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Thinking outside the box: problem-solving in free-living lizards

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Abstract

Despite evidence that organisms are more likely to exhibit their full range of cognitive abilities under conditions found in nature, studies evaluating cognition under such conditions remain rare, particularly in vertebrate species. Here, we conducted an experiment to evaluate problem-solving and motor self-regulation in free-living arboreal lizards, Anolis sagrei, under natural conditions. We presented lizards with a novel detour problem which challenged individuals to circumvent a transparent barrier in order to obtain a food reward. Individuals varied in their ability to solve the detour problem. Furthermore, those that solved the problem were able to improve their performance across trials by modifying the natural response of attempting to strike the reward through the transparent barrier, providing evidence of motor self-regulation. Solving the problem required individuals to modify their typical foraging behavior, as approaching the prey in a single burst of movement that culminated with an attack was an unsuccessful strategy. Contrary to expectations, our findings provide evidence of motor self-regulation in a visually oriented, sit-and-wait predator under natural conditions, suggesting motor self-regulation is not limited by foraging strategy. Our results also underscore the need to evaluate the cognitive abilities of free-living organisms in the wild, particularly for taxa that perform poorly under laboratory conditions.

Significance statement

Studies of animal cognition have a long history in animal behavior, which, in vertebrate species, has been dominated by experiments conducted under controlled laboratory conditions. Here, we showed that experiments can be taken “outside the box,” from the laboratory into natural conditions, and by doing so overcome some of the obstacles that have hindered our ability to study cognition in species unlikely to remain motivated when removed from the wild. We implemented a modified version of the cylinder task, which provided the stimuli needed for a visually oriented, sit-and-wait foraging lizard to participate in the experiments. Individuals of Anolis sagrei learned to solve the task by modifying what was previously described as a stereotyped prey capture behavior. In addition, individuals decreased the number of times they attempted to strike the prey through the transparent barrier. These findings provide further evidence of behavioral flexibility in anoles and new evidence of motor self-regulation. The latter demonstrates the need to extend our current understanding of potential forces favoring the evolution of cognition beyond those that have been proposed in birds and mammals. More generally, our findings demonstrate the importance of using experimental paradigms that are rooted in an understanding of the natural history of the species of interest.

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Data availability

The datasets generated during and analyzed during the current study are available in the Dryad repository, https://doi.org/10.5061/dryad.g79cnp5mq.

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Acknowledgments

We thank J. Jones and W. McHargue for assistance in the field; the members of the Chipojo lab, D. Steinberg, R. Cocroft, G. Burghardt; and two anonymous reviewers for helpful comments that greatly improved this manuscript; the National Science Foundation (DEB-0949357 and IOS-1051793); and the Bahamas Ministry of Agriculture and the Bahamas Environment, Science, and Technology Commission of the Ministry of the Environment for permission to conduct this research.

Ethics approval

This research adhered to the guidelines of the Institutional Animal Care and Use Committee at University of Missouri, Columbia protocol (#8244). We followed the Recommendations for the Care of Amphibians and Reptiles (Pough 1991) in the treatment of all animals used in this study. This is a field study, and as part of this study, animals were only individually marked and immediately released. The Bahamas Ministry of Agriculture and the Bahamas Environment, Science, and Technology Commission of the Ministry of the Environment provided permission to conduct this research.

Funding

This work was partially funded by the National Science Foundation (DEB-0949357 and IOS-1051793 to ML).

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Contributions

LS carried out the experiment, participated in data analysis, participated in the design of the study, and helped in drafting the manuscript; ML conceived of the study, helped with the data analysis, and drafted the manuscript. All authors gave final approval for publication.

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Correspondence to Manuel Leal.

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The authors declare that they have no conflict of interests.

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Communicated by T. Madsen

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Storks, L., Leal, M. Thinking outside the box: problem-solving in free-living lizards. Behav Ecol Sociobiol 74, 75 (2020). https://doi.org/10.1007/s00265-020-02852-x

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