Skip to main content
SpringerLink
Log in

Effect of Male House Mouse Pheromone Components on Behavioral Responses of Mice in Laboratory and Field Experiments

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Urine of male house mice, Mus musculus, is known to have primer pheromone effects on the reproductive physiology of female mice. Urine-mediated releaser pheromone effects that trigger certain behavioral responses are much less understood, and no field studies have investigated whether urine deposits by male or female mice, or synthetic mouse pheromone, increase trap captures of mice. In field experiments, we baited traps with bedding soiled with urine and feces of caged female or male mice, and recorded captures of mice in these and in control traps containing clean bedding. Traps baited with female bedding preferentially captured adult males, whereas traps baited with male bedding preferentially captured juvenile and adult females, indicating the presence of male- and female-specific sex pheromones in soiled bedding. Analyses of headspace volatiles emanating from soiled bedding by gas chromatography/mass spectrometry revealed that 3,4-dehydro-exo-brevicomin (DEB) was seven times more prevalent in male bedding and that 2-sec-butyl-4,5-dihydrothiazole (DHT) was male-specific. In a follow-up field experiment, traps baited with DEB and DHT captured 4 times more female mice than corresponding control traps, thus indicating that DEB and DHT are sex attractant pheromone components of house mouse males. Our study provides impetus to identify the sex attractant pheromone of female mice, and to develop synthetic mouse pheromone as a lure to enhance the efficacy of trapping programs for mouse control.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Barnard CJ, Fitzsimons J (1988) Kin recognition and mate choice in mice: the effects of kinship familiarity and social interference on intersexual interactions. Anim Behav 36:1078–1090

    Article  Google Scholar 

  • Berny PJ, Buronfosse T, Buronfosse F, Lamarque F, Lorgue G (1997) Field evidence of secondary poisoning of foxes (Vulpes vulpes) and buzzards (Buteo buteo) by bromadiolone, a 4-year survey. Chemosphere 35:1817–1829

    Article  CAS  PubMed  Google Scholar 

  • Bronson FH (1979) The reproductive ecology of the house mouse. Q Rev Biol 54:265–299

    Article  CAS  PubMed  Google Scholar 

  • Cavaggioni A, Mucignat-Caretta C, Zagotto G (2003) Absolute configuration of 2-sec-butyl-4,5-dihydrothiazole in male mouse urine. Chem Senses 28:791–797

    Article  CAS  PubMed  Google Scholar 

  • Cavaggioni A, Mucignat-Caretta C, Redaelli M, Zagotto G (2006) The scent of urine spots of male mice, Mus musculus: changes in chemical composition over time. Rapid Commun Mass Spectrom 20:3741–3746

    Article  CAS  PubMed  Google Scholar 

  • Drickamer LC (1986) Puberty-influencing chemosignals in mice: ecological and evolutionary considerations. In: Duvall D, Mueller-Schwarze D, Silverstein RM (eds) Chemical signals in vertebrates. IV. Plenum Press, New York, pp 441–455

    Google Scholar 

  • Drickamer LC (1988) Acceleration and delay of sexual maturation in female house mice (Mus domesticus) by urinary chemosignals: mixing urine sources in unequal proportions. J Comp Psychol 102:215–221

    Article  CAS  PubMed  Google Scholar 

  • Drickamer LC (1989a) Odor preferences of wild stock female house mice (Mus domesticus) tested at three ages using urine and other cues from conspecific males and females. J Chem Ecol 15:1971–1987

    Article  CAS  PubMed  Google Scholar 

  • Drickamer LC (1989b) Patterns of deposition of urine containing chemosignals that affect puberty and reproduction by wild stock male and female house mice (Mus domesticus). J Chem Ecol 15:1407–1421

    Article  CAS  PubMed  Google Scholar 

  • Drickamer LC (1992) Oestrous female house mice discriminate dominant from subordinate males and sons of dominant from sons of subordinate males by odour cues. Anim Behav 43:868–870

    Article  Google Scholar 

  • Drickamer LC (1995) Odors in traps: does most recent occupant influence capture rates for house mice? J Chem Ecol 21:541–555

    Article  CAS  PubMed  Google Scholar 

  • Drickamer LC, Mikesic DG, Shaffer KS (1992) Use of odor baits in traps to test reactions to intra- and interspecific chemical cues in house mice living in outdoor enclosures. J Chem Ecol 18:2223–2249

    Article  CAS  PubMed  Google Scholar 

  • Ehman KD, Scott ME (2001) Urinary odour preferences of MHC congenic female mice, Mus domesticus: implications for kin recognition and detection of parasitized males. Anim Behav 62:781–789

    Article  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  PubMed  Google Scholar 

  • Howald G, Donlan CJ, Galván JP, Russell JC, Parkes J, Samaniego A, Wang Y, Veitch D, Genovesi P, Pascal M, Saunders A, Tershy B (2007) Invasive rodent eradication on islands. Conserv Biol 21:1258–1268

    Article  PubMed  Google Scholar 

  • Hurst JL (1990a) Urine marking in populations of wild house mice Mus domesticus Rutty. I. Communication between males. Anim Behav 40:209–222

    Article  Google Scholar 

  • Hurst JL (1990b) Urine marking in populations of wild house mice Mus domesticus Rutty. II. Communication between females. Anim Behav 40:223–232

    Article  Google Scholar 

  • Hurst JL (1990c) Urine marking in populations of wild house mice Mus domesticus Rutty. III. Communication between the sexes. Anim Behav 40:233–243

    Article  Google Scholar 

  • Hurst JL, Robertson D, Tolladay U, Beynon R (1998) Proteins in urine scent marks of male house mice extend the longevity of olfactory signals. Anim Behav 55:1289–1297

    Article  CAS  PubMed  Google Scholar 

  • Hurst JL, Payne CE, Nevison CM, Marie AD, Humphries RE, Robertson DHL, Cavaggioni A, Beynon RJ (2001) Individual recognition in mice mediated by major urinary proteins. Nature 414:631–634

    Article  CAS  PubMed  Google Scholar 

  • Jemiolo B, Alberts J, Sochinski-Wiggins S, Harvey S, Novotny M (1985) Behavioural 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, Harvey S, Novotny M (1986) Promotion of the Whitten effect in female mice by synthetic analogs of male urinary constituents. Proc Natl Acad Sci U S A 83:4576–4579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liebich HM, Zlatkis A, Bertsch W, Van Dahm R, Whitten WK (1977) Identification of dihydrothiazoles in urine of male mice. Biol Mass Spectrom 4:69–72

    Article  CAS  Google Scholar 

  • Mori K, Tashiro T (1999) Pheromone synthesis. Part 197. Synthesis of the enantiomers of 2-sec-butyl-4,5-dihydrothiazole and (1R,5S,7R)-3,4-dehydro-exo-brevicomin, pheromone components of the male mouse, Mus musculus. Eur J Org Chem 9:2167–2173

    Google Scholar 

  • Mossman CA, Drickamer LC (1996) Odor preferences of female house mice (Mus domesticus) in seminatural enclosures. J Comp Psychol 110:131–138

    Article  CAS  PubMed  Google Scholar 

  • Mucignat-Caretta C (2002) Modulation of exploratory behavior in female mice by protein-borne male urinary molecules. J Chem Ecol 28:1853–1863

    Article  CAS  PubMed  Google Scholar 

  • Mucignat-Caretta C, Caretta A (1999a) Urinary chemical cues affect light avoidance behaviour in male laboratory mice, Mus musculus. Anim Behav 57:765–769

    Article  CAS  PubMed  Google Scholar 

  • Mucignat-Caretta C, Caretta A (1999b) Chemical signals in male house mice urine: protein-bound molecules modulate interactions between sexes. Behaviour 136:331–343

    Article  Google Scholar 

  • Mucignat-Caretta C, Caretta A (2014a) Message in a bottle: major urinary proteins and their multiple roles in mouse intraspecific chemical communication. Anim Behav 97:255–263

    Article  Google Scholar 

  • Mucignat-Caretta C, Caretta A, Baldini E (1998) Protein-bound male urinary pheromones: differential responses according to age and gender. Chem Senses 23:67–70

    Article  CAS  PubMed  Google Scholar 

  • Mucignat-Caretta C, Cavaggioni A, Redaelli M, Da Dalt L, Zagotto G, Gabai G (2014b) Age and isolation influence steroids release and chemical signaling in male mice. Steroids 83:10–16

    Article  CAS  PubMed  Google Scholar 

  • Musso AE, Takács SJ, Gries R, Gries G (2014) New compositions and methods for attracting and stimulating feeding by mice and rats. International Publication Number WO 2014/186885 A1. World Intellectual Property Organization

  • Nakamura K, Kikusui T, Takeuchi Y, Mori Y (2007) The critical role of familiar urine odor in diminishing territorial aggression toward a castrated intruder in mice. Physiol Behav 90:512–517

    Article  CAS  PubMed  Google Scholar 

  • Novotny M, Harvey S, Jemiolo B, Alberts J (1985) Synthetic pheromones that promote inter-male aggression in mice. Proc Natl Acad Sci U S A 82:2059–2061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Novotny MV, Xie T-M, Harvey S, Wiesler D, Jemiolo B, Carmack M (1995) Stereoselectivity in mammalian chemical communication: male mouse pheromones. Experientia 51:738–743

    Article  CAS  PubMed  Google Scholar 

  • Osada K, Tashiro T, Mori K, Izumi H (2008) The identification of attractive volatiles in aged male mouse urine. Chem Senses 33:815–823

    Article  CAS  PubMed  Google Scholar 

  • Rattner BA, Horak KE, Warner SE, Day DD, Meteyer CU, Volker SF, Eisemann JD, Johnston JJ (2011) Acute toxicity, histopathology, and coagulopathy in American kestrels (Falco sparverius) following administration of the rodenticide diphacinone. Environ Toxicol Chem 30:1213–1222

    Article  CAS  PubMed  Google Scholar 

  • R Core Team (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.

  • Riley SPD, Bromley C, Poppenga RH, Uzal FA, Whited L, Sauvajot RM (2007) Anticoagulant exposure and notoedric mange in bobcats and mountain lions in urban Southern California. J Wildl Manag 71:1874–1884

    Article  Google Scholar 

  • Rowe FP (1970) The response of wild mice (Mus musculus) to live traps marked by their own and foreign mouse odour. J Zool 162:517–520

    Article  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  PubMed  Google Scholar 

  • Shore RF, Birks JDS, Freestone P (1999) Exposure of non-target vertebrates to second-generation rodenticides in Britain, with particular reference to the polecat Mustela putorius. N Z J Ecol 23:199–206

    Google Scholar 

  • Singleton GR, Leirs H, Hinds LA, Zhang ZB (1999) Ecologically-based management of rodent pests: re-evaluating our approach to an old problem. In: Singleton GR, Hinds L, Leirs H, Zhang Z (eds) Ecologically-based Management of Rodent Pests. ACIAR, Canberra, pp 17–29

    Google Scholar 

  • Smith RH, Meyer AN (2015) Rodent control methods: non-chemical and non-lethal chemical, with special reference to food stores. In: Buckle AP, Smith RH (eds) Rodent pests and their control, 2nd edn. CAB International, Boston, pp 101–122

    Google Scholar 

  • Takács S, Gries R, Zhai H, Gries G (2016a) The sex attractant pheromone of male brown rats: identification and field experiment. Angew Chem Int Ed 55:6062–6066

    Article  Google Scholar 

  • Takács S, Kowalski P, Gries G (2016b) Natural and synthetic vocalizations of brown rat pups, Rattus norvegicus, enhance attractiveness of bait boxes in laboratory and field experiments. Pest Manag Sci 72:1873–1882

    Article  PubMed  Google Scholar 

  • Thomas PJ, Mineau P, Shore RF, Champoux L, Martin PA, Wilson LK, Fitzgerald G, Elliott JE (2011) Second generation anticoagulant rodenticides in predatory birds: probabilistic characterisation of toxic liver concentrations and implications for predatory bird populations in Canada. Environ Int 37:914–920

    Article  CAS  PubMed  Google Scholar 

  • Vandenbergh JG, Coppola DM (1986) The physiology and ecology of puberty modulation by primer pheromones. Adv Study Behav 16:71–108

    Article  Google Scholar 

  • Volfová R, Stejskal V, Aulický R, Frynta D (2010) Presence of conspecific odours enhances responses of commensal house mice (Mus musculus) to bait stations. Int J Pest Manag 57:35–40

    Article  Google Scholar 

  • Wiesler DP, Schwende FJ, Carmack M, Novotny M (1984) Structural determination and synthesis of a chemical signal of the male state and a potential multipurpose pheromone of the mouse Mus musculus. J Organomet Chem 49:882–884

    Article  CAS  Google Scholar 

  • Zhang JX, Rao XP, Sun L, Zhao CH, Qin XW (2007) Putative chemical signals about sex, individuality, and genetic background in the preputial gland and urine of the house mouse (Mus musculus). Chem Senses 32:293–303

    Article  CAS  PubMed  Google Scholar 

  • Zhang JX, Liu YJ, Zhang JH, Sun L (2008) Dual role of preputial gland secretion and its major components in sex recognition in mice. Physiol Behav 95:388–394

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank John Borden for field assistance; John Borden, Jenny Cory, and Michael Holmes for comments on the manuscript; Sharon Oliver for comments and word processing; Carl Schwarz for advice on statistical analyses; and two anonymous reviewers for meticulous reviews and constructive comments. The research was supported by the Thelma Finlayson Graduate Entrance Scholarship, the Sharon Clements Biological Sciences Award and the BP Beirne Prize in Pest Management to AM, and by a Natural Sciences and Engineering Research Council of Canada - Industrial Research Chair to GG, with Scotts Canada Ltd. as the industrial sponsor. The research was approved and supported by the Animal Care Committee of Simon Fraser University (protocol #1159B-15).

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, Canada

    Antonia E. Musso, Regine Gries, Huimin Zhai, Stephen Takács & Gerhard Gries

Authors
  1. Antonia E. Musso
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Regine Gries
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Huimin Zhai
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stephen Takács
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gerhard Gries
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gerhard Gries.

Electronic supplementary material

ESM 1

(DOCX 97 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Musso, A.E., Gries, R., Zhai, H. et al. Effect of Male House Mouse Pheromone Components on Behavioral Responses of Mice in Laboratory and Field Experiments. J Chem Ecol 43, 215–224 (2017). https://doi.org/10.1007/s10886-017-0819-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-017-0819-y

Keywords

Search

Navigation