Behavioural responses of native predators to an invasive toxic prey species

Abstract

One important impact of invasive species may be to modify the behaviour of native taxa. For example, the invasion of highly toxic cane toads (Bufo marinus) kills many anurophagous native predators, but other predators learn to recognize and avoid the toxic invader. We exposed native fish (northern trout gudgeons, Mogurnda mogurnda) and Dahl's aquatic frogs (Litoria dahlii) to cane toad tadpoles, then monitored the predator's responses during subsequent trials. Both the frogs and fish initially attacked toad tadpoles, but rapidly learned not to do so. Fish and adult frogs retained their aversion for at least a week, whereas recently metamorphosed frogs did not. Clearly, the spread of cane toads through tropical Australia can modify feeding responses of native aquatic predators. For predators capable of rapid avoidance learning, the primary impact of cane toads may be on foraging behaviour rather than mortality.

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

“…Importantly, prior to direct exposure there were clear differences in the number of attacks on cane toad tadpoles between the two populations, however, following direct exposure the difference was eliminated. More broadly, there is evidence that crimson-spotted rainbowfish showed avoidance learning with repeated exposure to toxic prey items which is in line with previous studies in a variety of terrestrial and aquatic taxa [32], [33], [34].…”

“…The marbled frog ( Limnodynastes convexiusculu ) ceased attempting to consume cane toads and ignored them as a possible food source after repeated direct exposure to live cane toad metamorphs [32]. Similar responses to cane toad tadpoles have been observed in other aquatic predators; northern trout gudgeons ( Mogurnda mogurnda ), Dahl's aquatic frog ( Litoria dahlii) , sooty grunter ( Hephaestus fuliginosus ) and barramundi ( Lates calcarifer ) ceased attacking cane toad tadpoles after repeated exposure [33], [34]. Thus far, however, no studies have investigated whether the learnt aversion to cane toad tadpoles occurs in the wild or whether the presence of toxic prey items has evolutionary consequences for avoidance learning in general.…”

Bangers and cash: Baiting efficiency in a heterogeneous population.

“…While 62% may seem a relatively poor level of bait success, we can reasonably expect that some fraction of these non-baitable animals may also avoid toads. Certainly there is evidence in other taxa that some level of innate avoidance of toads is present in toad-naïve predator populations (e.g., the common planigale ( Planigale maculata ) (Webb et al 2008), red-cheeked dunnart ( Sminthopsis virginiae ) (Webb, Pearson & Shine 2011), native rodents ( Melomys burtoni, Rattus colletti and Rattus tunneyi ) (Cabrera-Guzmán et al 2015), terrestrial snake species (Phillips, Brown & Shine 2003) scincid, agamid and varanid lizards (Smith & Phillips 2006; Llewelyn et al 2014; Pearson et al 2014), avian species (Beckmann & Shine 2009), and aquatic animals such as the barramundi ( Lates calcarifer ), sooty grunter ( Hephaestus fuliginosus ) (Crossland 2001) northern trout gudgeons, ( Mogurnda mogurnda), Dahl’s aquatic frogs ( Litoria dahlia ) (Nelson, Crossland & Shine 2011) and freshwater crocodiles ( Crocodylus johnstoni ) (Somaweera & Shine 2012). There is also evidence that such innate avoidance may provide the raw material on which natural selection can act to generate a rapid adaptive response to toads (Phillips & Shine 2006; Smith & Phillips 2006; Llewelyn et al 2011; Somaweera & Shine 2012; Ujvari, Oakwood & Madsen 2013; Kelly & Phillips 2017; Tingley et al 2017).…”

Locomotion and survival of two sympatric larval anurans, Bufo gargarizans (Anura: Bufonidae) and Rana zhenhaiensis (Anura: Ranidae), after partial tail loss

“…Aquatic predators are more widely distributed closer to the surface of ponds, which is the microhabitat of R. zhenhaiensis, whereas B. gargarizans tadpoles inhabit the button of ponds (FEI et al 2009). 2) The toad tadpole and the frog tadpole taste differently to predators (WEI et al 2013), which results in different the levels of tail damage between the two species. Many toad tadpoles are toxic and unpalatable to most aquatic predators, which decreases their chances of being predated and consequently losing their tails (LAURILA 1998, ÁLVAREZ & NICIEZA 2009, NELSON et al 2011a. On the other hand, the frog tadpole lacks the ability to produce toxins, which results in more attacks from a greater variety of predators (WERNER & MCPEEK 1994, LAURILA et al 2002, WILSON et al 2005.…”