Learned recognition of introduced predators determines survival of tadpole prey

Abstract

Summary Alien predators are one of the major causes for rapid decline and extinction of native species, because they often create novel ecological contexts in which the antipredatory responses of native organisms are no longer fit. Although larval amphibians are often capable of innately responding to chemical cues from local predators through changes in morphology and behaviour, naïve tadpoles generally cannot recognize introduced predators with which they have not shared an evolutionary past. However, in a few documented cases, aquatic organisms have been observed to alter morphology or behaviour in response to alien predators. Such a response may have evolved as adaptive recognition, increasing their repertoire of innate responses to include the novel predator or may have evolved as the prey's ability to learn new threats by association with conspecific alarm cues. The red swamp crayfish, Procambarus clarkii, is a harmful invasive species in aquatic systems world‐wide, causing great ecological impact on native amphibian populations during the last decades through intense predation of eggs and tadpoles. We demonstrate that naïve tadpoles of the western spadefoot toad, Pelobates cultripes, are not capable of innately recognizing water‐borne predator cues from the red swamp crayfish. Nevertheless, we demonstrate that P. cultripes tadpoles can learn to recognize the cues of the invasive predatory crayfish as a threat when they are exposed to predator cues combined with conspecific alarm cues. Finally, we show that tadpoles conditioned by joint exposure to crayfish and alarm cues enjoy higher survival during predation trials with invasive crayfish. Learning to recognize a newly introduced predator through association with conspecific alarm cues may allow successful generalization of antipredatory responses by tadpoles. This cognitive ability of tadpoles may contribute to reduce their vulnerability to alien predators and soothe the impact of invasions in natural populations.