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House Mouse (Mus musculus) Avoidance of Olfactory Cues from Ferrets and Other Mammalian and Reptilian Predators: Preliminary Results

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Chemical Signals in Vertebrates 14

Abstract

Like other small rodents, house mice (Mus musculus) are at the bottom of vertebrate predator -dominated food chain. After humans, house mice are the most widespread mammal on earth. With their short reproductive cycle and prolificity, they can quickly produce large populations that form a basic source of nutrients for a wide spectrum of predators. As macrosmatic animals, mice use olfaction as a primary tool to avoid predators. However, further research is required to fully understand the main predator olfactory cues and behavioral reactions linked to these stimuli . This study examines the chemical cues used by house mice to detect mammalian and reptilian predators. For this purpose, we carried out a choice test where, during a 10 min period, we measured the total duration that mice remained in either the area closest to or farthest from the predatory stimulus (ferret fur and faeces , snake sheds, fox faeces , dog faeces , and cat urine ); mice had no physical access to the stimulus, and both compared areas were identical. Our preliminary results show that mice significantly avoided ferret olfactory stimuli from fur and faeces . The other predator stimuli did not elicit significant avoidance . However, in some cases, this may be due to specific genetic and phenotypic features of the mouse strain tested. Our results are in line with previous work with ferret olfactory stimuli in mice . Nevertheless, further research should examine the role of ferret olfactory cues and semiochemicals as good indicators of their presence that lead to avoidance behaviour of rodents.

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References

  • Abrams PA (2000) The evolution of predator-prey interactions: theory and evidence. Annu Rev Ecol Syst 31:79–105

    Article  Google Scholar 

  • Alexander PDT (1951) A history of the ferret. J Hist Med 6:471–480

    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(8):1123–1144

    Article  Google Scholar 

  • Apfelbach R, Soini HA, Vasilieva NY, Novotny MV (2015) Behavioral responses of predator-naïve dwarf hamsters (Phodopus campbelli) to odor cues of the European ferret fed with different prey species. Physiol Behav 146:57–66

    Article  CAS  Google Scholar 

  • Apfelbach R, Wiest H, Vasilieva NY (2001) Ferret (Mustela putorius f. furo) odor affects the estrous cycle in Campbell’ s hamster females (Phodopus campbelli). Wiss Mitt Niederösterr Landesmuseum 14:147–152

    Google Scholar 

  • AVMA (2012) U.S. pet ownership & demographics sourcebook

    Google Scholar 

  • Banks PB, Daly A, Bytheway JP (2016) Predator odours attract other predators, creating an olfactory web of information. Biol Lett 12:20151053

    Article  Google Scholar 

  • Boursot P, Auffray JC, Britton-Davidian J, Bonhomme F (1993) The evolution of house mice. Annu Rev Ecol Syst 24:119–152

    Article  Google Scholar 

  • Bradley T, Lightfoot TL, Mayer J (2006) Exotic pet behaviour: birds, reptiles and small mammals, 1st edn. Saunders Elsevier, St. Louis

    Google Scholar 

  • Bramley GN, Waas JR (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

    Article  CAS  Google Scholar 

  • Bramley GN, Waas JR, Henderson HV (2000) Responses of wild Norway rats (Rattus norvegicus) to predator odors. J Chem Ecol 26:705–719

    Article  CAS  Google Scholar 

  • Bull JW, Maron M (2016) How humans drive speciation as well as extinction. Proc R Soc B Biol Sci 283:20160600

    Article  Google Scholar 

  • Buron G, Hacquemand R, Pourie G et al (2007) Comparative behavioral effects between synthetic 2,4,5-trimethylthiazoline (TMT) and the odor of natural fox (Vulpes vulpes) feces in mice. Behav Neurosci 121:1063–1072

    Article  Google Scholar 

  • Bytheway JP, Carthey AJR, Banks PB (2013) Risk vs. reward: how predators and prey respond to aging olfactory cues. Behav Ecol Sociobiol 67:715–725

    Article  Google Scholar 

  • Brinck C, Erlinge S, Sandell M (1983) Anal secretion in mustelids. J Chem Ecol 9:727–745

    Article  CAS  Google Scholar 

  • Capitani C, Bertelli I, Varuzza P et al (2004) A comparative analysis of wolf (Canis lupus) diet in three different Italian ecosystems. Mamm Biol—Zeitschrift für Säugetierkd 69:1–10

    Article  Google Scholar 

  • Church B (2007) Ferret-polecat domestication: genetic,taxonomic and phylogenetic relationships. In: Lewington JH (ed) Ferret husbandry, medicine and surgery, second. Saunders Elsevier, Philadelphia, pp 122–150

    Chapter  Google Scholar 

  • Clapperton BK (1985) Olfactory communication in the ferret (Mustela furo L.) and its application in wildlife management. Massey University

    Google Scholar 

  • Clapperton BK, Minot EO, Crump DR (1989) Scent lures from anal sac secretions of the ferret Mustela furo L. J Chem Ecol 15:291–308

    Article  CAS  Google Scholar 

  • Coborn J (1991) The atlas of snakes of the world, 1st edn. T.F.H Publications

    Google Scholar 

  • de Oliveira Crisanto K, de Andrade WMG, de Azevedo Silva KD et al (2015) The differential mice response to cat and snake odor. Physiol Behav 152:272–279

    Article  Google Scholar 

  • Dell’Omo G, Fiore M, Alleva E (1994) Strain differences in mouse response to odours of predators. Behav Processes 32:105–116

    Article  Google Scholar 

  • Díaz-Perales A, González de Olano D, Pérez-Gordo M, Pastor-Vargas C (2013) Allergy to uncommon pets: new allergies but the same allergens. Front Immunol 4:3–8

    Article  Google Scholar 

  • Díaz-Ruiz F, Delibes-Mateos M, García-Moreno JL et al (2013) Biogeographical patterns in the diet of an opportunistic predator: the red fox Vulpes vulpes in the Iberian Peninsula. Mamm. Rev. 43:59–70

    Article  Google Scholar 

  • Dietl G, Kelley P (2002) The fossil record of predator-prey arms races: coevolution and escalation hypotheses. Paleontol Soc Pap 8:353–374

    Article  Google Scholar 

  • Fendt M (2006) Exposure to urine of canids and felids, but not of herbivores, induces defensive behavior in laboratory rats. J Chem Ecol 32:2617–2627

    Article  CAS  Google Scholar 

  • Ferrero DM, Lemon JK, Fluegge D et al (2011) Detection and avoidance of a carnivore odor by prey. Proc Natl Acad Sci U S A 108:11235–11240

    Article  CAS  Google Scholar 

  • Goto T, Tanave A, Moriwaki K et al (2013) Selection for reluctance to avoid humans during the domestication of mice. Genes Brain Behav 12:760–770

    Article  CAS  Google Scholar 

  • Graphodatsky AS, Trifonov VA, Stanyon R (2011) The genome diversity and karyotype evolution of mammals. Mol Cytogenet 4:22

    Article  Google Scholar 

  • Hacquemand R, Jacquot L, Brand G (2010) Comparative fear-related behaviors to predator odors (TMT and natural fox feces) before and after Intranasal ZnSO4 treatment in mice. Front Behav Neurosci 4:188

    Article  CAS  Google Scholar 

  • Hanski I, Hansson L, Henttonen H (1991) Specialist predators, generalist predators, and the microtine rodent cycle. J Anim Ecol 60:353–367

    Article  Google Scholar 

  • Hess SE, Rohr S, Dufour BD et al (2008) Home improvement: C57BL/6J mice given more naturalistic nesting materials build better nests. J Am Assoc Lab Anim Sci 47:25–31

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hurst JL, West RS (2010) Taming anxiety in laboratory mice. Nat Methods 7:825–826

    Article  CAS  Google Scholar 

  • Jacobson ER (2007) Infectious diseases and pathology of reptiles, first. Taylor & Francis, London

    Book  Google Scholar 

  • Kimoto H, Haga S, Sato K, Touhara K (2005) Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437:898–901

    Article  CAS  Google Scholar 

  • Konradsen JR, Fujisawa T, van Hage M et al (2015) Allergy to furry animals: new insights, diagnostic approaches, and challenges. J Allergy Clin Immunol 135:616–625

    Article  Google Scholar 

  • Lanszki J, Heltai M (2007) Diet of the European polecat and the steppe polecat in Hungary. Mamm Biol 72:49–53

    Article  Google Scholar 

  • Leckie FM, Thirgood SJ, May R, Redpath SM (1998) Variation in the diet of red foxes on Scottish moorland in relation to prey abundance. Ecography (Cop) 21:599–604

    Article  Google Scholar 

  • Lodé T (1997) Trophic status and feeding habits of the European Polecat Mustela putorius L. 1758. Mamm Rev 27:177–184

    Article  Google Scholar 

  • Lowry H, Lill A, Wong BBM (2013) Behavioural responses of wildlife to urban environments. Biol Rev Camb Philos Soc 88:537–549

    Article  Google Scholar 

  • Masini CV, Sauer S, Campeau S (2005) Ferret odor as a processive stress model in rats: neurochemical, behavioral, and endocrine evidence. Behav Neurosci 119:280–292

    Article  CAS  Google Scholar 

  • Masini CV, Sauer S, White J et al (2006) Non-associative defensive responses of rats to ferret odor. Physiol Behav 87:72–81

    Article  CAS  Google Scholar 

  • Mason RT, Parker MR (2010) Social behavior and pheromonal communication in reptiles. J Comp Physiol Neuroethol SensY, Neural, Behav Physiol 196:729–749

    Article  CAS  Google Scholar 

  • McLennan IS, Taylor-Jeffs J (2004) The use of sodium lamps to brightly illuminate mouse houses during their dark phases. Lab Anim 38:384–392

    Article  CAS  Google Scholar 

  • Miyazaki M, Yamashita T, Hosokawa M, et al (2006a) Species-, sex-, and age-dependent urinary excretion of cauxin, a mammalian carboxylesterase. Comp Biochem Physiol B Biochem Mol Biol 145:270–277

    Article  Google Scholar 

  • Miyazaki M, Yamashita T, Suzuki Y, et al (2006b) A major urinary protein of the domestic cat regulates the production of felinine, a putative pheromone precursor. Chem Biol 13:1071–1079

    Article  CAS  Google Scholar 

  • Nolte DL, Mason JR, Epple G et al (1994) Why are predator urines aversive to prey? J Chem Ecol 20:1505–1516

    Article  CAS  Google Scholar 

  • Osada K, Miyazono S, Kashiwayanagi M (2015) The scent of wolves: pyrazine analogs induce avoidance and vigilance behaviors in prey. Front Neurosci 9:363

    Article  Google Scholar 

  • Papes F, Logan DW, Stowers L (2010) The vomeronasal organ mediates interspecies defensive behaviour through detection of protein pheromone homologs. Cell 141:692–703

    Article  CAS  Google Scholar 

  • Parker MR, Mason RT (2011) Pheromones in snakes: history, patterns and future research directions. Reprod Biol Phylogeny Snakes 552–571

    Google Scholar 

  • Pillay N, Alexander GJ, Lazenby SL (2003) Responses of striped mice, Rhabdomys pumilio, to faeces of a predatory snake. Behaviour 140:125–135

    Article  Google Scholar 

  • Pleguezuelos JM, Fernández-Cardenete JR, Honrubia S et al (2007) Correlates between morphology, diet and foraging mode in the ladder snake Rhinechis scalaris (Schinz, 1822). Contrib to Zool 76:179–186

    Article  Google Scholar 

  • Reyes-Velasco J, Card DC, Andrew AL et al (2015) Expression of venom gene homologs in diverse python tissues suggests a new model for the evolution of snake venom. Mol Biol Evol 32:173–183

    Article  CAS  Google Scholar 

  • Roberts S a, Simpson DM, Armstrong SD, et al (2010) Darcin: a male pheromone that stimulates female memory and sexual attraction to an individual male’s odour. BMC Biol 8:75

    Article  Google Scholar 

  • Roberts SC, Gosling LM, Thornton E a, Mcclung J (2001) Scent-marking by male mice under the risk of predation. Behav Ecol 12:698–705

    Article  Google Scholar 

  • Rosen JB, Asok A, Chakraborty T (2015) The smell of fear: innate threat of 2,5-dihydro-2,4,5-trimethylthiazoline, a single molecule component of a predator odor. Front. Neurosci. 9:292

    PubMed  PubMed Central  Google Scholar 

  • Santos MJ, Matos HM, Baltazar C et al (2009) Is polecat (Mustela putorius) diet affected by “mediterraneity”? Mamm Biol 74:448–455

    Article  Google Scholar 

  • Saviozzi P, Zuffi MAL (1997) An integrated approach to the study of diet of Vipera aspis. Herpetol Rev 28:23–24

    Google Scholar 

  • Shine R, Mason RT (2012) An airborne sex pheromone in snakes. Biol Lett 8:183–185

    Article  CAS  Google Scholar 

  • Sievert T, Laska M (2016) Behavioral responses of CD-1 mice to six predator odor components. Chem Senses 00:bjw015

    Google Scholar 

  • Spotte S (2014) Free-ranging cats. Behav Ecol Manag

    Google Scholar 

  • Stempel H, Jung M, Pérez-Gómez A et al (2016) Strain-specific loss of formyl peptide receptor 3 in the murine vomeronasal and immune systems. J Biol Chem 291:9762–9775

    Article  CAS  Google Scholar 

  • Sullivan AM, Maerz JC, Madison DM (2002) Anti-predator response of red-backed salamanders (Plethodon cinereus) to chemical cues from garter snakes (Thamnophis sirtalis): laboratory and field experiments. Behav Ecol Sociobiol 51:227–233

    Article  Google Scholar 

  • Tu MC, Lillywhite HB, Menon JG, Menon GK (2002) Postnatal ecdysis establishes the permeability barrier in snake skin: new insights into barrier lipid structures. J Exp Biol 205:3019–3030

    CAS  PubMed  Google Scholar 

  • Uetz P, Hallermann J, Hosek J (2017) www.reptiledatabase.org

  • Vasilieva NY, Cherepanova EV, von Holst D, Apfelbach R (2000) Predator odour and its impact on male fertility and reproduction in Phodopus campbelli hamsters. Naturwissenschaften 87:312–314

    Article  CAS  Google Scholar 

  • Voznessenskaya VV (2014) Influence of cat odor on reproductive behavior and physiology in the house mouse: Mus musculus. CRC Press/Taylor & Francis

    Google Scholar 

  • Wagner C, Holzapfel M, Kluth G et al (2012) Wolf (Canis lupus) feeding habits during the first eight years of its occurrence in Germany. Mamm Biol 77:196–203

    Article  Google Scholar 

  • Wahlsten D, Crabbe JC (2007) Chapter 15 behavioral testing. In: The mouse in biomedical research

    Google Scholar 

  • Wasko DK, Bonilla F, Sasa M (2014) Behavioral responses to snake cues by three species of Neotropical rodents. J Zool 292:142–150

    Article  Google Scholar 

  • Webb JK, Du W, Pike D, Shine R (2010) Generalization of predator recognition: velvet geckos display anti-predator behaviours in response to chemicals from non-dangerous elapid snakes. Curr Zool 56:337–342

    Google Scholar 

  • Weldon PJ, Divita FM, Middendorf GA (1987) Responses to snake odors by laboratory mice. Behav Process 14:137–146

    Article  CAS  Google Scholar 

  • Wyatt TD (2014) Proteins and peptides as pheromone signals and chemical signatures. Anim Behav 97:273–280

    Article  Google Scholar 

  • Zhang J-X, Soini HA, Bruce KE et al (2005) Putative chemosignals of the ferret (Mustela furo) associated with individual and gender recognition. Chem Senses 30:727–737

    Article  CAS  Google Scholar 

  • Zhang J-X, Sun L, Bin Zhang Z et al (2002) Volatile compounds in anal gland of Siberian weasels (Mustela sibirica) and steppe polecats (M. eversmanni). J Chem Ecol 28:1287–1297

    Article  CAS  Google Scholar 

  • Zimmerling LM, Sullivan TP (1994) Influence of mustelid semiochemicals on population dynamics of the deer mouse (Peromyscos maniculatus). J Chem Ecol 20:667–689

    Article  CAS  Google Scholar 

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Acknowledgements

We acknowledge X. Duchemin and X. Bonnet for the snake sheds, and E. Landen for English proofreading.

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Correspondence to Carlos Grau .

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Grau, C., Teruel, E., Leclercq, J., Pageat, P. (2019). House Mouse (Mus musculus) Avoidance of Olfactory Cues from Ferrets and Other Mammalian and Reptilian Predators: Preliminary Results. In: Buesching, C. (eds) Chemical Signals in Vertebrates 14. Springer, Cham. https://doi.org/10.1007/978-3-030-17616-7_13

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