A native dasyurid predator (common planigale, Planigale maculata) rapidly learns to avoid a toxic invader

Abstract

Interactions between invasive species and native fauna afford a unique opportunity to examine interspecific encounters as they first occur, without the complications introduced by coevolution. In northern Australia, the continuing invasion of the highly toxic cane toad Bufo marinus poses a threat to many frog-eating predators. Can predators learn to distinguish the novel toxic prey item from native prey (and thus, avoid being poisoned), or are longer-term genetically based changes to attack behaviour needed before predators can coexist with toads? To predict the short-term impact of cane toads on native predators, we need to know the proportion of individuals that will attack toads, the proportion surviving the encounter, and whether surviving predators learn to avoid toads. We quantified these traits in a dasyurid (common planigale, Planigale maculata) that inhabits tropical floodplains across northern Australia. Although 90% of naïve planigales attacked cane toads, 83% of these animals survived because they either rejected the toad unharmed, or killed and consumed the prey snoutfirst (thereby avoiding the toxin-laden parotoid glands). Most planigales showed one-trial learning and subsequently refused to attack cane toads for long time periods (up to 28 days). Toad-exposed planigales also avoided native frogs for up to 9 days, thereby providing an immediate benefit to native anurans. However, the predators gradually learnt to use chemical cues to discriminate between frogs and toads. Collectively, our results suggest that generalist predators can learn to distinguish and avoid novel toxic prey very rapidly -and hence, that small dasyurid predators can rapidly adapt to the cane toad invasion. Indeed, it may be feasible to teach especially vulnerable predators to avoid cane toads before the toads invade, by deploying low-toxicity baits that stimulate taste-aversion learning.

Occurrence of non-volant mammals on islands along the Kimberley coast of Western Australia

“…For example, the arboreal species Phascogale tapoatafa is difficult to detect and rarely trapped in the Northern Kimberley (Start et al 2007). Species that have restricted distributions in the Kimberley in general and were not detected on the islands include Mesembriomys gouldii, Conilurus penicillatus, Trichosurus vulpecula and Petropseudes dahli, the latter species being restricted to particular rocky habitat types (McKenzie et al 1975;Start et al 2007;Webb et al 2008). Tall open forests that contain hollow-bearing trees favoured by all these species (except P. dahli) (Friend et al 1991;Woinarski et al 1999) have a restricted distribution on the Kimberley islands, probably due to the mostly skeletal soils on the majority of the islands (Burbidge et al 1991).…”

“…However, a captive study showed that S. virginiae and P. maculata learned to avoid Cane Toads after initial encounters (Webb et al 2008;Shine 2010), and S. virginiae abundance did not vary at sites colonised by Cane Toads in Kakadu National Park, Northern Territory (Shine 2010).…”

Impact of the invasive cane toad (Bufo marinus) on an Australian frog (Opisthodon ornatus) depends on minor variation in reproductive timing

“…;mammals-Webb et al 2008). That aversion may reduce rates of predation on native anurans that superWcially resemble cane toads (Webb et al 2008). Other indirect eVects of toad invasion may include a reduction in the abundance of disease-carrying mosquitoes (Hagman and Shine 2007).…”

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

“…If the predator does not receive a lethal dose of toxin, it may alter its future behaviour as a result of the encounter. For example, marsupial carnivores (Planigale maculata), fishes (Lates calcifera, Mogurnda mogurnda) and frogs (Litoria dahlii) can learn in this way: after attempting to eat toxic B. marinus tadpoles or metamorphs, the predators subsequently avoid this prey type (Crossland 2001;Nelson 2008;Webb et al 2008). Such effects might influence predator-prey relationships in tropical Australia, the home of a diverse frog fauna (Tyler 1999).…”