Chemosensory Responses of Salamanders to Snake Odors

Flight, Freeze, and Dissociation
  • Dale M. Madison
  • John C. Maerz
  • James H. McDarby

Abstract

Some prey species avoid predators using flight or freeze responses, while some may show either response depending on the ecological context. Consequently, predator avoidance may be risk-sensitive, and the level of activity may be an important risk-specific component of the avoidance response. Red-backed salamanders, Plethodon cinereus, were exposed at times of low risk (night) and high risk (day) to the substrate odors of predatory garter snakes (Thamnophis sirtalis) maintained on low risk (goldfish) and high risk (redbacked salamander) diets. Salamanders maximally avoided snake odors over blank substrates in all except the lowest risk treatment, which was not avoided, and thus they appeared to show a threshold (all or none) response to snake odors. However, the concurrent activity level of the salamander (degree of movement during avoidance) showed small scale increases with each risk increment from the lowest risk treatment (goldfish diet at night) to the highest risk treatment (salamander diet during day). There was no evidence of a freeze response during predator avoidance. Partial ”dissociation” of avoidance and activity at night, i.e. no change in avoidance with a change in activity level, or vice versa, is discussed in the context of the biology of P. cinereus. Future studies of predator avoidance behavior should closely examine prey activity for clues to the diversity and intensity of risks that ultimately shape predator avoidance.

Keywords

Urea Dehydration Turkey Odour Broome 

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References

  1. Arnold, S. 1978. Some effects of early experience on feeding responses in the common garter snake, Thamnophis sirtalis. Anim. Behav., 26, 455–462.CrossRefGoogle Scholar
  2. Alexander, J. E, Jr. & Covich, A. P. 1991. Predator avoidance by the freshwater snail Physella virgata in response to the crayfish Procambarus simulans. Oecologia, 87, 435–442.CrossRefGoogle Scholar
  3. Burghardt, G. M. 1990. Chemically mediated predation in vertebrates: diversity, ontogeny and information. In: Chemical Signals in Vertebrates 5 (Ed. by D.W. Macdonald, D. Muller-Schwarze & S. E. Natynczuk), pp 475–499. New York: Oxford Univ. Press.Google Scholar
  4. Brandon, R. A. & Huheey, J. E. 1975. Diurnal activity, avian predation, and the question of warning coloration and cryptic coloration in salamanaders. Herpetol, 31, 252–255.Google Scholar
  5. Brodie E. D.,Jr. & Brodie, E. D. III. 1980. Differential avoidance of mimetic salamanders by free-ranging birds. Science, 208, 181–183.PubMedCrossRefGoogle Scholar
  6. Brodie E. D., Jr., Formanowicz, D. R. Jr. & Brodie E. D., III. 1991. Predator avoidance and antipredator mechanisms: distinct pathways to survival. Ethol. Ecol. & Evol, 3, 73–77.CrossRefGoogle Scholar
  7. Brodie E. D., Jr., Johnson J. A., & Dodd C. K., Jr. 1974. Immobility as a defensive behavior in salamanders. Herpetol, 30, 79–85.Google Scholar
  8. Carpenter, C.C. 1952. Comparative ecology of the common garter snake (Thamnophis s. sirtalis), the ribbon snake (Thamnophis s. sauritus), and Butler’s garter snake (Thamnophis butleri) in mixed populations. Ecol. Monogr., 22, 235–258.CrossRefGoogle Scholar
  9. Coker, C.M. 1931. Hermit thrush feeding on salamanders. Auk, 48, 277.CrossRefGoogle Scholar
  10. Drummond, H. 1985. The role of vision in the predatory behaviour of natricine snakes. Anim. Behav., 33, 206–215.CrossRefGoogle Scholar
  11. Ford, N. B. 1986. The role of pheromone trails in the sociobiology of snakes. In: Chemical Signals in Vertebrates (Ed. by D. Duvall, D. Muller-Schwarze & R. M. Silverstein), pp. 261–278. New York: Plenum.CrossRefGoogle Scholar
  12. Fuchs J. L., & G. M. Burghardt. 1971. Effects of early feeding experience on the responses of garter snakes to food chemicals. Learn. and Motiv., 2, 271–279.CrossRefGoogle Scholar
  13. Gibbons, J. W. & Semlitsch, R. D. 1987. Activity patterns. In: Snakes: Ecology and Evolutionary Biology (Ed.by R. A. Seigel, J. T. Collins & S. S. Novak), pp 396–421. New York: Macmillan.Google Scholar
  14. Hamilton W. J., Jr. 1951. The food and feeding behavior of the garter snake in New York State. Amer. Midl. Natr, 46, 385–390.CrossRefGoogle Scholar
  15. Heatwole, H. 1962. Environmental factors influencing local distribution and activity of the salamander, Plethodon cinereus. Ecology, 43, 460–472CrossRefGoogle Scholar
  16. Heinen, J. T. 1995. Predator cues and prey responses: A test using eastern garter snakes (Thamnophis s. sirtalis) and American toads (Bufo a. americanus).Copeia, 1995, 738–741.Google Scholar
  17. Heller S. & Halpern, M. 1981. Laboratory observations on conspecific and congeneric scent trailing in garter snakes (Thamnophis).Behav. Neur. Biol, 33, 372–377.CrossRefGoogle Scholar
  18. Holomuzki, J. R. 1986. Predator avoidance and diel patterns of microhabitat use by larval tiger salamanders. Ecology, 67, 737–748.CrossRefGoogle Scholar
  19. Jaeger, R. 1978. Plant climbing by salamanders: periodic availability of plant-dwelling prey. Copeia, 1978, 686–691.Google Scholar
  20. Jaeger, R. G. 1986. Pheromonal markers as territorial advertisement by terrestrial salamanders. In: Chemical Signals in Vertebrates 4 (Ed. by D. Duvall, D. Muller-Schwarze & R. M. Silverstein), pp. 191–203. New York: Plenum.CrossRefGoogle Scholar
  21. Keefe, M. L. 1991. Chemically mediated avoidance behavior in wild brook trout, Salvelinus fontinalis: the response to familiar and unfamiliar predaceous fishes and the influence of fish diet. Can. J. Zool., 70, 288–292.CrossRefGoogle Scholar
  22. Lima, S. L. & Dill, L. M. 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool, 68, 612–640.CrossRefGoogle Scholar
  23. Madison, D. M. 1977. Chemical communication in amphibians and reptiles. In: Chemical Communication in Vertebrates (Ed. by D. Muller-Schwarze & M. M. Mozell), pp. 135–168. New York: Plenum.CrossRefGoogle Scholar
  24. Madison, D.M., McDarby, J. H. & Maerz, J. C. 1999. Economy of avoidance of snake odors by salamanders: Diet and diel contingencies. Ethiology, in press.Google Scholar
  25. Magurran, A. E. 1989. Acquired recognition of predator odour in the European minnow (Phoxinus phoxinus). Ethology, 82, 216–223.CrossRefGoogle Scholar
  26. Mathis A. & Smith, R. J. 1993a. Fathead minnows, Pimephales promelas, learn to recognize northern pike, Esox lucius, as predators on the basis of chemical stimuli from minnows in the pike’s diet. Anim. Behav., 46, 645–656.CrossRefGoogle Scholar
  27. Mathis A. & Smith, R. J. 1993b. Chemical labelling of northern pike (Esox lucius) by the alarm pheromone of fathead minnows (Pimephales promelas). J. Chem. Ecol., 19, 1967–1979.CrossRefGoogle Scholar
  28. McDarby, J. H. 1997. Chemosensory avoidance of predators by the red-backed salamander, Plethodon cinereus. M. A. Thesis, State University of New York, Binghamton, NY.Google Scholar
  29. McDarby J. H., Madison, D.M. & Maerz, J. C. In press. Chemosensory avoidance of predators by the red-backed salamander, Plethodon cinereus. In: Advances in Chemical Signals in Vertebrates (Ed. by R. Johnston), pp. 489–496. New York: Plenum Publ. Corp.Google Scholar
  30. Parker, D. A. & Shulman, M. J. 1986. Avoiding predation: alarm responses of Caribbean sea urchins to simulated predation on conspecific and heterospecific sea urchins. Mar. Biol., 93, 201–208.CrossRefGoogle Scholar
  31. Reichenbach, N. G. & Dalrymple, G. H. 1986. Energy use, life histories, and the evaluation of potential competition in two species of garter snake. J. Herpetol., 20, 133–153.CrossRefGoogle Scholar
  32. Siegel S. & Castellan N. J., Jr. 1988. Nonparametric Statistics for the Behavioral Sciences. New York: McGraw-Hill.Google Scholar
  33. Sih, A. 1985. Evolution, predator avoidance, and unsuccessful predation. Am. Nat, 125, 153–157.CrossRefGoogle Scholar
  34. Sih A. & Kats, L. B. 1991. Effects of refuge availability on the responses of salamander larvae to chemical cues from predatory green sunfish. Anim. Behav., 42, 330–332.CrossRefGoogle Scholar
  35. Sih A., Kats, L. B. & Moore, R. D. 1992. Effects of predatory sunfish on the density, drift, and refuge use of stream salamander larvae. Ecology, 73, 1418–1430.CrossRefGoogle Scholar
  36. Simon, G. S. & Madison, D. M. 1984. Individual recognition in salamanders: cloacal odours. Anim. Behav, 32, 1017–1020.CrossRefGoogle Scholar
  37. Smith, R. J. 1992. Alarm signals in fishes. Rev. Fish. Biol. Fish., 2, 33–63.CrossRefGoogle Scholar
  38. Smith, R. J. 1997. Avoiding and deterring predators. In: Behavioural Ecology of Teleost Fishes (Ed. by J. J. Godin), pp. 163–190. New York: Oxford Univ. Press.Google Scholar
  39. Sugalski, M. T. & Claussen, D. L. 1997. Preference for soil moisture, soil pH, and light intensity by the salamander, Plethodon cinereus. J. Herpetol., 31, 245–250.CrossRefGoogle Scholar
  40. Turner, A. M. 1994. The effects of predator mediated habitat use on consumer-resource interactions. Ph. D. thesis, Michigan State University, East Lansing.Google Scholar
  41. Turner, A. M. 1996. Freshwater snails alter habitat use in response to predation. Anim. Behav, 51, 747–756.CrossRefGoogle Scholar
  42. Wilson, D. J. & Lefcort, H. 1993. The effect of predator diet on the alarm response of red-legged frog, Rana aurora, tadpoles. Anim. Behav., 46, 1017–1019.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1999

Authors and Affiliations

  • Dale M. Madison
    • 1
  • John C. Maerz
    • 1
  • James H. McDarby
    • 1
  1. 1.Department of Biological SciencesState University of New YorkBinghamtonUSA

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