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Evolutionary shifts in anti-predator responses of invasive cane toads (Rhinella marina)

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Abstract

A potential prey item’s response to encountering a predator depends on aspects of the predator (e.g., its locomotor capacity), the local environment (e.g., proximity to shelter) and the physiological state of the prey item, but in addition, anti-predator tactics also vary geographically among different populations within wide-ranging species. Using standardised trials, we tested responses of cane toads (Rhinella marina) to being placed on a laboratory runway and encouraged to flee. Overall, the toads least capable of rapid locomotion were the ones most likely to respond to simulated predator attack by exuding toxins rather than attempting to escape. A toad’s willingness to move down the runway and its propensity to exude toxin from the parotoid glands rather than fleeing were repeatable in successive trials and influenced by the animal’s location of origin, morphology, previous experience, and parentage. We found that specimens from Australia were more willing to flee than were those from the native range (French Guiana) or Hawai’i; larger toads, and those with relatively longer legs, were more willing to flee; captive-raised toads were less willing to flee and more willing to exude toxin. Captive-raised offspring resembled their wild-caught parents both in propensity to run and in propensity to exude toxin. Thus, geographic divergence among cane toad populations in anti-predator responses reflects a complex combination of processes, including both developmental plasticity and heritability.

Significance statement

The process of colonising novel environments exposes an organism to a host of different predators that exert selection on morphology, behaviour and physiology. Over time, this can lead to the evolution of novel phenotypes that are adapted to local conditions. Anthropogenically facilitated biological invasions provide a unique opportunity to study how species respond to colonisation of new environments. Here, we studied geographic variation in cane toad (Rhinella marina) anti-predator behaviours from a range of locations (including invasive and native populations) using standardised trials. Our results suggest that invasive Australian cane toads have undergone a shift in their anti-predator response, becoming more willing to flee than are conspecifics from other areas. Location of origin, morphology, prior experience and parentage all played a role in shaping a toad’s anti-predator response, suggesting that the behaviour represents a combination of plastic and heritable variation.

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Acknowledgments

We thank Samantha McCann, Georgia Ward-Fear, Greg Clarke, Matthew Greenlees, Michael Crossland, Simon Ducatez, Jayna DeVore, Crystal Kelehear, Martin Mayer, Maddie Sanders, Jodie Gruber, Chalene Bezzina, Damian Holden, Georgia Kosmala, Marta Vidal García and Kimberley Lemmen for assistance with toad collection; Melanie Elphick for formatting the manuscript; William Mautz for information and resources in Hawai’i; and Philippe Gaucher for his assistance in co-ordinating fieldwork in French Guiana. We also thank the anonymous reviewers for their suggestions to improve the manuscript.

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This study was funded by the Australian Research Council (Grant #FF0561365).

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Correspondence to Cameron M. Hudson.

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Ethical statement

This study was conducted with approval from the State of Hawai’i Department of Land and Natural Resources, Division of Forestry and Wildlife (permit number Ex15-15 and Ex15-16) and the Animal Care and Ethics Committee of the University of Sydney (protocol 6705). All procedures performed in studies involving animals were in accordance with the ethical standards of the institutions under which the studies were conducted. This article does not contain any studies with human participants performed by any of the authors.

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The data sets collected and/or analysed during the current study are available from the corresponding author on reasonable request.

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The authors declare that they have no conflict of interest.

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Communicated by C. R. Gabor

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Hudson, C.M., Brown, G.P. & Shine, R. Evolutionary shifts in anti-predator responses of invasive cane toads (Rhinella marina). Behav Ecol Sociobiol 71, 134 (2017). https://doi.org/10.1007/s00265-017-2367-4

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