Habitat fragmentation reduces genetic diversity and connectivity among toad populations in the Brazilian Atlantic Coastal Forest

Habitat fragmentation reduces genetic diversity and connectivity among toad

populations in the Brazilian Atlantic Coastal Forest

Marianna Dixo a,b,*, Jean Paul Metzger a, João S. Morgante b, Kelly R. Zamudio c

a Department of Ecology, University of São Paulo. Rua do Matão, Travessa 14, 321, Caixa Postal 11461, CEP 05508-090 São Paulo, SP, Brazil

b Department of Genetics and Evolutionary Biology, University of São Paulo. Rua do Matão, 277, CP 11461, CEP 05422-970 São Paulo, SP, Brazil

c Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, 14853-2701, USA

Abstract

Tropical rainforests are becoming increasingly fragmented and understanding the genetic consequences of fragmentation is crucial for conservation of their flora and fauna. We examined populations of the toad Rhinella ornata, a species endemic to Atlantic Coastal Forest in Brazil, and compared genetic diversity among small and medium forest fragments that were either isolated or connected to large forest areas by corridors. Genetic differentiation, as measured by FST, was not related to geographic distance among study sites and the size of the fragments did not significantly alter patterns of genetic connectivity. However, population genetic diversity was positively related to fragment size, thus haplotype diversity was lowest in the smallest fragments, likely due to decreases in population sizes. Spatial analyses of genetic discontinuities among groups of populations showed a higher proportion of barriers to gene flow among small and medium fragments than between populations in continuous forest. Our results underscore that even species with relatively high dispersal capacities may, over time, suffer the negative genetic effects of fragmentation, possibly leading to reduced fitness of population and cases of localized extinction. _ 2008 Elsevier Ltd. All rights reserved.

1. Introduction

Fragmentation of natural habitats is a major challenge in conservation biology and one of the top threats to biodiversity (Hanski, 1999; Fahrig, 2003; Henle et al., 2004). The negative effects of fragmentation result from the decrease in overall habitat availability and changes in spatial configuration and habitat quality of fragments (Fahrig, 2003; Ezard and Travis, 2006). Both theoretical and empirical studies show that habitat fragmentation can erode neutral and adaptive genetic diversity of populations due to decreases in effective population size and inter-population connectivity (Johansson et al., 2007). After fragmentation, small populations, and lower genetic diversity lead to genetic drift, higher risks of inbreeding, lower evolutionary potential, and consequently, higher risk of extinction (Avise et al., 1987; Young et al., 1996; Saccheri et al., 1998; Reed and Frankham, 2003). The maintenance of semi-natural levels of habitat connectivity via habitat corridors has been proposed as a means of reducing the negative effects of fragmentation (Harris, 1984; Bennett, 1990; Saunders et al., 1991). Corridors, if adequate in arrangement and number, can in theory offset the negative consequences of population isolation in fragments (Harris 1984; Mech and Hallett, 2001) and reduce demographic stochasticity Merriam, 1991). One of the difficulties in managing anthropogenically altered landscapes is that susceptibility to fragmentation is highly species- specific, depending in part on historical population sizes, dispersal capacity, and historical population structure (Williams et al., 2003; Galbusera et al., 2004; Cushman, 2006; Luoy et al., 2007).

Comparative analyses suggest that, in general, species that typically have lower population sizes are often less genetically diverse (Frankham, 1996), and therefore should be more susceptible to genetic erosion resulting from habitat fragmentation, but this effect can be mitigated in species with sustained levels of dispersal between fragments (Galbusera et al., 2004; Cushman, 2006). In contrast, some empirical studies show that surprisingly, habitat fragmentation can have similar effects on common species (Dixo, 2005; Peakall and Lindenmayer, 2006), including those that are habitat generalists and have high rates of gene flow (Williams et al., 2003). Thus, interactions between species characteristics and those of the altered landscape are complex, precluding generalizations of the effect of habitat alteration on entire lineages (Cushman, 2006).

Amphibians are declining worldwide at an unprecedented rate (Stuart et al., 2004) and are particularly threatened by anthropogenic habitat modification (Dodd and Smith, 2003; Cushman

2006). Amphibians are the vertebrate lineage with highest number of species threatened with extinction (Stuart et al., 2004; Beebee and Griffiths, 2005) and their vulnerability is at least partially explained by their often narrow environmental tolerances (Findlay and Houlahan, 1997; Bridges and Semlitsch, 2000; Pounds et al., 2006) and generally low dispersal capacities (Gibbs, 1998; deMaynedier and Hunter, 2000), both characteristics that exacerbate the negative effects of habitat degradation and loss of population connectivity.

In this study we used population genetic analyses to test for the predicted effects of fragmentation in populations of a toad endemic to the Brazilian Atlantic Rainforest, one of the top 10 biodiversity hot spots (Mittermeier et al., 1999; Myers et al., 2000) and one of the most fragmented biomes in the world, with only 12% of its original range remaining (SOS Mata Atlântica, 2008). Our study focused on Rhinella ornata, a habitat-generalist that is common in forested as well as edges of disturbed areas (Baldissera et al., 2004). We studied this species in forests on the Ibiúna Plateau, a highly developed region in southwestern Brazil that still harbors both large continuous tracts as well as forest fragments (Dixo, 2005; Pardini et al., 2005). R. ornata is able to move through the agricultural matrix that isolates fragments and is abundant in fragments of all sizes; nonetheless, populations in small and mediumsized fragments show significant annual variation in abundance, suggesting possible demographic instability of populations in fragments (Dixo, 2005).

We compared genetic diversity and structure of R. ornata populations in fragments and continuous tracts of Atlantic Rainforest to test the hypotheses that (i) this generalist species is vulnerable to genetic erosion, (ii) larger fragment sizes and corridors mitigate fragmentation and maintain genetic diversity in populations, and (iii) fragmentation negatively impacts gene flow among remaining patches of habitat, despite this species’ ability to survive in deforested areas. We might expect that this generalist species would not be highly susceptible to the negative impacts of habitat fragmentation; therefore, any evidence of genetic erosion in this generalist and relatively tolerant species, implies that less common and more specialized species may suffer even more severe effects as a result of forest fragmentation and isolation in this threatened landscape.

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