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Tetrodotoxin affects survival probability of rough-skinned newts (Taricha granulosa) faced with TTX-resistant garter snake predators (Thamnophis sirtalis)

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Abstract

Lethal chemical defenses in prey species can have profound effects on interactions with predators. The presence of lethal defenses in prey can correct the selective imbalance suggested by the life-dinner principle in which the fitness consequences of an encounter between predator and prey should be much greater for the prey species than the predator. Despite the apparent adaptive advantages of lethality the evolution of deadly prey presents a fundamental dilemma. How might lethal defenses confer an individual fitness advantage if both predators and prey die during interactions? We examined the interaction between the rough-skinned newt (Taricha granulosa), which contains a powerful neurotoxin called tetrodotoxin (TTX), and the common garter snake (Thamnophis sirtalis). In some sympatric populations, Th. sirtalis have evolved physiological resistance to TTX. Whether the newts’ toxin confers protection from snake predators or has been disarmed by the snakes’ physiological resistance has not yet been directly tested. In predator–prey trials, newts that were rejected by snakes had greater concentrations of TTX in their skin (4.52 ± 3.49 mg TTX/g skin) than those that were eaten (1.72 ± 1.53 mg TTX/g skin). Despite the plethora of taxa that appear to use TTX defensively, this is the first direct and quantitative demonstration of the antipredator efficacy of TTX. Because the survival probability of a newt (and thus fitness) is affected by individual TTX concentration, selection can drive the escalation of toxin levels in newts. The variable fitness consequences associated with both TTX levels of newts and resistance to TTX in snakes that may promote a strong and symmetrical coevolutionary relationship have now been demonstrated.

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Acknowledgments

This research was supported by the National Science Foundation NSF-DEB 9796291 & 9903829 to E. D. Brodie III, NSF-DEB 9521429 & 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. Collecting permits were provided by the Oregon Department of Fish and Wildlife.

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Authors and Affiliations

  1. Department of Biology, MSC 3AF, New Mexico State University, PO Box 30001, Las Cruces, NM, 88003-8001, 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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  3. Edmund D. Brodie Jr
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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. Tetrodotoxin affects survival probability of rough-skinned newts (Taricha granulosa) faced with TTX-resistant garter snake predators (Thamnophis sirtalis). Chemoecology 20, 285–290 (2010). https://doi.org/10.1007/s00049-010-0057-z

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  • DOI: https://doi.org/10.1007/s00049-010-0057-z

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