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Predators usurp prey defenses? Toxicokinetics of tetrodotoxin in common garter snakes after consumption of rough-skinned newts

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Abstract

Snakes are common predators of organisms, such as amphibians, with toxic defenses that can be lethal to other predators. Because snakes do not have the option of dissecting prey into edible versus inedible components, they face a full dose of any chemical defenses encountered during attempted predation. This limitation has likely resulted in intense selection favoring the evolution of alternative mechanisms for dealing with prey toxins. These mechanisms can be physiological (e.g., resistance to prey toxins) or behavioral (e.g., toxin sampling and rejection). When physiological resistance arises, the possibility of bioaccumulation of a toxin results. We examined the coevolutionary interaction between the common garter snake (Thamnophis sirtalis) and the rough-skinned newt (Taricha granulosa), which contains a powerful neurotoxin called tetrodotoxin (TTX). In some populations syntopic with newts, individuals of T. sirtalis have evolved resistance to TTX. We examined the persistence of TTX in T. sirtalis after administration of an oral dose of TTX to investigate the possibility that snakes are sequestering TTX. The half-life of TTX in snake liver was estimated at 8.1 days. Accordingly, clearance of 99% of a single dose of TTX averages 61 days. Negative fitness consequences of intoxication during and after newt consumption may be balanced by co-opting the newts’ chemical defense for protection from the snakes’ own predators. Accounting of the coevolutionary dynamic between snakes and newts must incorporate post-consumption affects of lingering TTX.

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Acknowledgments

This research was supported by the National Science Foundation NSF-DEB 9796291 and 9903829 to E. D. Brodie III, NSF-DEB 9521429 and 9904070 to E. D. Brodie, Jr., a Sigma Xi Grant in Aid of Research to B. L. Williams, and the Gaige Award from the American Society of Ichthyologist and Herpetologists (ASIH) to B. L. Williams. This research was approved by the Utah State University Institutional Animal Care and Use Committee (IACUC protocol number 1008). Voucher specimens were deposited in the University of Texas at Arlington’s Collection of Vertebrates. We thank J. E. Motychak, D. G. Mulcahy, and B. J. Ridenhour, and I. M. Asmundsson for assistance in the collection of animals. We thank A. H. Savitzky, A. Mori, and D. A. Hutchinson for organizing the symposium “Sequestered Defensive Compounds in Tetrapod Vertebrates: A Symposium in Memory of John W. Daly,” held at the Sixth World Congress of Herpetology in Manaus, Brazil, on 21 August 2008 and supported by NSF IOS-0813842. This manuscript is based on our presentation there.

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Authors and Affiliations

  1. Department of Biology, Utah State University, 320 N. 2000 W. (Aggie Blvd.), Uintah Basin, Vernal, UT, 84078-4228, USA

    Becky L. Williams

  2. Hopkins Marine Station, Stanford University, 120 Oceanview Blvd., Pacific Grove, CA, 93950-3024, USA

    Charles T. Hanifin

  3. Department of Biology, Utah State University, 5305 Old Main Hill, Logan, UT, 84322-5305, USA

    Edmund D. Brodie Jr.

  4. Mountain Lake Biological Station and Department of Biology, University of Virginia, P.O. Box 400328, Charlottesville, VA, 22904-4328, USA

    Edmund D. Brodie III

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  1. Becky L. Williams
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  2. Charles T. Hanifin
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  4. Edmund D. Brodie III
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Correspondence to Becky L. Williams.

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Williams, B.L., Hanifin, C.T., Brodie, E.D. et al. Predators usurp prey defenses? Toxicokinetics of tetrodotoxin in common garter snakes after consumption of rough-skinned newts. Chemoecology 22, 179–185 (2012). https://doi.org/10.1007/s00049-011-0093-3

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