Indirect ecological impacts of an invasive toad on predator–prey interactions among native species

Abstract

One of the many ways that invasive species can affect native ecosystems is by modifying the behavioural and ecological interactions among native species. For example, the arrival of the highly toxic cane toad (Bufo marinus) in tropical Australia has induced toad-aversion in some native predators. Has that shift also affected the predators' responses to native prey-for example, by reducing vulnerability of native tadpoles via a mimicry effect, or increasing vulnerability of other prey types (such as insects) via a shift in predator feeding tactics? We exposed a native predator (northern trout gudgeon, Mogurnda mogurnda) to toad tadpoles in the laboratory, and measured effects of that exposure on the fish's subsequent intake of native tadpoles and crickets. As predicted, toad-exposed fishes reduced their rate of predation on (palatable) tadpoles of native frogs (Litoria caerulea and L. nasuta). If alternative prey (crickets) were available also, the toad-exposed fishes shifted even more strongly away from predation on native tadpoles. Thus, invasion of a toxic species can provide a mimicry benefit to native taxa that resemble the invader, and can shift predation pressure onto other taxa.

Evolutionary Responses to Invasion: Cane Toad Sympatric Fish Show Enhanced Avoidance Learning

“…Cane toad sympatric fish displayed generalised aversion throughout the study which lasted for several months, indicating that generalised aversion acquired from exposure to cane toad tadpoles had a long-lasting effect on rainbowfish behaviour. These results support those of a previous study which demonstrated that experience with cane toads can produce a generalised aversion of similar prey types [40], [41]. The common planigale, Planigale maculata, is a small dasyurid that commonly feeds on frogs.…”

“…Planigale stopped feeding on frogs for up to 9 days following exposure to cane toads [40]. Similarly, lab experiments examining the effect of exposure to cane toad tadpoles in the northern trout gudgeon, Mogurnda mogurnda , showed a general shift away from native tadpoles [41]. Thus it seems likely that the toxic nature of the cane toad, even at the tadpole stage of the life cycle, is severe enough to generate aversion of similar prey types for considerable lengths of time.…”

A matter of proportion? Associational effects in larval anuran communities under fish predation

“…The proportion of the chemically defended tadpoles in the assemblage may equate to the level of predator experience with such prey. This leads to generalised aversion to all tadpoles when defended tadpoles are often encountered (Nelson et al 2010; Caller and Brown 2013) and killing of defended tadpoles when they are rarely encountered (Kruse and Stone 1984; Nomura et al 2011). This generalised aversion may be prevented if the fish use a taste-and-refuse strategy to differentiate between prey types (Nelson et al 2011).…”

“…Although here we focus on the effects resulting from unequal levels of defence against predators, the concept may be useful for tracking various interactions that are rather a by-product of current community composition than a consequence of selection for mimicking signals of another species. For animal communities, examples include ‘accidental mimicry’ between originally allopatric species or interactions between defended and undefended prey sharing an undiscriminating predator (Nelson et al 2010; Nesbit et al 2016; Wooster et al 2016; see also Robertson 2013, for ‘social traps’ resulting from coincidental visual resemblance in reef fish). Importantly, associational effects related to unequal defences in co-occurring species may in fact function as an incipient stage of the evolution of actual mimicry complexes (Mappes et al 1999; de Wert et al 2012).…”

Responses of Australian wading birds to a novel toxic prey type, the invasive cane toad Rhinella marina

“…The birds readily consumed the alternative food items offered (except that pied herons and little egrets rarely ate native frog tadpoles) but all of the species that we tested -Nankeen night herons, purple swamphens, pied herons and little egrets-avoided both cane toad metamorphs and cane toad tadpoles. Likely, cane toads are unpalatable to wading birds, as they are to some other types of native predators, including fish (Crossland and Alford 1998;Crossland 2001;Nelson et al 2010b), marsupials Llewelyn et al 2010b) and snakes (Llewelyn et al 2010a). The only case of regular consumption of cane toads was by purple swamphens, in trays containing both toad metamorphs and fruit (rather than toads alone).…”