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Chronic exposure of cat odor enhances aggression, urinary attractiveness and sex pheromones of mice

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Abstract

To test whether predator odor exposure negatively affects the behavior of prey, we exposed three groups of male house mice (Mus musculus) to the odors of cat (Felis catus) urine, rabbit (Oryctolagus cuniculus) urine and water (control), respectively, for consecutive 58 days and investigated how the treatments affected the response, aggressiveness, dominance, urinary attractiveness to females and pheromone composition of male mice. Compared to mice exposed to rabbit urine or water, those exposed to cat odor did not show any response habituation to the cat odor and became more aggressive, increased mark urine production and were more attractive to females when the latter were tested with their urine. Furthermore, gas chromatography coupled with mass spectrometry analysis revealed coincident elevations of the well-known male pheromones, E,E-α-farnesene, E-β-farnesene, R,R-dehydro-exo-brevicomin or S-2-sec-butyl-dihydrothiazole. In addition, rabbit urine exposure increased urinary attractiveness to females and pheromonal levels of the males in comparison with the mice exposed to water. This could be related to olfactory enrichment of heterospecific chemosignals, suggesting that predator odors were more beneficial. In light of these anti-intuitional findings in the chemical interaction between cats and mice, we conclude that predator odor affects prey more profoundly than previously believed and that its impact may not always be negative.

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References

  • Andersson M (1994) Sexual selection, Princeton University Press, Princeton

    Google Scholar 

  • Apfelbach R, Blanchard CD, Blanchard RJ, Hayes RA, McGregor IS (2005) The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci Biobehav Rev 29:1123–1144

    Article  PubMed  Google Scholar 

  • Arnqvist G, Rowe L (2005) Sexual conflict, Princeton University Press, Princeton

    Google Scholar 

  • Becker JB, Breedlove SM, Crews D, McCarthy MM (2002) Behavioral endocrinology, 2nd edn. MIT Press, Cambridge

    Google Scholar 

  • Bian J, Wu Y, Liu J (2005) Breeding behavior under temporal risk of predation in male root voles (Microtus oeconomus). J Mammal 86:953–960

    Article  Google Scholar 

  • Burwash MD, Tobin ME, Woolhouse AD, Sullivan TP (1998) Laboratory evaluation of predator odors for eliciting an avoidance response in roof rats (Rattus rattus). J Chem Ecol 24:49–66

    Article  CAS  Google Scholar 

  • Caine NG, Weldon PJ (1989) Responses by red-bellied tamarins (Saguinus labiatus) to fecal scents of predatory and non-predatory neotropical mammals. Biotropica 21:186–189

    Article  Google Scholar 

  • Desjardins C, Maruniak JA, Bronson FH (1973) Social rank in house mice: differentiation revealed by ultraviolet visualization of urinary marking patterns. Science 182:939–941

    Article  PubMed  CAS  Google Scholar 

  • Drickamer L (1995) Rates of urine excretion by house mouse (Mus domesticus): differences by age, sex, social status, and reproductive condition. J Chem Ecol 21:1481–1493

    Article  CAS  Google Scholar 

  • Engelhart A, Müller-Schwarze D (1995) Responses of beaver (Castor canadensis Kuhl) to predator chemicals. J Chem Ecol 21:1349–1364

    Article  CAS  Google Scholar 

  • Francis RC (1988) On the relationship between aggression and social dominance. Ethology 78:223–237

    Article  Google Scholar 

  • Gassett JW, Wiesler DP, Baker AG, Osborn DA, Miller KV, Marchinton RL, Novotny M (1996) Volatile compounds from interdigital gland of male white-tailed deer (Odocoileus virginianus). J Chem Ecol 22:1689–1696

    Article  CAS  Google Scholar 

  • Gray S, Hurst JL (1995) The effects of cage cleaning on aggression within groups of male laboratory mice. Anim Behav 49:821–826

    Google Scholar 

  • Haemisch A, Voss T, Gärtner K (1994) Effects of environmental enrichment on aggressive behavior, dominance hierarchies, and endocrine stats in male DBA/2J mice. Physiol Behav 56:1041–1048

    Article  PubMed  CAS  Google Scholar 

  • Harvey S, Jemiolo B, Novotny M (1989) Pattern of volatile compounds in dominant and subordinate male mouse urine. J Chem Ecol 15:2061–2072

    Article  CAS  Google Scholar 

  • Herman CS, Valone TJ (2000) The effect of mammalian predator scent on the foraging behavior of Dipodomys merriami. Oikos 91:139–145

    Article  Google Scholar 

  • Jemiolo B, Alberts J, Sochinski-Wiggins S, Harvey S, Novotny M (1985) Behavioral and endocrine responses of female mice to synthetic analogues of volatile compounds in male urine. Anim Behav 33:1114–1118

    Article  Google Scholar 

  • Jemiolo B, Xie T-M, Novotny M (1991) Socio-sexual olfactory preference in female mice: attractiveness of synthetic chemosignals. Physiol Behav 50:1119–1122

    Article  PubMed  CAS  Google Scholar 

  • Kemble ED, Bolwahnn BL (1997) Immediate and long-term effects of novel odors on risk assessment in mice. Physiol Behav 61:543–549

    Article  PubMed  CAS  Google Scholar 

  • Mandairon N, Stack C, Linster C (2006) Olfactory enrichment improves the recognition of individual components in mixtures. Physiol Behav 89:379–384

    Article  PubMed  CAS  Google Scholar 

  • Mason JR, Epple G, Nolte DL (1994) Semiochemicals and improvements in rodent control. In: Galef BE, Mainardi M, Valsecchi P (eds) Behavioral aspects of feeding: basic and applied research in mammals. Harwood Academic, Chur, Switzerland, pp 327–346

    Google Scholar 

  • McGregor PK, Ayling SJ (1990) Varied cages result in more aggression in male CFLP mice. Appl Anim Behav Sci 26:277–281

    Article  Google Scholar 

  • Monclús R, Rödel HG, Holst DV, Miguel, JD (2005) Behavioral and physiological responses of naïve European rabbits to predator odor. Anim Behav 70:753–761

    Article  Google Scholar 

  • Müller-Schwarze D (1995) Chemical repellents for beaver: new leads. In: Apfelbach R, Müller-Schawarze D, Reutter K, Weiler E (eds) Advances in the biosciences 93A. Elsevier, Oxford, pp 479–484

    Google Scholar 

  • Novotny M, Harvey S, Jemiolo B (1990) Chemistry of male dominance in the house, Mus domesticus. Experimenta 46:109–113

    Article  CAS  Google Scholar 

  • Novotny M, Ma W, Zidek L, Daev E (1999) Recent biochemical insights into puberty acceleration, estrus induction and puberty delay in the house mouse. In: Johnston RE, Müller-Schwarze D, Sorenson P (eds) Advances in chemical communication in vertebrates. Plenum, New York, pp 99–116

    Google Scholar 

  • Perrot-Sinal TS, Ossenkopp K-P, Kavaliers M (1999) Effects of repeated exposure to fox odor on locomotor activity levels and spatial movement patterns in breeding male and female meadow voles (Microtus pennsylvanicus). J Chem Ecol 25:1567–1584

    Article  CAS  Google Scholar 

  • Perrot-Sinal T, Ossenkopp KP, Kavaliers M (2000) Influence of a natural stressor (predator odor) on locomotor activity in the meadow vole (Microtus pennsylvanicus): modulation by sex, reproductive condition and gonadal hormones. Psychoneuroendocrinology 25:259–276

    Article  PubMed  CAS  Google Scholar 

  • Roy V, Belzung C, Delarue C, Chapillon P (2001) Environmental enrichment in BALB/c mice: effects in classical tests of anxiety and exposure to a predatory odor. Physiol Behav 74:313–320

    Article  PubMed  CAS  Google Scholar 

  • Schwende FJ, Wiesler D, Jorgenson JW, Carmack M, Novotny M (1986) Urinary volatile constituents of the house mouse, Mus musculus, and their endocrine dependency. J Chem Ecol 12:277–296

    Article  CAS  Google Scholar 

  • Soini HA, Bruce KE, Wiesler D, David F, Sandra P, Novotny MV (2005) Stir bar sorptive extraction: a new quantitative and comprehensive sampling technique for determination of chemical signal profiles from biological media. J Chem Ecol 31:377–392

    Article  PubMed  CAS  Google Scholar 

  • Sullivan TP, Crump DR, Wieser H, Dixon EA (1990) Comparison of release devices for stoat (Mustela ermined) semiochemicals used as montane vole (Microtus montanus) repellents. J Chem Ecol 16:951–957

    Article  CAS  Google Scholar 

  • Sun L, Müller-Schwarze D (1999) Chemical signals in the beaver. In: Johnston RE, Müller-Schwarze D, Sorenson P (eds) Advances in chemical communication in vertebrates. Plenum, New York, pp 281–288

    Google Scholar 

  • Takahashi LK, Nakashima BR, Hong H, Watanabe K (2005) The smell of danger: a behavioral and neural analysis of predator odor-induced fear. Neurosci Biobehav Rev 29:1157–1167

    Article  PubMed  Google Scholar 

  • Vasilieva NA, Cherepanova EV, Safranova L (1999) Influence of cat’s urinary chemosignals on sexual maturation and meiosis in Campbell’s hamster males (Phodopus campelli). In: Johnston RE, Müller-Schwarze D, Sorenssen PW (eds) Advances in chemical signals in vertebrates. Kluwer/Plenum, New York, pp 445–455

    Google Scholar 

  • Zahavi A (1975) Mate selection: a selection for a handicap. J Theor Biol 53:205–214

    Article  PubMed  CAS  Google Scholar 

  • Zhang JX, Zhang ZB, Wang ZW (2001) Scent, social status, and reproductive condition in rat-like hamsters (Cricetulus trition). Physiol Behav 74:415–420

    Article  PubMed  CAS  Google Scholar 

  • Zhang JX, Cao C, Gao H, Yang ZS, Ni J, Wu FY, Zhang ZB, Wang ZW (2003) Effects of weasel odor on behavior and physiology of two hamster species. Physiol Behav 79:549–552

    Article  PubMed  CAS  Google Scholar 

  • Zhang JX, Cao C, Gao H, Yang ZS, Ni J, Wu FY, Zhang ZB, Wang ZW (2004) Effect of gender and age on the responses of the rat-like hamster (Cricetulus triton) to predator odor (in Chinese). Acta Zool Sin 50:151–157

    Google Scholar 

  • Zhang JX, Soini HA, Bruce KE, Wiesler D, Woodley SK, Baum MJ, Novotny MV (2005) Putative chemosignals of the ferret (Mustela furo) associated with individual and gender recognition. Chem Senses 30:727–737

    Article  PubMed  CAS  Google Scholar 

  • Zhang JX, Sun L, Novotny M (2007) Mice respond differently to urine and its major volatile constituents from male and female ferrets. J Chem Ecol 33:603–612

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This research was supported by grants (No. DC 24180 to M.Y.N) from the National Institute of Deafness and Other Communication Disorders, National Institute of Health (NIH) and the U.S. Department of Health and Human Services. The manuscript preparation was supported by the CAS Innovative Research International Partnership Project (CXTDS2005-4 to J.X.Z and L.S.) and the China NSF (No. 30670268 to J.X.Z).

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Authors and Affiliations

  1. State Key Laboratory of Integrated Management of Pest Insects and Rodents in Agriculture, Institute of Zoology, Chinese Academy of Sciences, Datunlu RD, Beijing, 100101, China

    Jian-Xu Zhang

  2. Department of Biological Sciences, Central Washington University, Ellensburg, WA, 98926-7537, USA

    Lixing Sun

  3. Institute for Pheromone Research and Department of Chemistry, Indiana University, Bloomington, IN, 47405, USA

    Jian-Xu Zhang, Kevin E. Bruce & Milos V. Novotny

Authors
  1. Jian-Xu Zhang
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  2. Lixing Sun
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  3. Kevin E. Bruce
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  4. Milos V. Novotny
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Correspondence to Jian-Xu Zhang.

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Zhang, JX., Sun, L., Bruce, K.E. et al. Chronic exposure of cat odor enhances aggression, urinary attractiveness and sex pheromones of mice. J Ethol 26, 279–286 (2008). https://doi.org/10.1007/s10164-007-0060-1

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  • DOI: https://doi.org/10.1007/s10164-007-0060-1

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