Skip to main content
SpringerLink
Log in

Garter snakes do not respond to TTX via chemoreception

  • Short Communication
  • Published:
Chemoecology Aims and scope Submit manuscript

Abstract

Snakes detect and recognize prey through chemoreception using their tongue, but can they also detect toxins secreted by prey? Taste-rejection has been described in predators as a means of sampling prey for toxicity prior to ingestion but at the cost of minor intoxication and energy expenditure. Toxin detection prior to attack of prey might reduce these costs. Thamnophis sirtalis (common garter snake) is among the predators that have been shown to employ taste-rejection of toxic prey but, as with all snakes, they primarily use vomeronasal chemoreception to evaluate potential prey. We investigated whether T. sirtalis use chemoreception as means of perceiving tetrodotoxin (TTX) found in their newt prey. We used the common tongue-flick behavioral assay to evaluate response to TTX and found that naïve T. sirtalis did not respond differently to the toxin than a control. We conclude that T. sirtalis cannot detect TTX by chemoreception, or do not alter their behavior if they do.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

References

  • Arnold SJ (1981a) Behavioral variation in natural populations 1. Phenotypic, genetic and environmental correlations between chemoreceptive responses to prey in the garter snake, Thamnophis-elegans. Evolution 35(3):489–509

    Article  Google Scholar 

  • Arnold SJ (1981b) Behavioral variation in natural populations 2 The inheritance of a feeding response in crosses between geographic races of the garter snake, Thamnophis-elegans. Evolution 35(3):510–515

    Article  Google Scholar 

  • Arnold SJ (1981c) The microevolution of feeding behavior. In: Kamil AC, Sargent TD (eds) Foraging behavior: ecological ethological and psychological approaches. Garland Publishing, New York, pp 409–514

    Google Scholar 

  • Bernasconi ML, Turlings TCJ, Ambrosetti L, Bassetti P, Dorn S (1998) Herbivore-induced emissions of maize volatiles repel the corn leaf aphid, Rhopalosiphum maidis. Entomol Exp Appl 87(2):133–142

    Article  CAS  Google Scholar 

  • Brodie ED Jr (1968) Investigations on the skin toxin of the adult rough-skinned newt, Taricha granulosa. Copeia 1968:307–313

    Article  Google Scholar 

  • Brodie ED III, Brodie ED Jr (1990) Tetrodotoxin resistance in garter snakes: an evolutionary response of predators to dangerous prey. Evolution 44(3):651–659

    Article  Google Scholar 

  • 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(1):221–224

    Article  Google Scholar 

  • Brodie ED III, Brodie ED Jr (1999) Predator-prey arms races. Bioscience 49(7):557–568

    Article  Google Scholar 

  • Brodie ED Jr, Hensel JL, Johnson JA (1974) Toxicity of urodele amphibians taricha, Notophthalmus, Cynops and Paramesotriton (Salamandridae). Copeia 1974(2):506–511

  • Brodie ED III, Ridenhour BJ, Brodie ED Jr (2002) The evolutionary response of predators to dangerous prey: hotspots and coldspots in the geographic mosaic of coevolution between garter snakes and newts. Evolution 56(10):2067–2082

    PubMed  Google Scholar 

  • Brower LP, Calvert WH (1985) Foraging dynamics of bird predators on overwintering Monarch butterflies in Mexico. Evolution 39(4):852–868

    Article  Google Scholar 

  • Burghardt GM (1966) Stimulus control of the prey attack response in naïve garter snakes. Psychonomic Science 4:37–38

    Google Scholar 

  • Burghardt GM (1969) Comparative pre-attack studies in newborn snakes of the genus Thamnophis. Behaviour 33:77–114

    Article  Google Scholar 

  • Burghardt GM (1970a) Chemical perception in reptiles. In: Johnston JW, Moulton DG, Turk A (eds) Advances in chemoreception, Communication by chemical signals, vol 1 Appleton-Century-Crofts, New York, pp 241–308

  • Burghardt GM (1970b) Intraspecific geographical variation in chemical food cue preferences of newborn garter snakes (Thamnophis sirtalis). Behaviour 36:246–257

    Article  Google Scholar 

  • Burghardt GM (1971) Chemical-cue preferences of newborn snakes: influence of prenatal maternal experience. Science 171(3974):921–923

    Article  PubMed  CAS  Google Scholar 

  • Burghardt GM (1980) Behavioral and stimulus correlates of vomeronasal functioning in reptiles: feeding, grouping, sex, and tongue use. In: Mfiller-Schwarze D, Silverstein RM (eds) Chemical signals in vertebrates and aquatic invertebrates. Plenum Press, New York, pp 275–301

    Google Scholar 

  • Burghardt GM (1992) Prior exposure to prey cues influences chemical prey preference and prey choice in neonatal garter snakes. Anim Behav 44(4):787–789

    Article  Google Scholar 

  • Burghardt GM (1993) The comparative imperative: genetics and ontogeny of chemoreceptive prey responses in natricine snakes. Brain Behav Evol 41(3–5):138–146

    Article  PubMed  CAS  Google Scholar 

  • Burghardt GM, Pruitt CH (1975) Role of tongue and senses in feeding of naive and experienced garter snakes. Physiol Behav 14(2):185–194

    Article  PubMed  CAS  Google Scholar 

  • Burghardt GM, Goss SE, Schell FM (1988) Comparison of earthworm-derived and fish-derived chemicals eliciting prey attack by garter snakes (Thamnophis). J Chem Ecol 14(3):855–881

    Article  CAS  Google Scholar 

  • Busch KL (1995) Desorption ionization mass-spectrometry. J Mass Spectrom 30(2):233–240

    Article  CAS  Google Scholar 

  • Cooper WE (2007) Elevated tongue-flicking rate to cricket surface chemicals by the arthropodivorous rough green snake Opheodrys aestivus. Amphib Reptil 28(3):413–417

    Article  Google Scholar 

  • Cooper WE, Burghardt GM (1990a) A comparative-analaysis of scoring methods for chemical-descrimination of prey by squamate reptiles. J Chem Ecol 16(1):45–65

    Article  Google Scholar 

  • Cooper WE, Burghardt GM (1990b) Vomerolfaction and vomodor. J Chem Ecol 16(1):103–105

    Article  Google Scholar 

  • Cooper WE, Secor S (2007) Strong response to anuran chemical cues by an extreme dietary specialist, the eastern hog-nosed snake (Heterodon platirhinos). Can J Zool-Rev Can Zool 85(5):619–625. doi:10.1139/z07-041

    Article  Google Scholar 

  • Cooper WE, Perez-Mellado V, Vitt LJ, Budzinsky B (2002) Behavioral responses to plant toxins by two omnivorous lizard species. Physiol Behav 76(2):297–303

    Article  PubMed  CAS  Google Scholar 

  • Delphia CM, Mescher MC, De Moraes CM (2007) Induction of plant volatiles by herbivores with different feeding habits and the effects of induced defenses on host-plant selection by thrips. J Chem Ecol 33(5):997–1012

    Article  PubMed  CAS  Google Scholar 

  • Drummond H (1983) Aquatic foraging in garter snakes: a comparison of specialists and generalist. Behaviour 86:1–30. doi:10.1163/156853983x00543

    Article  Google Scholar 

  • Drummond H (1985) The role of vision in the predatory behavior of natricine snakes. Anim Behav 33 (FEB):206–215. doi:10.1016/s0003-3472(85)80134-2

  • 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(32):13415–13420. doi:10.1073/pnas.0901224106

    Google Scholar 

  • Fuchs JL, Burghardt GM (1971) Effects of early feeding experience on the responses of garter snakes to food chemicals. Learn Motiv 2(3):271–279

    Article  Google Scholar 

  • Geffeney S, Brodie ED Jr, Ruben PC, Brodie ED III (2002) Mechanisms of adaptation in a predator-prey arms race: TTX-resistant sodium channels. Science 297(5585):1336–1339

    Article  PubMed  CAS  Google Scholar 

  • 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(7034):759–763

    Article  PubMed  CAS  Google Scholar 

  • Halpern M (1983) Nasal chemical senses in snakes. In: Ewert JP, Capranica RR, Ingle DJ (eds) Advances in vertebrate neuroethology. Plenum Press, New York

    Google Scholar 

  • Halpern M (1992) Nasal chemical senses in reptiles: structure and function. In: Gans C, Crews D (eds) Biology of the reptilia, vol 18. pp 423–523

  • Hanifin CT, Yotsu-Yamashita M, Yasumoto T, Brodie ED Jr, Brodie ED III (1999) Toxicity of dangerous prey: variation of tetrodotoxin levels within and among populations of the newt Taricha granulosa. J Chem Ecol 25(9):2161–2175

    Article  CAS  Google Scholar 

  • Hanifin CT, Brodie ED Jr, Brodie ED III (2008) Phenotypic mismatches reveal escape from arms-race coevolution. PLoS Biol 6(3):471–482. doi:e6010.1371/journal.pbio.0060060

    Article  CAS  Google Scholar 

  • How CK, Chern CH, Huang YC, Wang LM, Lee CH (2003) Tetrodotoxin poisoning. Am J Emerg Med 21(1):51–54. doi:10.1053/ajem.2003.50008

    Article  PubMed  Google Scholar 

  • Kao CY (1966) Tetrodotoxin, saxitoxin, and their significance in the study of excitation phenomena. Pharmacol Rev 18:997–1049

    PubMed  CAS  Google Scholar 

  • Lange WR (1990) Puffer fish poisoning. Am Fam Physician 42(4):1029–1033

    PubMed  CAS  Google Scholar 

  • Langham GM (2006) Rufous-tailed jacamars and aposematic butterflies: do older birds attack novel prey? Behav Ecol 17(2):285–290. doi:10.1093/beheco/arj027

    Article  Google Scholar 

  • Lindquist N (1996) Palatability of invertebrate larvae to corals and sea anemones. Mar Biol 126(4):745–755

    Article  Google Scholar 

  • Lipkind GM, Fozzard HA (1994) A structural model of the tetrodotoxin and saxitoxin binding-site of the Na+ channel. Biophys J 66(1):1–13

    Article  PubMed  CAS  Google Scholar 

  • Mebs D, Arakawa O, Yotsu-Yamashita M (2010) Tissue distribution of tetrodotoxin in the red-spotted newt Notophthalmus viridescens. Toxicon 55(7):1353–1357. doi:10.1016/j.toxicon.2010.02.009

    Article  PubMed  CAS  Google Scholar 

  • Mosher H, Fuhrman F, Bichwald H, Fischer H (1964) Tarichatoxin-tetrodotoxin: a potent neurotoxin. Science 144:1100–1110

    Article  PubMed  CAS  Google Scholar 

  • Motychak JE, Brodie ED Jr, Brodie ED III (1999) Evolutionary response of predators to dangerous prey: preadaptation and the evolution of tetrodotoxin resistance in garter snakes. Evolution 53(5):1528–1535

    Article  Google Scholar 

  • Narahashi T, Moore JW, Poston RN (1967) Tetrodotoxin derivatives: chemical structure and blockage of nerve membrane conductance. Science 156:976–978

    Article  PubMed  CAS  Google Scholar 

  • Schwenk K (1995) Of tongues and noses: chemoreception in lizards and snakes. Trends Ecol Evol 10(1):7–12

    Article  PubMed  CAS  Google Scholar 

  • Sheffield LP, Law JM, Burghard GM (1968) On the nature of chemical food sign stimuli for newborn garter snakes. Commun Behav Biol 2:7–12

    Google Scholar 

  • Sillén-Tullberg B (1985) Higher survival of an aposematic than of a cryptic form of a distasteful bug. Oecologia 67(3):411–415

    Article  Google Scholar 

  • Sims JK, Ostman DC (1986) Pufferfish poisoning: emergency diagnosis and management of mild human tetrodotoxication. Ann Emerg Med 15(9):1094–1098

    Article  PubMed  CAS  Google Scholar 

  • Skelhorn J, Rowe C (2006) Taste-rejection by predators and the evolution of unpalatability in prey. Behav Ecol Sociobiol 60(4):550–555. doi:10.1007/s00265-006-0199-8

    Article  Google Scholar 

  • Skelhorn J, Rowe C (2009) Distastefulness as an antipredator defence strategy. Anim Behav 78(3):761–766. doi:10.1016/j.anbehav.2009.07.006

    Article  Google Scholar 

  • Sun K, Wat J, So P (1994) Puffer fish poisoning. Anaesth Intensive Care 22(3):307–308

    PubMed  CAS  Google Scholar 

  • Tubaro A, Hungerford J (2007) Toxicology of marine toxins. In: Gupta RC (ed) Veterinary toxicology: basic and clinical principles. Elsevier, Oxford, pp 725–752

    Google Scholar 

  • Wakely JF, Fuhrman GJ, Fuhrman FA, Fischer HG, Mosher HS (1966) The occurrence of tetrodotoxin (tarichatoxin) in Amphibia and the distribution of the toxin in the organs of newts (Taricha). Toxicon 3:195–203

    Article  PubMed  CAS  Google Scholar 

  • Wiklund C, Jarvi T (1982) Survival of distasteful insects after being attacked by naive birds: a reappraisal of the theory of aposematic coloration evolving through individual selection. Evolution 36(5):998–1002

    Article  Google Scholar 

  • 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(1):112–115

    Google Scholar 

  • 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(2):155–163

    Article  Google Scholar 

  • Williams BL, Hanifin CT, Brodie ED Jr, Brodie ED III (2010) Tetrodotoxin affects survival probability of rough-skinned newts (Taricha granulosa) faced with TTX-resistant garter snake predators (Thamnophis sirtalis). Chemoecology 20(4):285–290. doi:10.1007/s00049-010-0057-z

    Article  CAS  Google Scholar 

  • Yotsu M, Iorizzi M, Yasumoto T (1990) Distribution of tetrodotoxin, 6-epitetrodotoxin, and 11-deoxytetrodotoxin in newts. Toxicon 28(2):238–241

    Article  PubMed  CAS  Google Scholar 

  • Yotsu-Yamashita M, Mebs D (2001) The levels of tetrodotoxin and its analogue 6-epitetrodotoxin in the red-spotted newt, Notophthalmus viridescens. Toxicon 39(8):1261–1263

    Article  PubMed  CAS  Google Scholar 

  • Yotsu-Yamashita M, Mebs D (2003) Occurrence of 11-oxotetrodotoxin in the red-spotted newt, Notophthalmus viridescens, and further studies on the levels of tetrodotoxin and its analogues in the newt’s efts. Toxicon 41(7):893–897

    Article  PubMed  CAS  Google Scholar 

  • Yotsu-Yamashita M, Mebs D, Kwet A, Schneider M (2007) Tetrodotoxin and its analogue 6-epitetrodotoxin in newts (Triturus spp.; Urodela, Salamandridae) from southern Germany. Toxicon 50(2):306–309

    Article  PubMed  CAS  Google Scholar 

  • Young BA (1997) On the absence of taste buds in monitor lizards (Varanus) and snakes. J Herpetol 31(1):130–137

    Article  Google Scholar 

Download references

Acknowledgments

The authors would like to thank John Chuckalovcak, Charles Hanifin, and Shana Geffeney for helpful advice on this project. They would also like to thank the Brodie Lab and the graduate student writing group for helpful comments on earlier drafts of this manuscript. Comments from two anonymous reviewers on an earlier version of this manuscript were very helpful. They are most grateful to the Mountain Lake Biological Station, University of Virginia for allowing them to obtain animals from their site and to the University of Virginia for allowing them space to maintain the animals as well as approving the protocols necessary to conduct this research. This investigation was approved by the ACUC (protocol #3567 08 09) and the Institutional Biosafety Committee (protocol #405-06). Funding for this research was provided by the National Science Foundation (NSF-DEB 0922216 to EDBIII).

Author information

Authors and Affiliations

  1. Department of Biology, University of Virginia, Charlottesville, VA, 22904, USA

    Leleña A. Avila, Ryan Wiggins & Edmund D. Brodie III

  2. Mountain Lake Biological Station, University of Virginia, Pembroke, VA, 24136, USA

    Leleña A. Avila & Edmund D. Brodie III

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

    Edmund D. Brodie Jr.

Authors
  1. Leleña A. Avila
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ryan Wiggins
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edmund D. Brodie Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Edmund D. Brodie III
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Leleña A. Avila.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Avila, L.A., Wiggins, R., Brodie, E.D. et al. Garter snakes do not respond to TTX via chemoreception. Chemoecology 22, 263–268 (2012). https://doi.org/10.1007/s00049-011-0094-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00049-011-0094-2

Keywords

Search

Navigation