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Anxiety-like behavior and tectal gene expression in a foraging/predator avoidance tradeoff task using adult African clawed frogs Xenopus laevis

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Abstract

Animals often halt foraging in the presence of predator cues, an ecological phenomenon known as the foraging/predator avoidance tradeoff. Although some have proposed that anxiety may exist in animals exposed to predator cues, few studies have examined whether such interactions lead to anxiety-like behavior in animals other than laboratory rodents and zebrafish. In this experiment, a foraging/predator avoidance tradeoff task was modified using adult male African clawed frogs (Xenopus laevis) and a looming visual predator stimulus to determine if (1) visual predator cues reduce appetitive behavior, (2) visual predator cues lead to predator avoidance behavior, and (3) if visual predator cues alter the abundance of transcripts in the optic tectum known to be modulated in other brain areas during anxiety. Frogs exposed to the predator stimulus did not reduce their food intake, although sweeping, a foraging behavior, was significantly reduced by the predator stimulus. Predator-exposed animals spent significantly more time stationary and entered the predator zone less compared controls. There were no statistically significant changes in relative transcript abundance of anxiety-related peptides between the groups in the optic tectum. Collectively, this tradeoff task was able to induce discrete avoidance and appetitive behaviors that are similar to anxiety-like behaviors observed in other predator avoidance models; however, the effects of visual threats on feeding and anxiety-related transcript abundance requires further study.

Significance statement

Halting foraging activities to increase vigilance and engage avoidance behaviors has been proposed to play an adaptive role in survival of predator encounters in a number of animal species. Some have proposed that anxiety evolved as a state associated with the engagement of avoidance and antipredator behavior. However, few studies have examined whether such foraging/predator avoidance tradeoffs result in anxiety-like behavior in animals other than rodents. We developed a foraging/predator avoidance tradeoff task in an aquatic frog species to determine if the sight of a looming visual threat interferes with feeding and causes anxiety-like behavior in an amphibian. Our data suggest that some, but not other (feeding, for example), behavioral aspects of foraging/predator avoidance tradeoffs mimic anxiety-like behavior when a visual threat is present. These data contribute to a growing body of literature indicating that anxiety may be an adaptive response to predator threats in non-mammalian species.

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Data are available in the “Supplementary information.”

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Acknowledgements

We thank the Texas Tech University Department of Biological Sciences and the Texas Tech University Association of Biologists for funds to NMM. We also acknowledge Drs. Karina Alvina, Lauren Gollahon, Naima Moustaid-Moussa, and Ernest Smith for assistance with experimental design and Marcos Arciniega and Hailey Luckie for help with behavior analysis. Finally, we thank the anonymous reviewers and editorial team at BES for their valuable contributions. This work was completed in partial fulfillment of the requirements for a doctoral degree in the Department of Biological Sciences at Texas Tech University (NMM).

Funding

Funding was provided by the National Science Foundation IOS #1,656,734, Texas Tech University Department of Biological Sciences, and a Graduate Student Research Support Award provided by Texas Tech University Graduate School.

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  1. Department of Biological Sciences, Texas Tech University, Lubbock, TX, 79409-3131, USA

    N. M. Menon & J. A. Carr

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Both authors contributed to the design of the study. Material preparation, data collection, and analysis were performed by NMM. Writing and editing was done by NMM with guidance and editing from JAC. Guidance, resources, and supervision on this project was provided by JAC.

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Correspondence to J. A. Carr.

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All procedures involving animals were approved by the Texas Tech Animal Care and Use Committee (protocol number 18089–11) and follow Association for Assessment and Accreditation of Laboratory Animal Care International (AAALAC International) guidelines including the Eighth Edition of the Guide for the Care and Use of Laboratory Animals (NRC 2011) and the European Convention for the Protection of Vertebrate Animals Used for Experimental and Other Scientific Purposes, Council of Europe (ETS 123).

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Menon, N.M., Carr, J.A. Anxiety-like behavior and tectal gene expression in a foraging/predator avoidance tradeoff task using adult African clawed frogs Xenopus laevis. Behav Ecol Sociobiol 76, 115 (2022). https://doi.org/10.1007/s00265-022-03219-0

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