Eat your heart out: choice and handling of novel toxic prey by predatory water rats Marissa L. Parrott A,E , J. Sean Doody B,C , Colin McHenry C and Simon Clulow C,D A Wildlife Conservation and Science, Zoos Victoria, Parkville, Vic. 3052, Australia. B Department of Biological Sciences, University of South Florida – St Petersburg, St Petersburg, FL 33705, USA. C School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW 2308, Australia. D Department of Biological Sciences, Macquarie University, Sydney, NSW 2109, Australia. E Corresponding author. Email: mparrot@zoo.org.au Abstract. We investigated predator–prey interactions between cane toads (Rhinella marina) and native water rats (Hydromys chrysogaster), where toads are novel prey. We show that wild water rats preferentially targeted larger toads, and consumed specific non-toxic organs only. Rats either rapidly learned these behaviours, or adapted them from hunting native frogs. Additional keywords: ancestral behavioural repertoire, heart, invasion, lethal toxic ingestion, liver, muscle, organ targeting, rapid learning Received 5 March 2019, accepted 27 August 2019, published online 23 September 2019 Introduction The ability of animals to adapt to novel circumstances, through learning or evolutionary change, can affect both the fitness of individuals and the fate of populations. The cane toad (Rhinella marina) has invaded numerous countries including Australia, where it has spread extensively across the north of the country (Brown et al. 2014). Cane toads present predators with potential novel prey as there are no native toads in Australia (Lever 2001; Clulow and Swan 2018). However, cane toad toxins, which are largely found in the parotoid glands and skin, can cause lethal toxic ingestion to would-be predators (reviewed in Lever 2001; Shine 2010). A great diversity in predator responses to toxic cane toads has been observed (reviewed in Shine 2010), ranging from success- ful ingestion without apparent ill effects to lethal toxic ingestion with population-level declines, extirpations and knock-on effects throughout animal communities via trophic cascades (Letnic et al. 2008; Doody et al. 2015, 2017). For example, ingestion, or simply mouthing, by monitor lizards (Varanus spp.) and northern quolls (Dasyurus hallucatus) results in severe population declines shortly after toad arrival (Doody et al. 2009, 2014, 2017; Woinarski et al. 2010). In contrast, some predators, particularly birds, are able to consume cane toads without any apparent harm to the predator. These predators often use a complex behavioural repertoire that involves specific handling techniques. For example, crows (Corvus orru) and kites (Milvus migrans, Haliastur indus, H. sphenurus) have been observed turning cane toads inside out to (apparently) avoid the skin toxins while consuming the muscles, tongue and innards (Covacevich and Archer 1975; Mitchell et al. 1995; Forsyth 2000; Wren 2000; Beckmann and Shine 2011). Among mammals, rodents are also able to exploit the cane toad as a food source. Experimental trials showed that three species of native rodents (Melomys burtoni, Rattus colletti, R. tunneyi), were able to kill and consume small toads with few ill-effects (Cabrera- Guzma ´n et al. 2015). Experiments also suggested that the rodents attacked toads on the basis of size, with smaller rodents targeting smaller juvenile toads, and larger individuals targeting larger juveniles (Cabrera-Guzma ´n et al. 2015). However, a decline of native rodents in areas invaded by cane toads suggests that, in addition to key threats such as changed fire regimes, toad toxins may be an issue for some rodents (Woinarski et al. 2010). Given the precipitous decline in native mammal fauna, particularly in northern Australia (Woinarski et al. 2010), it is important to elucidate mechanisms by which mammals are being affected by contemporary changes to the environment. According to anecdotal reports, the water rat, or rakali (Hydromys chrysogaster), kills and consumes cane toads; rats have been observed consuming toads, and dead toads were found within rat nests (collated in Cabrera-Guzma ´n et al. 2015). However, it is unknown whether the ability to consume the toads is via a level of tolerance to the toad toxin (a physiological adaptation), or through targeted consumption of non-toxic components (a behavioural adaptation). It is also unknown whether rats target smaller toads to minimise toxin consumption, or larger toads to maximise energetic benefit. CSIRO PUBLISHING Australian Mammalogy https://doi.org/10.1071/AM19016 Journal compilation Ó CSIRO 2019 www.publish.csiro.au/journals/am Research Note