nine well-defined and commonly used ecological characteristics and taxon-specific traits to explore their significance as potential predictors of species vulnerability to fragmentation:
- 1Natural abundance. Based on theory and empirical evidence, species that occur naturally at low abundance should be more susceptible to fragmentation due to an increased risk of stochastic extinction (Davies et al. 2000; Henle et al. 2004).
- 2Body size. Larger species are often attributed a higher extinction risk than small-bodied ones as they tend to have smaller populations, slower life histories and larger home ranges because of greater energy requirements (Purvis et al. 2000; Tscharntke et al. 2002). In line with this reasoning, we hypothesized larger species to be more vulnerable to fragmentation.
- 3Edge-sensitivity. The proportion of habitat edges increases with fragmentation and studies have shown differential responses of species to a range of edge-effects (Harper et al. 2005; Ewers & Didham 2006). Long-term persistence in fragmented landscapes requires individuals to cross habitat boundaries regularly and disperse between remnant patches. We therefore predicted edge-avoiding species which depend on the core habitat of forests to exhibit higher fragmentation sensitivity.
- 4Trophic level. Theory predicts that species at the top of food chains are more extinction-prone than those at lower trophic levels due to more unstable population dynamics (Henle et al. 2004). We hence expected animalivorous bats to be affected more negatively by fragmentation than phytophagous species.
- 5Dietary specialization. Dietary specialists are thought to be more extinction-prone, as they should become more susceptible to an increased variation in the availability of particular food resources as a consequence of fragmentation. Higher diversity of available resources and degree of specialization may lead to an increased importance of this trait for tropical compared to temperate-zone bats (cf. Safi & Kerth 2004).
- 6Vertical stratification. Bat species which forage mainly in the canopy and depend mainly on patchily distributed resources should also be more mobile and hence be less fragmentation-sensitive than species with limited mobility, such as understory bats, which forage primarily on spatio-temporally predictable but often more locally restricted food resources (Kalko 1998; Bernard 2001; Kalko & Handley 2001). Additionally, we expected generalists that use all forest strata opportunistically to be least fragmentation-sensitive because they are likely to adjust quickly to alterations in forest structure.
- 7Mobility. We test the prediction that species with high mobility are more likely to persist in fragmented landscapes than less mobile species (Henle et al. 2004; Ewers & Didham 2006).
- 8Wing morphology. In bats, wing morphology has been shown to be an important predictor of many ecological characteristics including foraging habitat, foraging strategy, dispersal ability and home range size (Norberg & Rayner 1987; Arita & Fenton 1997). Bats characterized by high wing loading and long and narrow wings (high aspect ratio) are fast and energy-efficient flyers, while those with shorter and broader wings have higher manoeuverability in cluttered habitats but increased costs for commuting over longer distances (Norberg & Rayner 1987). Wing morphology may hence limit movements in fragmented landscapes and we expected fragmentation sensitivity to be related negatively to wing loading and aspect ratio.
- 9Ecologically scaled landscape indices (ESLIs). Species persistence in fragmented landscapes may also depend upon interactions between ecological and landscape attributes influencing patterns of species occurrence and abundance (Vos et al. 2001). ESLIs are measures which link explicitly ecologically relevant characteristics of species, such as mobility to landscape structure, and hence provide a more sound alternative to general landscape indices (Vos et al. 2001; Swihart & Verboom 2004).