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Receiving behaviour is sensitive to risks from eavesdropping predators

  • Behavioral Ecology - Original Paper
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Abstract

Conspicuous signals may attract both intended receivers as well as unintended receivers such as predators. However, signalling individuals are not the only ones at risk when communicating, as the intended receiver may encounter eavesdropping predators that are attracted to the same signals. Here, we show that the house mouse (Mus domesticus) behaviourally responds to social signals (scents) as though receiving carries a risk of predation. We presented mice with their own scents (low social benefit to receiving) and those from an unknown “intruder” (high social benefit to receiving) under high (cat urine added) and low (water added) perceived predation risk. Mice traded-off the potential social benefits of receiving a signal against the costs of potential predator encounter. Receiving rates of both social signals (own and intruder) were high under low predation risk. Mice reduced receiving of both social signals when predation risk was increased; however, the effect was greater for their own low value scent than for the high social value intruder scent. Notably, rates of signalling did not vary with the level of perceived predation risk. Our findings suggest that mice traded-off the potential social benefits of receiving a signal (scent mark) against the costs of potential predator encounter. We suggest that, for some species, the costs of communication are borne more by the receivers than the signallers, and that the influence of risks to receivers on the design of communication systems may have been underestimated.

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References

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

    Google Scholar 

  • Banks PB (1998) Responses of Australian bush rats, Rattus fuscipes, to the odor of introduced Vulpes vulpes. J Mammal 79:1260–1264

    Article  Google Scholar 

  • Banks PB, Norrdahl K, Korpimäki E (2000) Nonlinearity in the predation risk of prey mobility. Proc R Soc Lond B 267:1621–1625

    Article  CAS  Google Scholar 

  • Belwood JJ, Morris GK (1987) Bat predation and its influence on calling behavior in neotropical katydids. Science 238:64–67

    Article  PubMed  Google Scholar 

  • Berton F, Vogel E, Belzung C (1998) Modulation of mice anxiety in response to cat odor as a consequence of predators diet. Physiol Behav 65:247–254

    Article  PubMed  CAS  Google Scholar 

  • Bertram SM, Orozco SX, Bellani R (2004) Temporal shifts in conspicuousness: mate attraction displays of the texas field cricket, Gryllus texensis. Ethology 110:963–975

    Article  Google Scholar 

  • Blanchard DC, Griebel G, Blanchard RJ (2001) Mouse defensive behaviors: pharmacological and behavioral assays for anxiety and panic. Neurosci Biobehav Rev 25:205–218

    Article  PubMed  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 

  • Brown JS (1988) Patch use as an indicator of habitat preference, predation risk and competition. Behav Ecol Sociobiol 22:37–47

    Article  Google Scholar 

  • Brown RE (1985) The rodents II: Suborder Myomorpha. In: Brown RE, MacDonald DW (eds) Social odours in mammals, vol 1. Clarendon Press, Oxford, pp 345–457

    Google Scholar 

  • Brown RE, MacDonald DW (1985) Social odours in mammals, vol 1 & 2. Clarendon Press, Oxford

    Google Scholar 

  • Corridi P, Chiarotti F, Bigi S, Alleva E (1993) Familiarity with conspecific odor and isolation induced aggressive-behavior in male-mice (Mus domesticus). J Comp Psychol 107:328–335

    Article  PubMed  CAS  Google Scholar 

  • Dawkins MS, Guilford T (1991) The corruption of honest signalling. Anim Behav 41:865–873

    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 

  • Dickman CR (1992) Predation and habitat shift in the house mouse, Mus domesticus. Ecology 73:313–322

    Article  Google Scholar 

  • Drickamer LC (1982) Acceleration and delay of sexual maturation in female mice via chemosignals: circadian rhythm effects. Biol Reprod 27:596–601

    Article  PubMed  CAS  Google Scholar 

  • Drickamer LC, Mikesic DG, Shaffer KS (1992) Use of odor baits in traps to test reactions to intraspecific and interspecific chemical cues in house mice living in outdoor enclosures. J Chem Ecol 18:2223–2250

    Article  CAS  Google Scholar 

  • Endler JA (1992) Signals, signal conditions and the direction of evolution. Am Nat 139:S125–S153

    Article  Google Scholar 

  • Endler JA (1993) Some general comments on the evolution and design of animal communication systems. Philos Trans R Soc Lond B 340:215–225

    Article  CAS  Google Scholar 

  • Fitzgerald BM, Turner DC (2000) Hunting behaviour of domestic cats and their impact on prey populations. In: Turner DC, Bateson P (eds) The domestic cat: the biology of its behaviour. Cambridge University Press, Cambridge, pp 151–175

    Google Scholar 

  • Gosling LM (1982) A reassessment of the function of scent marking in territories. Z Tierpsychol 60:89–118

    Google Scholar 

  • Gosling LM (1985) The even-toed ungulates: order Artiodactyla. In: Brown RE, MacDonald DW (eds) Social odours in mammals, vol 2. Oxford University Press, Oxford, pp 550–618

    Google Scholar 

  • Gosling LM, McKay HV (1990) Competitor assessment by scent matching: an experimental test. Behav Ecol Sociobiol 26:415–420

    Article  Google Scholar 

  • Grafe TU (1997) Costs and benefits of mate choice in the lek-breeding reed frog, Hyperolius marmoratus. Anim Behav 53:1103–1117

    Article  Google Scholar 

  • Hedrick AV, Dill LM (1993) Mate choice by female crickets is influenced by predation risk. Anim Behav 46:193–196

    Article  Google Scholar 

  • Hudson PJ (1992) Grouse in space and time: the population biology of a managed gamebird. Game Conservancy, Fordingbridge

    Google Scholar 

  • Humphries RE, Robertson DHL, Beynon RJ, Hurst JL (1999) Unravelling the chemical basis of competitive scent marking in house mice. Anim Behav 58:1177–1190

    Article  PubMed  Google Scholar 

  • Hurst JL (1987) The functions of urine marking in a free-living population of house mice, Mus domesticus Rutty. Anim Behav 35:1433–1442

    Article  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 (1993) The priming effects of urine substrate marks on interactions between male house mice, Mus musculus-domesticus Schwarz and Schwarz. Anim Behav 45:55–81

    Article  Google Scholar 

  • Hurst JL, Beynon RJ (2004) Scent wars: the chemobiology of competitive signalling in mice. BioEssays 26:1288–1298

    Article  PubMed  CAS  Google Scholar 

  • Hurst JL, Fang JM, Barnard CJ (1993) The role of substrate odors in maintaining social tolerance between male house mice, Mus musculus domesticus. Anim Behav 45:997–1006

    Article  Google Scholar 

  • Kimelman BR, Lubow RE (1974) The inhibitory effect of preexposed olfactory cues on intermale aggression in mice. Physiol Behav 12:919–922

    Article  PubMed  CAS  Google Scholar 

  • Kirkpatrick M (1996) Good genes and direct selection in evolution of mating preferences. Evolution 50:2125–2140

    Article  Google Scholar 

  • Kodric-Brown A (1989) Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Behav Ecol Sociobiol 25:393–401

    Article  Google Scholar 

  • Kotler BP, Brown JS, Hasson O (1991) Factors affecting gerbil foraging behavior and rates of owl predation. Ecology 72:2249–2260

    Article  Google Scholar 

  • Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659

    Article  Google Scholar 

  • Nevison CM, Armstrong S, Beynon RJ, Humphries RE, Hurst JL (2003) The ownership signature in mouse scent marks is involatile. Proc R Soc Lond B 270:1957–1963

    Article  CAS  Google Scholar 

  • Newsome AE (2002) Cat, Felis catus. In: Strahan R (ed) The Mammals of Australia. Reed New Holland, Sydney, pp 700–702

    Google Scholar 

  • Peake TM (2005) Eavesdropping in communication networks. In: McGregor PK (ed) Animal communication networks. Cambridge University Press, Cambridge, pp 13–37

    Google Scholar 

  • Pocklington R, Dill LM (1995) Predation on females or males: who pays for bright male traits? Anim Behav 49:1122–1124

    Article  Google Scholar 

  • Read J, Bowen Z (2001) Population dynamics, diet and aspects of the biology of feral cats and foxes in arid South Australia. Wildl Res 28:195–203

    Article  Google Scholar 

  • Roberts SC (2007) Scent marking. In: Wolff JO, Sherman PW (eds) Rodent societies: an ecological and evolutionary perspective. University of Chicago Press, Chicago, pp 255–266

    Google Scholar 

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

    Article  Google Scholar 

  • Rosenthal GG, Martinez TYF, de Leon FJG, Ryan MJ (2001) Shared preferences by predators and females for male ornaments in swordtails. Am Nat 158:146–154

    Article  PubMed  CAS  Google Scholar 

  • Ryan MJ, Wagner WE (1987) Asymmetries in mating preferences between species—female swordtails prefer heterospecific males. Science 236:595–597

    Article  PubMed  Google Scholar 

  • Ryan MJ, Tuttle MD, Taft LK (1981) The costs and benefits of frog chorusing behavior. Behav Ecol Sociobiol 8:273–278

    Article  Google Scholar 

  • Sakaluk SK, Belwood JJ (1984) Gecko phonotaxis to cricket calling song—a case of satellite predation. Anim Behav 32:659–662

    Article  Google Scholar 

  • Singleton GR (2002) House mouse, Mus musculus. In: Strahan R (ed) The mammals of Australia, 2nd edn. Reed New Holland, Sydney, pp 646–647

    Google Scholar 

  • Singleton G, Krebs CJ, Davis S, Chambers L, Brown P (2001) Reproductive changes in fluctuating house mouse populations in southeastern Australia. Proc R Soc Lond B 268:1741–1748

    Article  CAS  Google Scholar 

  • Storaas T, Kastdalen L, Wegge P (1999) Detection of forest grouse by mammalian predators: a possible explanation for high brood losses in fragmented landscapes. Wildl Biol 5:187–192

    Google Scholar 

  • Wolff JO (2004) Scent marking by voles in response to predation risk—a field-laboratory validation. Behav Ecol 15:286–289

    Article  Google Scholar 

  • Wyatt TD (2003) Pheromones and animal behaviour: communication by smell and taste. Cambridge University Press, Cambridge

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zuk M, Kolluru GR (1998) Exploitation of sexual signals by predators and parasitoids. Q Rev Biol 73:415–438

    Article  Google Scholar 

Download references

Acknowledgments

We thank CSIRO’s Rodent Research Group and the Mallee Research Station for access to mouse enclosures and the Randwick Veterinary Clinic for cat urine. We are grateful to J. Bytheway and C. Lewis for assistance in the field. Earlier drafts of this manuscript were improved by comments from C. Price, A. Lothian, A. Carthey, E. Lee, A. Munn and S. Pryke. This research was conducted with the permission of the UNSW Animal Care and Ethics Committee (permission no. ACE 0598A).

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  1. Jennifer L. Kelley

    Present address: Centre for Evolutionary Biology, School of Animal Biology, University of Western Australia, Perth, WA, 6009, Australia

Authors and Affiliations

  1. School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, 2052, Australia

    Nelika K. Hughes, Jennifer L. Kelley & Peter B. Banks

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  1. Nelika K. Hughes
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  2. Jennifer L. Kelley
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  3. Peter B. Banks
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Correspondence to Nelika K. Hughes.

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Communicated by Janne Sundell.

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Hughes, N.K., Kelley, J.L. & Banks, P.B. Receiving behaviour is sensitive to risks from eavesdropping predators. Oecologia 160, 609–617 (2009). https://doi.org/10.1007/s00442-009-1320-2

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