Amphibian Richness Patterns in Atlantic Forest Areas Invaded by American Bullfrogs
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bs_bs_banner Austral Ecology (2014) 39, 864–874 Amphibian richness patterns in Atlantic Forest areas invaded by American bullfrogs CAMILA BOTH,1,2* BRUNO MADALOZZO,3 RODRIGO LINGNAU4 AND TARAN GRANT1,5 1Programa de Pós-Graudação em Zoologia, Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, 3Programa de Pós-Graduação em Biodiversidade Animal, Universidade Federal de Santa Maria, Santa Maria, 4Universidade Tecnológica Federal do Paraná, Francisco Beltrão, and 5Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, Brazil; and 2School of Biological Sciences, University of Sydney, Sydney, New South Wales, Australia (Email: [email protected]) Abstract The relationship between invasion success and native biodiversity is central to biological invasion research. New theoretical and analytical approaches have revealed that spatial scale, land-use factors and commu- nity assemblages are important predictors of the relationship between community diversity and invasibility and the negative effects of invasive species on community diversity. In this study we assess if the abundance of Lithobates catesbeianus, the American bullfrog, negatively affects the richness of native amphibian species in Atlantic Forest waterbodies in Brazil. Although this species has been invading Atlantic Forest areas since the 1930s, studies that estimate the invasion effects upon native species diversity are lacking. We developed a model to understand the impact of environmental, spatial and species composition gradients on the relationships between bullfrogs and native species richness. We found a weak positive relationship between bullfrog abundance and species richness in invaded areas. The path model revealed that this is an indirect relationship mediated by community composition gradients. Our results indicate that bullfrogs are more abundant in certain amphibian communities, which can be species-rich. Local factors describing habitat heterogeneity were the main predictors of amphibian species richness and composition and bullfrog abundance. Our results reinforce the important role of habitats in determining both native species diversity and potential invasibility. Key words: Anura, Brazil, diversity, invasion, Lithobates catesbeianus, Ranidae. INTRODUCTION Charles Elton predicted a scenario of ecological and economical losses linked with species invasions The immigration of novel species into communities or (Simberloff 2011), and since his seminal synthesis in uncolonized patches is an important process for com- ‘The Ecology of Invasions by Animals and Plants’ munity development, structure and composition (Elton 1958) there is growing interest to identify (MacArthur & Wilson 1967; Connell & Slatyer 1977; species traits linked to invasion propensity and com- Loreau & Mouquet 1999).We are currently witnessing munity properties facilitating or preventing invasions. an age of biological invasions, with novel species In his book, Elton observed that ‘tropical systems are less being incorporated into local communities not only invaded than species poor temperate and boreal systems’. by dispersal, but also by intentional or accidental Elton associated ‘tropical resistance’ with highly introductions. Such invasions are not restricted to diverse communities, harbouring large numbers of taxa, regions, biomes, or continents (Soulé 1990), and enemies and parasites, which, in turn, can impede the they have attracted much attention because they can establishment of novel species. This idea is currently be economically expensive. For instance, exotic species recognized as the diversity–invasibility hypothesis (see can negatively affect crops, fisheries, public health Justus 2008). Elton himself recognized that this should systems etc., resulting in the expense of billions of only partially explain the low invasion rates in the dollars (Pimentel et al. 2001). Further, invasions can tropics. Studies subsequent to Elton (1958) explained also be expensive in an ecological and evolutionary the diversity–invasibility hypothesis in the light of context, since they have been linked to recent species resource exploitation. Following this rationale, diverse extinctions (Clavero & García-Berthou 2005). tropical communities are more resistant because richer communities tend to be saturated with species that *Corresponding author. exploit resources in complementary ways (MacArthur Accepted for publication April 2014. & Levins 1967; MacArthur 1970). © 2014 The Authors doi:10.1111/aec.12155 Austral Ecology © 2014 Ecological Society of Australia BULLFROG INVASION AND ANURAN DIVERSITY 865 The diversity–invasibility hypothesis is still a central species and community diversity patterns, asking issue in ecology (Fridley et al. 2007).There is evidence whether invasions are related to less diverse commu- from observational studies that alien species diversity nities or differences in community composition, while is low in richer systems, although some studies have controlling for environmental and spatial variation. found no relationship at all (e.g. Case & Bolger 1991). Classical examples of invasion effects on ecosystem Experimental studies supplied evidence that supports diversity come from freshwater habitats that have suf- both negative (e.g. Tilman 1997) and positive relation- fered historically from structural modifications. These ships (e.g. Robinson et al. 1995) between diversity and are among the most endangered ecosystems, and invasion. Nevertheless, there are also experimental biotic modifications imposed by the addition of inva- studies highlighting the lack of a relationship between sive species could lead to local extinction of freshwater diversity and invasion (e.g. Robinson & Dickerson species (Witte et al. 1992; Dodds & Whiles 2010). 1984). The presence of such contrasting results has Waterbodies such as lakes, ponds, pools and tempo- been termed ‘the invasion paradox’ (Fridley et al. rary streams can be viewed as small islands, which 2007) and seems to be related to spatial scale. In an seem to be very sensitive to invasions (Ricciardi & extensive review, Fridley et al. (2007) showed that MacIsaac 2011). The bullfrog (or American bullfrog) large-scale studies suggest a positive relationship Lithobates catesbeianus (Shaw 1802) is a member of the between invasive species and native richness. Such ‘hall of fame’ of freshwater invasive species. It is cited positive correlation indicates that richer communities as one of the 100 worst alien species in the world are able to accommodate introduced species, despite (Lever 2003) and is one of the causes of amphibian high numbers and abundance of native species, known declines in North America. Furthermore, the species as ‘biotic acceptance’ (Stohlgren et al. 2006). In con- appears to be an important vector of fatal amphibian trast, at smaller scales relationships are often negative, diseases such as chytridiomycosis (Daszak et al. 2004; especially in experimental studies (Fridley et al. 2007). Schloegel et al. 2010). Bullfrogs benefit from human- Nonetheless, a positive relationship between non- modified landscapes (Adams 1999; Zampella & native and native species might be due to sampling Bunnell 2000; D’Amore et al. 2010; Fuller et al. artefacts (Fridley et al. 2004). Apparently positive or 2011), the presence of non-native fish in fresh waters negative relationships might also result from analytical (Adams & Wasson 2000; Adams et al. 2003), and models that ignore important co-variables that might simple aquaculture enclosures that enable a continu- be related to invasive species abundance or richness ous source of propagules (Liu & Li 2009). and native species diversity (Taylor & Irwin 2004). Bullfrogs originate from eastern North America Factors such as propagule pressure, disturbance and and are distributed from Mexico to south Canada; other environmental gradients often function synergis- however, invasive populations occur in western North tically to explain invasion patterns (Elton 1958; Von America, Europe, Asia, and Central and South Ameri- Holle & Simberloff 2005). Therefore, in situ studies can countries where they were introduced for aquacul- that consider distinct spatial scales and address the ture practices (Santos-Barrera et al. 2009). In invaded relationship between native richness and invasive sites, they can be negatively correlated with native frog species are required for a thorough understanding of abundance and with the occurrence of certain native the diversity–invasibility hypothesis. This is especially frog species; they can also reduce tadpole survival true for approaches that consider causal links connect- (Kupferberg 1997; Kiesecker & Blaustein 1998; Kats ing environmental and community gradients. & Ferrer 2003; Wang & Li 2009) and are often impli- In many systems, invasions are a concrete reality, cated as a factor in the decline of native amphibians despite several decades of research and efforts for their and potential species loss (Kraus 2009). A negative prevention (Richardson 2011). In previously invaded relationship between bullfrogs and native anuran rich- ecosystems, we are challenged to estimate the invasive ness has been reported in China (Li et al. 2011). species effects on diversity rather than to understand Bullfrogs have been present in Brazil since the whether diversity will prevent invasions.The same pre- 1930s, and invasions have continued to occur and dictions about the relationship between diversity and expand since then, probably