Coevolution of deadly toxins and predator resistance: Self-assessment of resistance by garter snakes leads to behavioral rejection of toxic newt prey

Herpetologica

Volumn 59, Issue 2, 2003, Pages 155-163

  Williams, Becky L ^a   Brodie Jr , Edmund D ^a   Brodie III, Edmund D ^b  

^a UTAH STATE UNIVERSITY   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Predation Predator prey; Resistance; Selection; Taricha; Tetrodotoxin; Thamnophis; Toxin

Indexed keywords

ANTIPREDATOR DEFENSE; COEVOLUTION; SNAKE; TOXIN;

AMPHIBIA; REPTILIA; SALAMANDRIDAE; SERPENTES; TARICHA; TARICHA GRANULOSA; THAMNOPHIS; THAMNOPHIS SIRTALIS;

EID: 0038782005     PISSN: 00180831     EISSN: None     Source Type: Journal    
DOI: 10.1655/0018-0831(2003)059[0155:CODTAP]2.0.CO;2     Document Type: Article

References (48)

1. ALATALO, R. V., AND J. MAPPES. 1996. Tracking the evolution of warning signals. Nature 382:708-709.
2. BRODIE, E. D., JR. 1968. Investigations on the skin toxin of the adult roughskinned newt, Taricha granulosa. Copeia 1968:307-313.
3. BRODIE, E. D. III, AND E. D. BRODIE, JR. 1990. Tetrodotoxin resistance in garter snakes: an evolutionary response of predators to dangerous prey Evolution 44:651-659.
4. _. 1991. Evolutionary response of predators to dangerous prey: reduction of toxicity of newts and resistance of garter snakes in island populations. Evolution 45:221-224.
5. _. 1999a. Predator-prey arms races. Bioseience 49:557-568.
6. _. 1999b. The cost of exploiting poisonous prey: tradeofffs in a predator-prey arms race. Evolution 53:626-631.
7. BRODIE, E. D., JR., AND P. K. DUCEY. 1991. Antipredator skin secretions of some tropical salamanders (Bolitoglossa) are toxic to snake predators. Biotropica 23:58-62.
8. BRODIE, E. D., JR., AND M. S. TUMBARELLO. 1978. The antipredator functions of Dendrobates auratus (Amphibia, Anura, Dendrobatidae) skin secretion in regard to a snake predator (Thamnophis). Journal of Herpetology 12:264-265
9. BRODIE, E. D., JR., J. L. HENSEL, JR., AND J. A. JOHNSON. 1974. Toxicity of the urodele amphibians Taricha, Notophthalmus, Cyclops and Paramesotriton (Salamandridae). Copeia 1974:506-511.
10. BRODIE, E. D. III, E. D. BRODIE, JR., AND J. E. MOTYCHAK. 2002. Recovery of garter snakes (Thamnophis sirtalis) from the effects of tetrodotoxin. Journal of Herpetology. 36:95-98.
11. BROWER, L. P., J. V. Z. BROWER, AND C. T. COLLINS. 1963. Experimental studies of mimicry. 7. Relative palatability and mullerian mimicry among neotropical butterflies of the subfamily Heliconiiae. Zoologica: New York Zoological Society 48:65-84.
12. DALY, J. W., R. J. HIGHET, AND C. W. MYERS. 1984. Occurence of skin alkaloids in non-dendrobatid frogs from Brazil (Bufonidae), Australia (Myobatrachidae), and Madagascar (Mantellinae). Toxicon 22:905-919.
13. DALY, J. W., C. W. MYERS, AND N. WHITTAKER. 1987. Further classification of skin alkaloids from neotropical poison frogs (Dendrobatidae), with a general survey of toxic, noxious substances in the Amphibia. Toxicon 25:1021-1095.
14. DAWKINS, R., AND J. R. KREBS. 1979. Arms races between and within species. Proceedings of the Royal Society of London B 205:489-511.
15. DUELLMAN, W. E., AND L. TRUEB. 1986. Biology of the Amphibians. McGraw-Hill Book Co., New York, New York, U.S.A.
16. EISNER, T. E. 1966. Beetle's spray discourages predators, Natural History 75:42-47.
17. EISNER, T., M. EISNER, C. ROSSINI, V. K. IYENGARR, B. L. ROACH, E. BENEDIKT, AND J. MEINWALD. 2000. Chemical defense against predation in an insect egg. Proceedings of the National Academy of Sciences 97:1634-1639.
18. FISHER, R. A. 1930. The Genetical Theory of Natural Selection. Oxford University Press, Oxford, U.K.
19. FORMANOWICZ, D. R., JR., AND E. D. BRODIE, JR. 1985. Unpalatability and toxicity of an introduced species (cinnabar moth larvae) to native predators. American Midland Naturalist 133:401-403.
20. GREENE, H. W. 1997. Snakes: the Evolution of Mystery in Nature. University of California Press, Berkeley, California, U.S.A.
21. HANIFIN, C. T., M. YOTSU-YAMASHITA, T. YASUMOTO, E. D. BRODIE III, AND E. D. BRODIE, JR. 1999. Toxicity of dangerous prey: variation of tetrodotoxin levels within and among populations of the newt Taricha granulosa. Journal of Chemical Ecology 25:2161-2175.
22. HANIFIN, C. T., E. D. BRODIE III, AND E. D. BRODIE, JR. 2002. Tetrodotoxin levels of the rough-skin newt, Taricha granulosa, increase in long-term captivity. Toxicon 40:1149-1153.
23. JÄRVI, T., B. SILLIÉN-TULLBERRG, AND C. WIKLUND. 1981. The cost of being aposematic: an experimental study of predation on larvae of Papilio machaon by the great tit Parus major. Oikos 36:267-272.
24. LEIMAR, O., M. ENQUIST, AND B. SILLÉN-TULLBERG. 1986. Evolutionary stability of aposematic coloration and prey unprofitability: a theoretical analysis. American Naturalist 128:469-490.
25. LINDROTH, R. L., G. O. BATZLI, AND S. I. AVILDSEN. 1986. Lespedeza phenolics and Penstemon alkaloids: effects on digestion efficiencies and growth of voles. Journal of Chemical Ecology 12:713-728.
26. LIPKIND, G. M., AND H. A. FOZZARD. 1994. A structural model of the tetrodotoxin and saxitoxin binding site of the Na+ channel. Biophysics Journal 66:1-13.
27. LIZANA, M., AND V. P. MELLADO. 1990. Depradacion por la nutria (Lutra lutra) del sapo de la Sierra Gredos (Bufo bufo gredosicola). Doñana, Acta Vertebrata 17:109-112.
28. MEBS, D. 2001. Toxicity in animals. Trends in evolution? Toxicon 39:87-96.
29. MOSHER, H. S., F. A. FUHRMAN, H. D. BUCHWALD, AND H. G. FISCHER. 1964. Tarichatoxin-tetrodotoxin: a potent neurotoxin. Science 144:1100-1110.
30. MOTYCHAK, J. E., E. D. BRODIE, JR., AND E. D. BRODIE III. 1999. Evolutionary response of predators to dangerous prey: preadaptation and the evolution of tetrodotoxin resistance in garter snakes. Evolution 53:1528-1535.
31. MYERS, C. W., J. W. DALY, AND B. MALKIN. 1978. A dangerously toxic new frog (Phyllobates) used by Emberá Indians of western Columbia, with discussion of blowgun fabrication and dart poisoning. Bulletin of the American Museum of Natural History 161:307-365.
32. NABAHASHI, T., J. W. MOORE, AND R. N. POSTON. 1967. Tetrodotoxin derivatives: chemical structure and blockage of nerve membrane conductance. Science 156:976-978.
33. PETERSON, C. C., B. M. WALTON, AND A. F. BENNETT. 1998. Intrapopulation variation in ecological energetics of the garter snake Thamnophis sirtalis, with analysis of the precision of doubly labeled water measurements. Physiological Zoology 71:333-349.
34. RIDENHOUR, B. J., E. D. BRODIE, JR., AND E. D. BRODIE III. 1999. Effects of repeated injection of tetrodotoxin on growth and resistance to tetrodotoxin in the garter snake Thamnophis sirtalis. Copeia 1999:531-535.
35. RUSSELL, F. E. 1965. Comparative pharmacology of some animal toxins. Federal Proceedings 26:1206-1224.
36. SERVEDIO, M. R. 2000. The effects of predator learning, forgetting, and recognition errors on the evolution of warning coloration. Evolution 54:751-763.
37. SHURE, D. J., L. A. WILSON, AND C. HOCHWENDER. 1989. Predation on aposematic efts of Notophthalmus viridescens. Journal of Herpetology 23:437-439.
38. SIH, A. 1985. Evolution, predator avoidance, and unsuccessful predation. American Naturalist 125:153-157.
39. SPEED, M. P., AND J. R. G. TURNER. 1999. Learning and memory in mimicry: II. Do we understand the mimicry spectrum? Biological Journal of the Linnean Society 67:281-312.
40. THOMPSON, J. N. 1994. The Coevolutionary Process. The University of Chicago Press, Chicago, Illinois, U.S.A.
41. _. 1997. Evaluating the dynamics of coevolution among geographically structured populations. Ecology 78:1619-1623.
42. _. 1999. Coevolution and escalation: are ongoing coevolutionary meanderings important. American Naturalist 153:S92-S93.
43. VERMEIJ, G. J. 1982. Unsuccessful predation and evolution. American Naturalist 120:701-720.
44. _. 1985. Adaptations, effects, and fortuitous survival: comment on a paper by A. Sih. American Naturalist 125:470-472.
45. WAKELY, J. F., G. J. FUHRMAN, F. A. FUHRMAN, H. G. FISCHER, AND H. S. MOSHER. 1966. The occurrence of tetrodotoxin (tarichatoxin) in Amphibia and the distribution of the toxin in the organs of newts (Taricha). Toxicon 3:195-203.
46. WILLIAMS, B. L., E. D. BRODIE, JR., AND E. D. BRODIE III. 2002. Comparisons between toxic effects of tetrodotoxin administered orally and by intraperitoneal injection to the garter snake Thamnophis sirtalis. Journal of Herpetology 36:112-115.
47. YACHI, S., AND M. HIGASHI. 1998. The evolution of warning signals. Nature 394:882-884.
48. YOTSU-YAMASHITA, M., AND D. MEBS. 2001. The levels of tetrodotoxin and its analogue 6-epitetrodotoxin in the red-spotted newt, Notophthalmus viridescens. Toxicon 39:1261-1263.