Disentangling the trophic interactions between American bullfrogs and native anurans: Complications resulting from post‐metamorphic ontogenetic niche shifts

Abstract

1. The American bullfrog, Lithobates catesbeianus (Shaw, 1802), is considered one of the world's worst invaders because of its potential to affect native fauna adversely, especially amphibians, through predation, competition, breeding interference, and disease transmission.2. Here, the potential impact of introduced American bullfrogs (juveniles and adults) on native adult green frogs, Pelophylax kl. esculentus (Linnaeus, 1758), was investigated in a pond ecosystem by means of stomach-content and stable-isotope analyses. Specifically, this study was aimed at assessing the impact of the American bullfrog on native green frogs in terms of predation and competition (i.e. feeding ecology and habitat use), and uncovering changes in interspecific interactions linked to the ontogenetic dietary-habitat shifts of the invaders. 3. Stomach contents and isotope analyses suggest that L. catesbeianus changes trophic position in the food chain and undergoes ontogenetic dietary-habitat shifts during its life cycle. The species therefore has the potential to exert a double impact on native green frogs: as a predator at the adult stage and as a competitor (for food and habitat use) at the juvenile stage. 4. Stomach-content and isotope analyses gave similar results, suggesting that the predation impact by adult American bullfrogs on green frogs is mediated by the presence of the alien red swamp crayfish, Procambarus clarkii (Girard, 1852). Juvenile American bullfrogs and native amphibians overlap in their diet composition and in their habitat use, suggesting the existence of potential competition between the two species. 5. Ontogenetic dietary-habitat shifts in the American bullfrog, local conditions, and trophic interactions should be seriously considered in management approaches to promote the long-term coexistence of L. catesbeianus and native amphibians. Such management options have been neglected in the literature, and are worthy of further investigation to understand their efficacy on native species.

Trophic structure of a pond community dominated by an invasive alien species: Insights from stomach content and stable isotope analyses

“…The introduction of a non‐native predator ( L. catesbeianus ) at the second highest level of the study food web, linked by a predator–prey relationship to non‐native P. clarkii , could have a marginal role in affecting the structure of the whole community, potentially because of the primacy of L. catesbeianus – P. clarkii interactions (Bissattini & Vignoli, 2017; Bissattini, Buono & Vignoli, 2018; Bissattini, Buono & Vignoli, 2019). In this context, unpredictable and unwanted outcomes following IAS removal in isolation are likely to occur since invaders are well established, strongly interspersed with native species, and connected at different trophic levels ( Zavaleta, Hobbs & Mooney, 2001; Schlaepfer et al, 2005).…”

“…However, most often, the combined effects of non‐native predators on native prey species are lower than the expected sum of individual effects owing to antagonistic interactions among IAS (Jackson, 2015; Wasserman et al, 2016; Bissattini & Vignoli, 2017; Jackson et al, 2017; Bissattini, Buono & Vignoli, 2018; Bissattini, Buono & Vignoli, 2019). Indeed, there are several cases in which non‐native prey represents an alternative food source for non‐native predators, decreasing the predation pressure on native resources (Karl & Best, 1982; Murphy & Bradfield, 1992; Liu et al, 2015; Bissattini, Buono & Vignoli, 2018; Liu et al, 2018; Bissattini, Buono & Vignoli, 2019). This suggests that invaders in different trophic positions may replace the ecological role of extinct taxa, mitigating the trophic downgrading (Cucherousset, Blanchet & Olden, 2012).…”

“…Here, a system of ponds dominated by IAS was analysed by combining two different approaches: stomach content analysis and stable isotope analysis. Stable carbon ( δ 13 C) and nitrogen ( δ 15 N) isotope ratios are a useful tool to describe qualitatively and quantitatively how organisms interact via diet, highlighting the potential trophic overlap and competition among species (Haubrock et al, 2018a; Bissattini, Buono & Vignoli, 2019). Stable isotope analysis can be used to compare the trophic ecology and the effect of IAS on trophic levels, thus estimating their impact on local communities (Balzani et al, 2016; Haubrock et al, 2019a; Haubrock et al, 2019b).…”

Floodplains provide important amphibian habitat despite multiple ecological threats

“…It is possible that our native amphibian assemblage was not as susceptible to bullfrogs due to their use of terrestrial habitats post-metamorphosis. Where native amphibian species are more reliant on aquatic habitats, such as in desert or Mediterranean climates, they may be more vulnerable to bullfrog predation or competition (Bissattini et al 2019). Bullfrogs may also be more problematic where they transmit deadly amphibian pathogens, which pose a serious threat for native amphibians in Brazil and Europe (Garner et al 2006, Carvalho et al 2017.…”

Density and diet of invasive alien anuran species in a disturbed landscape: A case in the University of the Philippines Mindanao, Davao City, Philippines

“…The feeding behavior of frog species in the wild includes insects and arthropods, having specialized diet on selection of prey with species restricted in forests and man-altered environments (Braga et al 2012). Comparison of diet in invasive and native populations is necessary to understand dietary requirements, dietary flexibility, and the associated impacts of invasive species (Courant et al 2017;Bissattini and Vignoli 2017;Bissattini et al 2018Bissattini et al , 2019.…”