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
Alexander PDT (1951) A history of the ferret. J Hist Med 6:471–480
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
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
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
AVMA (2012) U.S. pet ownership & demographics sourcebook
Banks PB, Daly A, Bytheway JP (2016) Predator odours attract other predators, creating an olfactory web of information. Biol Lett 12:20151053
Boursot P, Auffray JC, Britton-Davidian J, Bonhomme F (1993) The evolution of house mice. Annu Rev Ecol Syst 24:119–152
Bradley T, Lightfoot TL, Mayer J (2006) Exotic pet behaviour: birds, reptiles and small mammals, 1st edn. Saunders Elsevier, St. Louis
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
Bramley GN, Waas JR, Henderson HV (2000) Responses of wild Norway rats (Rattus norvegicus) to predator odors. J Chem Ecol 26:705–719
Bull JW, Maron M (2016) How humans drive speciation as well as extinction. Proc R Soc B Biol Sci 283:20160600
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
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
Brinck C, Erlinge S, Sandell M (1983) Anal secretion in mustelids. J Chem Ecol 9:727–745
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
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
Clapperton BK (1985) Olfactory communication in the ferret (Mustela furo L.) and its application in wildlife management. Massey University
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
Coborn J (1991) The atlas of snakes of the world, 1st edn. T.F.H Publications
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
Dell’Omo G, Fiore M, Alleva E (1994) Strain differences in mouse response to odours of predators. Behav Processes 32:105–116
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
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
Dietl G, Kelley P (2002) The fossil record of predator-prey arms races: coevolution and escalation hypotheses. Paleontol Soc Pap 8:353–374
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
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
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
Graphodatsky AS, Trifonov VA, Stanyon R (2011) The genome diversity and karyotype evolution of mammals. Mol Cytogenet 4:22
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
Hanski I, Hansson L, Henttonen H (1991) Specialist predators, generalist predators, and the microtine rodent cycle. J Anim Ecol 60:353–367
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
Hurst JL, West RS (2010) Taming anxiety in laboratory mice. Nat Methods 7:825–826
Jacobson ER (2007) Infectious diseases and pathology of reptiles, first. Taylor & Francis, London
Kimoto H, Haga S, Sato K, Touhara K (2005) Sex-specific peptides from exocrine glands stimulate mouse vomeronasal sensory neurons. Nature 437:898–901
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
Lanszki J, Heltai M (2007) Diet of the European polecat and the steppe polecat in Hungary. Mamm Biol 72:49–53
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
Lodé T (1997) Trophic status and feeding habits of the European Polecat Mustela putorius L. 1758. Mamm Rev 27:177–184
Lowry H, Lill A, Wong BBM (2013) Behavioural responses of wildlife to urban environments. Biol Rev Camb Philos Soc 88:537–549
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
Masini CV, Sauer S, White J et al (2006) Non-associative defensive responses of rats to ferret odor. Physiol Behav 87:72–81
Mason RT, Parker MR (2010) Social behavior and pheromonal communication in reptiles. J Comp Physiol Neuroethol SensY, Neural, Behav Physiol 196:729–749
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
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
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
Nolte DL, Mason JR, Epple G et al (1994) Why are predator urines aversive to prey? J Chem Ecol 20:1505–1516
Osada K, Miyazono S, Kashiwayanagi M (2015) The scent of wolves: pyrazine analogs induce avoidance and vigilance behaviors in prey. Front Neurosci 9:363
Papes F, Logan DW, Stowers L (2010) The vomeronasal organ mediates interspecies defensive behaviour through detection of protein pheromone homologs. Cell 141:692–703
Parker MR, Mason RT (2011) Pheromones in snakes: history, patterns and future research directions. Reprod Biol Phylogeny Snakes 552–571
Pillay N, Alexander GJ, Lazenby SL (2003) Responses of striped mice, Rhabdomys pumilio, to faeces of a predatory snake. Behaviour 140:125–135
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
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
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
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
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
Santos MJ, Matos HM, Baltazar C et al (2009) Is polecat (Mustela putorius) diet affected by “mediterraneity”? Mamm Biol 74:448–455
Saviozzi P, Zuffi MAL (1997) An integrated approach to the study of diet of Vipera aspis. Herpetol Rev 28:23–24
Shine R, Mason RT (2012) An airborne sex pheromone in snakes. Biol Lett 8:183–185
Sievert T, Laska M (2016) Behavioral responses of CD-1 mice to six predator odor components. Chem Senses 00:bjw015
Spotte S (2014) Free-ranging cats. Behav Ecol Manag
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
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
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
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
Voznessenskaya VV (2014) Influence of cat odor on reproductive behavior and physiology in the house mouse: Mus musculus. CRC Press/Taylor & Francis
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
Wahlsten D, Crabbe JC (2007) Chapter 15 behavioral testing. In: The mouse in biomedical research
Wasko DK, Bonilla F, Sasa M (2014) Behavioral responses to snake cues by three species of Neotropical rodents. J Zool 292:142–150
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
Weldon PJ, Divita FM, Middendorf GA (1987) Responses to snake odors by laboratory mice. Behav Process 14:137–146
Wyatt TD (2014) Proteins and peptides as pheromone signals and chemical signatures. Anim Behav 97:273–280
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
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
Zimmerling LM, Sullivan TP (1994) Influence of mustelid semiochemicals on population dynamics of the deer mouse (Peromyscos maniculatus). J Chem Ecol 20:667–689
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We acknowledge X. Duchemin and X. Bonnet for the snake sheds, and E. Landen for English proofreading.
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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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