Abstract
Our previous chemical investigation showed that the concentrations of urinary volatiles from males were much higher than those from females in the ferret (Mustela furo). The current study was designed to examine the behavioral significance and ecological relevance of this difference for one of the main prey of the ferret, the house mouse (Mus musculus). Our data showed that male mice displayed no difference in their response to raw male and female ferret urine. However, they showed significantly less response to female mouse urine mixed with ferret urine than to pure female mouse urine, and to female mouse urine mixed with male ferret urine than to female mouse urine mixed with female ferret urine. Furthermore, high levels of the three major volatiles (quinoline, 2,5-dimethylpyrazine, and 4-hepatanone) in male ferret urine were as effective as raw male ferret urine was in inhibiting the response of male mice. We discuss the ecological and behavioral significance of these findings in terms of chemical mimicry and cognitive feature extraction of predator odors in mice.
Similar content being viewed by others
References
Andreolini, F., Jemiolo, B., and Novotny, M. 1987. Dynamics of excretion of urinary chemosignals in the house mouse (Mus musculus) during the natural estrous cycle. Experientia 45:998–1002.
Apfelbach, R., Blanchard, C. D., Blanchard, R. J., Hayes, R. A., and 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.
Bramley, G. N. and Joseph, R. W. 2001. Laboratory and field evaluation of predator odors as repellents for kiore (Rattus exulans) and ship rats (R. rattus). J. Chem.Ecol. 27:1029–1047.
Brinck, C., Erlinge, S., and Sandell, M. 1983. Anal sac secretion in Mustelids: A comparison. J. Chem. Ecol. 9:727–745.
Buesching, C. D., Waterhouse, J. S., and Macdonald, D. W. 2002a. Gaschromatographic analyses of the subcaudal gland secretion of the European badger (Meles meles). Part I: Chemical differences related to individual parameters. J. Chem. Ecol. 28:41–56.
Buesching, C. D., Waterhouse, J. S., and Macdonald, D. W. 2002b. Gaschromatographic analyses of the subcaudal gland secretion of the European badger (Meles meles). Part II: Time-related variation in the individual-specific composition. J. Chem. Ecol. 28:57–69.
Burwash, M. D., Tobin, M. E., Woolhouse, A. D., and Sullivan, T. P. 1998. Field testing synthetic predator odors for roof rats (R. rattus) in Hawaiian macadamia nut orchards. J. Chem Ecol. 24:603–630.
Cloe, A. L., Woodley, S. K., Waters, P., Zhou, H., and Baum, M. J. 2004. Contribution of anal scent gland and urinary odors to mate recognition in the ferret. Physiol. Behav. 82:871–875.
Dettner, K. and Liepert, C. 1994. Chemical mimicry and camouflage. Annu. Rev. Ento. 39:129–154.
Eisner, T., Morgan, R. C., Attygalle, A. B., Smedley, S. R., Herath, K. B. and Meinwald, J. 1997. Defensive production of quinoline by a phasmid insect (Oreophoetes peruana). J. Exp. Biol. 200:2493–2500.
Epple, G., Mason, J., Nolte, D. and Campbell, D. 1993. Effects of predator odors on feeding in the mountain beaver (Aplodontia rufa). J. Mammal. 74:715–722.
Epple, G., Mason, J. R., Aronov, E., Nolte, D. L., Hartz, R. A., Kaloostian, R., Campbell, D. and Smith, A. B. 1995. Feeding responses to predator-based repellents in the mountain beaver (Aplodontia rufa). Ecol. Appl. 5:1163–1170.
Jemiolo, B. and Novotny, M. 1993. Long-term effect of a urinary chemosignal on reproductive fitness in female mice. Biol. Reprod. 48:926–929.
Jemiolo, B., Andreolini, F., Wiesler, D. and Novotny, M. 1987. Variations in the mouse (Mus musculus) urinary volatiles during different periods of pregnancy and lactation. J. Chem. Ecol. 13:1941–1956.
Lai, S-C, Vasilieva, N. Y. and Johnston, R. E. 1996. Odors providing sexual information in Dijungarian hamsters: evidence for an across-odor code. Horm. Behav. 30:26–36.
Mappes, T., Koskela, E. and Ylönen, H. 1998. Breeding suppression in voles under predation risk of small mustelids: laboratory or methodological artifact? Oikos 82:365–369.
Müller-Schwarze, D. 1995. Chemical repellents for beaver: New leads, pp. 479–484, in R. Apfelbach, D. Müller-Schwarze, K. Reutter, and E. Weiler (eds.). Advances in Biosciences, Vol 93: Chemical Signals in Vertebrates 7. Elsevier Science Ltd., Great Britain.
Mason, J. R., Epple, G. and Nolte, D. L. 1994. Semiochemicals and improvements in rodent control. pp. 327–346, in B. E. Galef, M. Mainardi, and P. Valsecchi (eds.). Behavioral Aspects of Feeding: Basic and Applied Research in Mammals. Harwood Academic, Chur, Switzerland.
Nolte, D. L, Mason, J. R. and Clark, L. 1993. Avoidance of bird repellents by mice (Mus musculus). J. Chem. Ecol. 19:427–432.
Novotny, M., Jemiolo, B., Harvey, S., Wiesler, D. and Marchlewska-Koj, A. 1986. Adrenal-mediated endogenous metabolites inhibit puberty in female mice. Science 231:722–725.
Pasteur, G. 1982. A classification review of mimicry systems. Annu. Rev. Ecol. Syst. 13:169–199.
Preti, G., Muetterties, E. L., Furman, J. M., Kennelly, J. J. and Johns, B. E. 1976. Volatile constitutes of dog (Canis familiaris) and coyote (C. latrans) anal sacs. J. Chem. Ecol. 2:177–186.
Raymer, J. 1984. Investigations into the chemical nature of chemo-olfactory communication in the wolf (Canis lupus). PhD dissertation). Indiana University, Bloomington.
Raymer, J., Wiesler, D., Novotny, M., Asa, C., Seal, U. S., and Mech, L. D. 1985. Chemical investigations of wolf (Canis lupus) anal sac secretion in relation to breeding season. J. Chem. Ecol. 11:593–608.
Roberts, S. C., Gosling, L. M., Thornton, E. A. and McClung, J. 2001. Scent-marking by male mice under the risk of predation. Behav. Ecol. 12:698–705.
Schildknecht, H. and Birkner, C. 1983. Struktur und Wirkung der Musteliden-Ökomone, III: Analyse der Analbeutelsekrete Mitteleuropa ischer Musteliden. Chemiker-Zeitung 107:267–270 (in German).
Schildknecht, H., Stenuf, G. and Krauss, D. 1986. Structure and action of mammalian ecomones. VI. Behavior-active chemical signals from the urine of the ferret (Mustela putorius furo). Chemiker-Zeitung 110:185–195 (in German).
Schulte, B. A., Müller-Schwarze, D., Tang, R. and Webster, F. X. 1994. Beaver (Castor canadensis) responses to major phenolic and neutral compounds in castoreum. J. Chem. Ecol. 20:3063–3081.
Service, K. M., Brereton, R. G. and Harris, S. 2001. Analysis of badger urine volatiles using gas chromatography-mass spectrometry and pattern recognition techniques. Analyst 126:615–623.
Stoddart, M. 1980. The Ecology of Vertebrate Olfaction, Chapman & Hall Ltd, London.
Sullivan, T., Crump, D. and Sullivan, D. 1988a. Use of predator odors as repellents to reduce feeding damage by herbivores. 3. Montane and meadow voles (Microtus montanus and M. pennsylvannicus). J. Chem. Ecol. 14:363–378.
Sullivan, T., Crump, D. and Sullivan, D. 1988b. Use of predator odors as repellents to reduce feeding damage by herbivores. 4. Northern pocket gophers (Thomomys talipoides). J. Chem. Ecol. 14:379–390.
Vernfset-Maury, E., Polak, E. H. and Demael, A. 1984. Structure-activity relationship of stress-inducing odorants in the rat. J. Chem. Ecol. 10:1007–1019.
Zhang, J., Zhang, Z. and Wang, Z. 2001. Males’ olfactory discrimination of receptive state of female in rat-like hamsters (Cricetulus triton), pp. 385–390, in A. Marchlewska-Koj, J. J. Lepri, and D. Müller-Schwarze (eds.). Chemical Signals in Vertebrates 9, Kluwer Academic/Plenum Publishers, New York.
Zhang, J., Ni, J., Ren, X., Sun, L., Zhang, Z. and Wang, Z. 2003. Possible coding for recognitions of sexes, individuals and species in anal gland volatiles of Mustela eversmanni and M. sibirica. Chem. Senses 28:371–378.
Zhang, J., Soini, H., Bruce, K., Wiesler, D., Woodley, S., Baum, M. and Novotny M. 2005. Putative chemosignals of the ferret (Mustela furo) associated with individual and gender recognition. Chem. Senses 30:727–737.
Acknowledgments
We are grateful to Dr. Janne Sundell for valuable comments on our earlier draft. We are grateful to Drs. Sarah K. Woodley and Michael J. Baum who provided us with ferret urine. This research was supported by grants [No. DC 24180 to M.V. N] from the National Institute of Deafness and Other Communication Disorders, National Institute of Health (NIH), and US Department of Health and Human Services. The manuscript preparation and data processing were partially supported by the CAS Innovative Research International Partnership Project (CXTDS2005-4).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zhang, JX., Sun, L. & Novotny, M. Mice Respond Differently to Urine and Its Major Volatile Constituents from Male and Female Ferrets. J Chem Ecol 33, 603–612 (2007). https://doi.org/10.1007/s10886-006-9220-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-006-9220-y