Donning your enemy's cloak: Ground squirrels exploit rattlesnake scent to reduce predation risk

Proceedings of the Royal Society B: Biological Sciences

Volumn 275, Issue 1636, 2008, Pages 847-852

  Clucas, Barbara ^a   Owings, Donald H ^a   Rowe, Matthew P ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Sam Houston State University   (United States)

Author keywords

Antipredator behaviour; Camouflage; Chemical defence; Ground squirrels; Rattlesnakes

Indexed keywords

ANTIPREDATOR DEFENSE; CHEMICAL DEFENSE; DOMINANCE; ECTOPARASITE; FLEA; HOST PREFERENCE; OLFACTORY CUE; PREDATION RISK; PREDATOR-PREY INTERACTION; RODENT; SCENT MARKING; SKIN; SNAKE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ECTOPARASITE; FEMALE; LICKING; MALE; NONHUMAN; ODOR; PREDATION; PREDATOR; PREY; PRIORITY JOURNAL; RISK REDUCTION; SMELLING; SNAKE; SQUIRREL;

CROTALUS; SCIURIDAE; SIPHONAPTERA (FLEAS); SPERMOPHILUS;

EID: 39149109586     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2007.1421     Document Type: Article

References (36)

1. Apfelbach, R., Blanchard, C. D., Blanchard, R. J., Hayes, R. A. & McGregor, I. S. 2005 The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci. Biobehav. Rev. 29, 1123-1144. (doi:10.1016/j.neubiorev.2005.05.005)
2. Biardi, J. E. 2000 Adaptive variation and coevolution in California ground squirrel (Spermophilus beecheyi) and rock squirrel (Spermophilus variegatus) resistance to rattlesnake venom. PhD dissertation, University of California, Davis.
3. Blumstein, D. T., Evans, C. & Daniels, J. C. 2006 JWATCHER 1.0. See http://www.jwatcher.ucla.edu/.
4. Brodie, E. D. 1977 Hedgehogs use toad venom in their own defence. Nature 268, 627-628. (doi:10.1038/268627a0)
5. Bursten, S. N., Kimsey, R. B. & Owings, D. H. 1997 Ranging of male Oropsylla montana fleas via male California ground squirrel (Spermophilius beecheyi) juveniles. J. Parasitol. 83, 804-809. (doi:10.2307/3284271)
6. Caro, T. M. 2005 Antipredator defenses in birds and mammals. Chicago, IL: University of Chicago Press.
7. Carroll, J. F., Kramer, M., Weldon, P. J. & Robbins, R. G. 2005 Anointing chemicals and ectoparasites: effects of benzoquinones from millipedes on the lone star tick, Amblyomma americanum. J. Chem. Ecol. 31, 63-75. (doi:10.1007/s10886-005-0974-4)
8. Clark, R.W. 2004 Timber rattlesnakes (Crotalus horridus) use chemical cues to select ambush sites. J. Chem. Ecol. 30, 607-617. (doi:10.1023/B:JOEC.0000018632.27010.1e)
9. Clark, R. W. 2007 Public information for solitary foragers: timber rattlesnakes use conspecific chemical cues to select ambush sites. Behav. Ecol. 18, 487-490. (doi:10.1093/beheco/arm002)
10. Clucas, B., Rowe, M. P., Owings, D. H. & Arrowood, P. C. 2008 Snake scent application in ground squirrels, Spermophilus spp.: a novel form of antipredator behavior? Anim. Behav. 75, 299-307. (doi:10.1016/j.anbehav.2007.05.024)
11. Conover, M. R. 2007 Predator prey dynamics: the role of olfaction. Boca Raton, FL: CRC Press.
12. Cott, H. B. 1957 Adaptive coloration in animals. London, UK: Methuen & Co.
13. Drea, C. M., Vignieri, S. N., Cunningham, S. B. & Glickman, S. E. 2002 Responses to olfactory stimuli in spotted hyenas (Crocuta crocuta): I. Investigation of environmental odors and the function of rolling. J. Comp. Psychol. 116, 331-341. (doi:10.1037/0735-7036.116.4.331)
14. Edmunds, M. 1974 Defense in animals. New York, NY: Longman Group Limited.
15. Eisner, T. & Grant, R. P. 1981 Toxicity, odor aversion, and "olfactory aposematism". Science 213, 476. (doi:10.1126/science.7244647)
16. Hennessy, D. F. & Owings, D. H. 1988 Rattlesnakes create a context for localizing their search for potential prey. Ethology 77, 317-329.
17. Hennessy, D. F., Owings, D. H., Rowe, M. P., Coss, R. G. & Leger, D. W. 1981 The information afforded by a variable signal: constraints on snake-elicited tail flagging by California ground squirrels. Behaviour 78, 188-226.
18. Hersek, M. J. & Owings, D. H. 1993 Tail flagging by adult California ground squirrels: a tonic signal that serves different functions for males and females. Anim. Behav. 46, 129-138. (doi:10.1006/anbe.1993.1168)
19. Kobayashi, T. & Watanabe, M. 1986 An analysis of snake-scent application behavior in Siberian chipmunks (Eutamias sibiricus asiaticus). Ethology 72, 40-52.
20. Krasnov, B. R., Khokhlova, I. S., Oguzoglu, I. & Burdelova, N. V. 2002 Host discrimination by two desert fleas using an odour cue. Anim. Behav. 64, 33-40. (doi:10.1006/anbe.2002.3030)
21. Lima, S. L. & Dill, L. M. 1990 Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68, 619-640.
22. Owings, D. H. & Coss, R. G. 1977 Snake mobbing by California ground squirrels - adaptive variation and ontogeny. Behaviour 62, 50-69.
23. Owings, D. H. & Coss, R. G. In press. Hunting California ground squirrels: constraints and opportunities for northern Pacific rattlesnakes. In The biology of rattlesnakes (eds W. K. Hayes, K. R. Beaman, M. D. Cardwell & S. P. Bush). Loma Linda, CA: Loma Linda University Press.
24. Owings, D. H., Coss, R. G., McKernon, D., Rowe, M. P. & Arrowood, P. C. 2001 Snake-directed antipredator behavior of rock squirrels (Spermophilus variegatus): population differences and snake-species discrimination. Behaviour 138, 575-595. (doi:10.1163/156853901316924485)
25. Poran, N. S., Coss, R. G. & Benjamini, E. 1987 Resistance of California ground-squirrels (Spermophilus beecheyi) to the venom of the northern Pacific rattlesnake (Crotalus viridis oreganus) - a study of adaptive variation. Toxicon 25, 767-777. (doi:10.1016/0041- 0101(87)90127-9)
26. Rowe, M. P., Coss, R. G. & Owings, D. H. 1986 Rattlesnake rattles and burrowing owl hisses: a case of acoustic Batesian mimicry. Ethology 72, 53-71.
27. Rundus, A. S., Owings, D. H., Joshi, S., Chinn, E. & Giannini, N. 2007 Ground squirrels use an infrared signal to deter rattlesnake predation. Proc. Natl Acad. Sci. USA 104, 14 372-14 376. (doi:10.1073/pnas. 0702599104)
28. Schuetz, J. G. 2005 Common waxbills use carnivore scat to reduce the risk of nest predation. Behav. Ecol. 16, 133-137. (doi:10.1093/beheco/ arh139)
29. Spruijt, B. M., Van Hooff, J. A. R. A. M. & Gispen, W. H. 1992 Ethology and neurobiology of grooming behavior. Physiol. Rev. 72, 825-852.
30. SPSS 2002 SPSS for Mac OS X, rel. 11.0.2. Chicago, IL: SPSS, Inc.
31. Theodoratus, D. H. & Chiszar, D. 2000 Habitat selection and prey odor in the foraging behavior of western rattlesnakes (Crotalus viridis). Behaviour 137, 119-135. (doi:10.1163/156853900501908)
32. Vane-Wright, R. I. 1980 On the definition of mimicry. Biol. J. Linn. Soc. 13, 1-6.
33. Weldon, P. J. 2004 Defensive anointing: extended chemical phenotype and unorthodox ecology. Chemoecology 14, 1-4. (doi:10.1007/s00049-003- 0259-8)
34. Weldon, P. J., Aldrich, J. R., Klun, J. A., Oliver, J. E. & Debboun, M. 2003 Benzoquinones from millipedes deter mosquitoes and elicit self-anointing in capuchin monkeys (Cebus spp.). Naturwissenschaften 90, 301-304. (doi:10.1007/s00114-003-0427-2)
35. Xu, Z. J., Stoddart, D. M., Ding, H. B. & Zhang, J. 1995 Self-anointing behavior in the rice-field rat, Rattus rattoides. J. Mammal. 76, 1238-1241. (doi:10.2307/1382617)
36. Zhang, J., Cao, C., Gao, H., Yang, Z., Sun, L., Zhang, Z. & Wang, Z. 2003 Effects of weasel odor on behavior and physiology of two hamster species. Physiol. Behav. 79, 549-552. (doi:10.1016/S0031-9384(03)00123-9)