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Chemoecology

, Volume 22, Issue 3, pp 179–185 | Cite as

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

  • Becky L. WilliamsEmail author
  • Charles T. Hanifin
  • Edmund D. BrodieJr.
  • Edmund D. BrodieIII
Research Paper

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.

Keywords

Tetrodotoxin TTX Thamnophis sirtalis Taricha granulosa Coevolution Sequester 

Notes

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.

References

  1. Arnold SJ (1993) Foraging theory and prey-size-predator-size relations in snakes. In: Seigal RA, Collins JT (eds) Snakes: ecology and behavior. McGraw-Hill, Inc., USA, pp 87–115Google Scholar
  2. Avila C (1995) Natural products of opisthobranch molluscs: a biological review. Oceanogr Mar Biol Annu Rev 33:487–559Google Scholar
  3. Brodie ED Jr (1968) Investigations on the skin toxin of the adult rough-skinned newt, Taricha granulosa. Copeia 1968:307–313CrossRefGoogle Scholar
  4. Brodie ED III, Brodie ED Jr (1990) Tetrodotoxin resistance in garter snakes: an evolutionary response of predators to dangerous prey. Evolution 44:651–659CrossRefGoogle Scholar
  5. Brodie ED III, Brodie ED Jr (1991) Evolutionary response of predators to dangerous prey—reduction of toxicity of newts and resistance of garter snakes in island populations. Evolution 45:221–224CrossRefGoogle Scholar
  6. Brodie ED III, Brodie ED Jr (1999a) Predator–prey arms races. Bioscience 49:557–568CrossRefGoogle Scholar
  7. Brodie ED III, Brodie ED Jr (1999b) The cost of exploiting poisonous prey: evolutionary tradeoffs in a predator–prey arms race. Evolution 53:626–631CrossRefGoogle Scholar
  8. Brodie ED Jr, Ducey PK (1991) Antipredator skin secretions of some tropical salamanders (Bolitoglossa) are toxic to snake predators. Biotropica 23:58–62CrossRefGoogle Scholar
  9. Brodie ED III, Brodie ED Jr, Motychak JE (2002a) Recovery of garter snakes (Thamnophis sirtalis) from the effects of tetrodotoxin. J Herpetol 36:95–98CrossRefGoogle Scholar
  10. Brodie ED Jr, Ridenhour BJ, Brodie ED III (2002b) The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts. Evolution 56:2067–2082PubMedGoogle Scholar
  11. Brodie ED III, Feldman CR, Hanifin CT, Motychak JE, Mulcahy DG, Williams BL, Brodie ED Jr (2005) Evolutionary response of predators to dangerous prey: parallel arms races between garter snakes and newts involving tetrodotoxin as the phenotypic interface of coevolution. J Chem Ecol 31:343–355PubMedCrossRefGoogle Scholar
  12. Brouillette AN (2008) Sex-biased predation on Taricha by a novel predator in Annadel State Park. Thesis, Utah State UniversityGoogle Scholar
  13. Cimino G, Fontana A, Gavagnin M (1999) Marine opisthobranch molluscs: chemistry and ecology in sacoglossans and dorids. Curr Org Chem 3:327–372Google Scholar
  14. Cott HB (1940) Adaptive coloration in animals. Methuen & Co., LondonGoogle Scholar
  15. Daly JW, Myers CW, Whittaker N (1987) Further classification of skin alkaloids from neotropical poison frogs (Dendrobatidae), with a general survey of toxic, noxious substances in the amphibia. Toxicon 25:1021–1095CrossRefGoogle Scholar
  16. Daly JW, Garaffo HM, Spande TF, Jaramillo C, Rand AS (1994) Dietary source for skin alkaloids of poison frogs (Dendrobatidae)? J Chem Ecol 20:943–955CrossRefGoogle Scholar
  17. Derby CD (2007) Escape by inking and secreting: marine molluscs avoid predators through a rich array of chemicals and mechanisms. Biol Bull 213:274–289PubMedCrossRefGoogle Scholar
  18. Dumbacher JP, Wako A, Derrickson SR, Samuelson A, Spande TF, Daly JW (2004) Melyrid beetles (Choresine): a putative source for the batrachotoxin alkaloids found in poison-dart frogs and toxic passerine birds. Proc Natl Acad Sci USA 101:15857–15860PubMedCrossRefGoogle Scholar
  19. Edgehouse MJ (2008) Garter snake (Thamnophis) natural history: food habits and interspecific aggression. Dissertation, Utah State UniversityGoogle Scholar
  20. Feldman CR, Brodie ED Jr, Brodie ED III, Pfrender ME (2009) The evolutionary origins of beneficial alleles during the repeated adaptation of garter snakes to deadly prey. Proc Natl Acad Sci USA 106:13415–13420PubMedCrossRefGoogle Scholar
  21. Fitch HS (1965) An ecological study of the garter snake Thamnophis sirtalis. Univ Kansas Publ Mus Nat Hist 15:493–564Google Scholar
  22. Fozzard HA, Lipkind GM (2010) The tetrodotoxin binding site. Mar Drugs (submitted)Google Scholar
  23. Gamberale-Stille G, Guilford T (2003) Contrast versus colour in aposematic signals. Anim Behav 65:1021–1026CrossRefGoogle Scholar
  24. Geffeney S, Ruben PC, Brodie ED Jr, Brodie ED III (2002) Mechanisms of adaptation in a predator–prey arms race: TTX-resistant sodium channels. Science 297:1336–1339PubMedCrossRefGoogle Scholar
  25. Geffeney SL, Fujimoto E, Brodie ED III, Brodie ED Jr, Ruben PC (2005) Evolutionary diversification of TTX-resistant sodium channels in a predator–prey interaction. Nature 434:759–763PubMedCrossRefGoogle Scholar
  26. Glass JK (1972) Feeding behavior of the western shovel-nosed snake, Chionactis occipitalis klauberi, with special reference to scorpions. Southwest Nat 16:445–447CrossRefGoogle Scholar
  27. Greene RR, Feldman CR (2009) Thamnophis atratus atratus diet. Herpetol Rev 40:103–104Google Scholar
  28. Gregory PT, Nelson KJ (1991) Predation on fish and intersite variation in the diet of common garter snakes, Thamnophis sirtalis, on Vancouver Island. Can J Zool 69:988–994CrossRefGoogle Scholar
  29. Hanifin CT, Yotsu-Yamashita M, Yasumoto T, Brodie ED III, Brodie ED Jr (1999) Toxicity of dangerous prey: variation of tetrodotoxin levels within and among populations of the newt Taricha granulosa. J Chem Ecol 25:2161–2175CrossRefGoogle Scholar
  30. Hanifin CT, Brodie ED Jr, Brodie ED III (2008) Phenotypic mismatches reveal escape from arms-race coevolution. Public Libr Sci Biol 6:e60Google Scholar
  31. Hanson JA, Vial JL (1956) Defensive behavior and effects of toxins in Bufo alvarius. Herpetologica 12:141–149Google Scholar
  32. Hille B (2001) Ion channels of excitable membranes. Sinauer Associates, SunderlandGoogle Scholar
  33. Hutchinson DA, Mori A, Savitzky AH, Burghardt GM, Wu X, Meinwald J, Schroeder FC (2007) Dietary sequestration of defensive steroids in nuchal glands of the Asian snake Rhabdophis tigrinus. Proc Natl Acad Sci USA 104:2265–2270PubMedCrossRefGoogle Scholar
  34. Hutchinson DA, Savitzky AH, Mori A, Meinwald J, Schroeder FC (2008) Maternal provisioning of sequestered defensive steroids by the Asian snake Rhabdophis tigrinus. Chemoecology 18:181–190CrossRefGoogle Scholar
  35. Hutchinson DA, Savitzky AH, Mori A, Burghardt GM, Meinwald J, Schroeder FC (2011) Chemical investigations of defensive steroid sequestration by the Asian snake Rhabdophis tigrinus. Chemoecology. doi: 10.1007/s00049-011-0078-2
  36. Jost MC, Hillis DM, Lu Y, Kyle JW, Fozzard HA, Zakon HH (2008) Toxin-resistant sodium channels: parallel adaptive evolution across a complete gene family. Mol Biol Evol 25:1016–1024PubMedCrossRefGoogle Scholar
  37. Kao CY (1966) Tetrodotoxin, saxitoxin, and their significance in the study of excitation phenomena. Pharmacol Rev 18:997–1049PubMedGoogle Scholar
  38. Kao CY, Levinson SR (1986) Tetrodotoxin, saxitoxin, and the molecular biology of the sodium channel. New York Academy of Sciences, New YorkGoogle Scholar
  39. Lee P, Ruben PC (2010) The biophysical costs associated with tetrodotoxin resistance in the garter snake, Thamnophis sirtalis. Mar Drugs (submitted)Google Scholar
  40. Lizana M, Mellado VP (1990) Depradacion por la nutria (Lutra lutra) del sapo de la Sierra Gredos (Bufo bufo gredosicola). Doñana, Acta Vertebr 17:109–112Google Scholar
  41. Llewelyn JS, Phillips BL, Shine R (2009) Sublethal costs associated with the consumption of toxic prey by snakes. Austral Ecol 34:179–184Google Scholar
  42. Maruta S, Yamaoka K, Yotsu-Yamashita M (2008) Two critical residues in p-loop regions of puffer fish Na+ channels on TTX sensitivity. Toxicon 51:381–387PubMedCrossRefGoogle Scholar
  43. Matsui T, Yamamori K, Furukawa K, Kono M (2000) Purification and some properties of a tetrodotoxin binding protein from the blood plasma of kusafugu, Takifugu niphobles. Toxicon 38:463–468PubMedCrossRefGoogle Scholar
  44. Matsumoto T, Nagashima Y, Takayama K, Shimakura K, Shiomi K (2005) Difference between tetrodotoxin and saxitoxins in accumulation in puffer fish Takifugu rubripes liver tissue slices. Fish Physiol Biochem 31:95–100Google Scholar
  45. Matsumoto T, Nagashima Y, Kusuhara H, Sugiyama Y, Ishizaki S, Shimakura K, Shiomi K (2007) Involvement of carrier-mediated transport system in uptake of tetrodotoxin into liver tissue slices of puffer fish Takifugu rubripes. Toxicon 50:173–179PubMedCrossRefGoogle Scholar
  46. McAllister KR, Skriletz J, Hall B, Garner MM (1997) Taricha granulosa (roughskin newt) toxicity. Herpetol Rev 28:82Google Scholar
  47. Medinsky MA, Klaassen CD (1996) Toxicokinetics. In: Klaassen CD (ed) Casarett and Doull’s toxicology: the basic science of poisons. McGraw Hill Companies, Inc., New York, pp 187–198Google Scholar
  48. Miller N (1909) The American toad. Am Nat 43:641–688; 730–745Google Scholar
  49. Mobley JA, Stidham TA (2000) Great horned owl death from predation of a toxic California newt. Wilson Bull 112:563–564CrossRefGoogle Scholar
  50. Mochida K (2009) A parallel geographical mosaic of morphological and behavioural aposematic traits of the newt, Cynops pyrrhogaster (Urodela: Salamandridae). Biol J Linn Soc 97:613–622CrossRefGoogle Scholar
  51. Mochida K, Matsui K (2007) Counter-defense technique to mitigate prey toxicity in raccoons (Procyon lotor). Mamm Study 32:135–138CrossRefGoogle Scholar
  52. Mori A, Burghardt GM (2008) Comparative experimental tests of natricine antipredator displays, with special reference to the apparently unique displays in the Asian genus, Rhabdophis. J Ethol 26:61–68CrossRefGoogle Scholar
  53. Mori A, Moriguchi H (1988) Food habits of snakes in Japan: a critical review. Snake 20:98–113Google Scholar
  54. Mori A, Burghardt GM, Savitzky AH, Roberts KA, Hutchinson DA, Goris RC (2011) Nuchal glands: a novel defensive system in snakes. Chemoecology. doi: 10.1007/s00049-011-0086-2
  55. Mosher HS, Fuhrman FA, Buchwald HD, Fischer HG (1964) Tarichatoxin—tetrodotoxin: a potent neurotoxin. Science 144:1100–1110PubMedCrossRefGoogle Scholar
  56. Myers CW, Daly JW, Malkin B (1978) A dangerously toxic new frog (Phyllobates) used by Ember′a Indians of western Columbia, with discussion of blowgun fabrication and dart poisoning. Bull Am Mus Nat Hist 161:307–365Google Scholar
  57. Nagashima Y, Toyoda M, Hasobe M, Shimakura K, Shiomi K (2003) In vitro accumulation of tetrodotoxin in puffer liver tissue slices. Toxicon 41:569–574PubMedCrossRefGoogle Scholar
  58. Nakamura K (1935) On a new integumental poison gland found in the nuchal region of a snake, Natrix tigrina. Mem Coll Sci Kyoto Imp Univ 10B:229–240Google Scholar
  59. Norris KS, Kavanau JL (1966) The burrowing of the western shovel-nosed snake, Chionactis occipitalis, and the undersand environment. Copeia 4:650–664CrossRefGoogle Scholar
  60. Ogura Y (1958) Some recent problems on fugu-toxin, particularly on crystalline tetrodotoxin. Seitai No Kagaku 9:281–287Google Scholar
  61. Opitz SEW, Müller C (2009) Plant chemistry and insect sequestration. Chemoecology 19:117–154CrossRefGoogle Scholar
  62. Phillips B, Shine R (2007) When dinner is dangerous: toxic frogs elicit species-specific responses from a generalist snake predator. Am Nat 170:936–942PubMedCrossRefGoogle Scholar
  63. Roper TJ (1990) Responses of domestic chicks to artificially coloured insect prey: effects of previous experience and background colour. Anim Behav 39:466–473CrossRefGoogle Scholar
  64. Saporito RA, Spande TF, Garraffo HM, Donnelly MA (2009) Arthropod alkaloids in poison frogs: a review of the ‘dietary hypothesis’. Heterocycles 79(1):277–297CrossRefGoogle Scholar
  65. Saporito RA, Donnelly MA, Spande TF, Garraffo HM (2011) A review of chemical ecology in poison frogs. Chemoecology. doi: 10.1007/s00049-011-0088-0
  66. Schaaf RT, Garton JS (1970) Raccoon predation on the American Toad, Bufo americanus. Herpetologica 26:334–335Google Scholar
  67. Shine R, Olsson MM, Lemaster MP, Moore IT, Mason RT (2000) Effects of sex, body size, temperature, and location on the antipredator tactics of free-ranging gartersnakes (Thamnophis sirtalis, Colubridae). Behav Ecol 11:239–245CrossRefGoogle Scholar
  68. Shure DJ, Wilson LA, Hochwender C (1989) Predation on aposematic efts of Notophthalmus viridescens. J Herpetol 23:437–439CrossRefGoogle Scholar
  69. Smith HM, White FN (1955) Adrenal enlargement and its significance in the hognose snakes (Heterodon). Herpetologica 11:137–144Google Scholar
  70. Toledo RC, Jared C (1995) Cutaneous granular glands and amphibian venoms. Comp Biochem Physiol 111A:1–29CrossRefGoogle Scholar
  71. Westphal MF, O’Donnell RP (2007) Startle patterns versus aposematism: a study of color pattern variation in garter snakes, genus Thamnophis. In: Westphal MF (ed) On the evolution of correlated color traits in garter snakes. Dissertation, Oregon State UniversityGoogle Scholar
  72. Williams BL, Brodie ED Jr, Brodie ED III (2002) Comparisons between toxic effects of tetrodotoxin administered orally and by intraperitoneal injection to the garter snake Thamnophis sirtalis. J Herpetol 36:112–115Google Scholar
  73. Williams BL, Brodie ED Jr, Brodie ED III (2003) Coevolution of deadly toxins and predator resistance: self-assessment of resistance by garter snakes leads to behavioral rejection of toxic newt prey. Herpetologica 59:155–163CrossRefGoogle Scholar
  74. Williams BL, Brodie ED Jr, Brodie ED III (2004) A resistant predator and its toxic prey: persistence of newt toxin leads to poisonous (not venomous) snakes. J Chem Ecol 30:1901–1919PubMedCrossRefGoogle Scholar
  75. Wiseman KD, Pool AC (2007) Thamnophis couchii (Sierra garter snake): predator–prey interaction. Herpetol Rev 38:344Google Scholar
  76. Wright JW (1966) Predation on the Colorado river toad, Bufo alvarius. Herpetologica 22:127–128Google Scholar
  77. Yoshida S (1994) Tetrodotoxin-resistant sodium channels. Cell Mol Neurobiol 14:227–243PubMedCrossRefGoogle Scholar
  78. Yotsu M, Endo A, Yasumoto T (1989) An improved tetrodotoxin analyzer. Agric Biol Chem 53:893–895CrossRefGoogle Scholar
  79. Yotsu M, Iorizzi M, Yasumoto T (1990) Distribution of tetrodotoxin, 6-epitetrodotoxin, and 11-deoxytetrodotoxin in newts. Toxicon 28:238–241PubMedCrossRefGoogle Scholar

Copyright information

© Springer Basel AG 2011

Authors and Affiliations

  • Becky L. Williams
    • 1
    Email author
  • Charles T. Hanifin
    • 2
  • Edmund D. BrodieJr.
    • 3
  • Edmund D. BrodieIII
    • 4
  1. 1.Department of BiologyUtah State UniversityVernalUSA
  2. 2.Hopkins Marine StationStanford UniversityPacific GroveUSA
  3. 3.Department of BiologyUtah State UniversityLoganUSA
  4. 4.Mountain Lake Biological Station and Department of BiologyUniversity of VirginiaCharlottesvilleUSA

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