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

Abstract

The introduced cane toad (Bufo marinus) poses a major threat to biodiversity due to its lifelong toxicity. Several terrestrial native Australian vertebrates are adapting to the cane toad’s presence and lab trials have demonstrated that repeated exposure to B. marinus can result in learnt avoidance behaviour. Here we investigated whether aversion learning is occurring in aquatic ecosystems by comparing cane toad naïve and sympatric populations of crimson spotted rainbow fish (Melanotaenia duboulayi). The first experiment indicated that fish from the sympatric population had pre-existing aversion to attacking cane toad tadpoles but also showed reduced attacks on native tadpoles. The second experiment revealed that fish from both naïve and sympatric populations learned to avoid cane toad tadpoles following repeated, direct exposure. Allopatric fish also developed a general aversion to tadpoles. The aversion learning abilities of both groups was examined using an experiment involving novel distasteful prey items. While both populations developed a general avoidance of edible pellets in the presence of distasteful pellets, only the sympatric population significantly reduced the number of attacks on the novel distasteful prey item. These results indicate that experience with toxic prey items over multiple generations can enhance avoidance leaning capabilities via natural selection.

Trade‐offs affect the adaptive value of plasticity: stronger cannibal‐induced defenses incur greater costs in toad larvae

“…The cues that alert hatchlings to the approach of cannibalistic tadpoles may also have an anti‐predator function. Although toad tadpoles are slow and conspicuous, their skin is highly distasteful, discouraging predation by both fish and a variety of invertebrates (Wassersug 1971, Crossland 2001, Caller and Brown 2013). Swabs of this skin alone can induce hatchling plasticity (M. R. Crossland, J. L. DeVore, and R. Shine, unpublished data ).…”

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 ).…”

Numbers, neighbors, and hungry predators: What makes chemically defended aposematic prey susceptible to predation?

“…Instead, we suggest that the results were genuinely caused by avoidance learning, that is, the fish learned about the prey defenses after sampling a number of chemically defended tadpoles and refrained from further sampling (“acquisition phase” and “asymptotic phase” of aversive learning, respectively; Skelhorn et al., 2016). The process of learning to avoid defended prey has been demonstrated in fish (Caller & Brown, 2013; Giménez‐Casalduero et al., 1999; Glandt, 1984). Alternatively, the predators may continue to sample the defended prey, but sampling may become less detrimental (i.e., inflicting fewer injuries) to prey with growing predator experience, which correlates with prey density (Kruse & Stone, 1984; Nelson et al., 2010).…”