Accessible Unlicensed Requires Authentication Published by De Gruyter August 3, 2020

Do prairie voles (Microtus ochrogaster) change their activity and space use in response to domestic cat (Felis catus) excreta?

Brian Keane, Phillip J. Long, Yasmeen Fleifil and Nancy G. Solomon
From the journal Mammalia


Behavioral changes that reduce the risk of predation in response to predator-derived odor cues are widespread among mammalian taxa and have received a great deal of attention. Although voles of the genus Microtus are staples in the diet of many mammalian predators, including domestic cats (Felis catus), there are no previous studies on vole space utilization and activity levels in response to odor cues from domestic cats. Therefore, the objective of our study was to investigate responses of adult prairie voles (Microtus ochrogaster) living in semi-natural habitats to odor cues from domestic cat excreta. Contrary to expectations, neither adult males or females showed significant changes in space use or willingness to enter traps in response to cat odors. One hypothesis to explain our results are that prairie voles have not co-evolved with domestic cats long enough to respond to their odors. Other possible explanations include whether levels of odors in the environment were sufficient to trigger a response or that the perceived risk of predation from odor cues alone did not outweigh relative costs of changing space use and activity levels. Future studies should consider multiple factors when determining what cues are sufficient to elicit antipredatory behavior.

Corresponding author: Brian Keane, Department of Biological Sciences and Center for Animal Behavior, Miami University - Regionals, Hamilton, OH, 45011, USA,

Funding source: National Science Foundation

Award Identifier / Grant number: IOB0614015

Funding source: National Science Foundation - Research Experience for Undergraduates

Award Identifier / Grant number: DBI-0353915


Thanks to Rodney Kolb and the staff at Miami University’s Ecology Research Center for all their help with the logistics of this project. We thank Adam Blundell, Jennifer Corman, Kristin Gunter, Hillary Hoffman Adam Litz, and Lindsey Williams for their help with field work during summer 2007. We also thank staff at the Animal Adoption Foundation, Hamilton, OH for providing the cat litter with cat excreta. We thank Hank Stevens for providing advice on data analysis and Jacob Schlichter for assistance with checking data.

  1. Author contribution: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: This research was supported by a NSF-REU grant (DBI-0353915) to PJL and a NSF grant (IOB0614015) to BK and NGS.

  3. Conflict of interest statement: The authors declare no conflicts of interest regarding this article.


Anisman, H., Hayley, S., Kelly, O., Borowski, T., and Merali, Z. (2001). Psychogenic, neurogenic, and systemic stressor effects on plasma corticosterone and behavior: mouse strain-dependent outcomes. Behav. Neurosci. 115: 443–454, Search in Google Scholar

Apfelbach, R., Blanchard, C.D., Blanchard, R.J., Hayes, R.A., and McGregor, I.S. (2005). The effects of predator odors in mammalian prey species: a review of field and laboratory studies. Neurosci. Biobehav. Rev. 29: 1123–1144, Search in Google Scholar

Arias-Del Razo, I., Hernández, L., Laundré, J.W., and VelascoVázquez, L. (2012). The landscape of fear: habitat use by a predator (Canis latrans) and its main prey (Lepus californicus and Sylvilagus audubonii). Can. J. Zool. 90: 683–693, Search in Google Scholar

Banks, P.B. (1998). Responses of Australian bush rats, Rattus fuscipes, to the odor of introduced Vulpes vulpes. J. Mammal. 79: 1260–1264, Search in Google Scholar

Banks, P.B. and Dickman, C.R. (2007). Alien predation and the effects of multiple levels of prey naivete. Trends Ecol. Evol. 22: 229–230, Search in Google Scholar

Banks, P.B., Nelika, K., Hughes, A., and Rose, T. (2003). Do native Australian small mammals avoid faeces of domestic dogs? Responses of Rattus fuscipes and Antechinus stuartii. Aust. Zool. 32: 406–409, Search in Google Scholar

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

Blanchard, D.C., Markham, C., Yang, M., Hubbard, D., Madarang, E., and Blanchard, R.J. (2003). Failure to produce conditioning with low-dose trimethylthiazoline or cat feces as unconditioned stimuli. Behav. Neurosci. 117: 360–368, Search in Google Scholar

Blumstein, D.T., Barrow, L., and Luterra, M. (2008). Olfactory predator discrimination in yellow-bellied marmots. Ethology 114: 1135–1143, Search in Google Scholar

Bolbroe, T., Jeppesen, L.L., and Leirs, H. (2000). Behavioural response of field voles under mustelid predation risk in the laboratory: more than neophobia. Ann. Zool. Fenn. 37: 169–178. Search in Google Scholar

Borowski, Z. (1998a). Influence of predator odour on the feeding behavior of the root vole (Microtus oeconomus Pallas, 1776). Can. J. Zool. 76: 1791–1794, Search in Google Scholar

Borowski, Z. (1998b). Influence of weasel (Mustela nivalis Linneaus, 1776) odour on spatial behaviour of root voles (Microtus oeconomus Pallas, 1776). Can. J. Zool. 76: 1799–1804, Search in Google Scholar

Borowski, Z. (2002). Individual and seasonal differences in antipredatory behaviour of root voles—a field experiment. Can. J. Zool. 80: 1520–1525, Search in Google Scholar

Brachetta, V., Schleich, C.E., and Zenuto, R.R. (2016). Source odor, intensity, and exposure pattern affect antipredatory responses in the subterranean rodent Ctenomys talarum. Ethology 122: 923–936, Search in Google Scholar

Bradbury, J.W. and Vehrencamp, S.L. (1998). Principles of animal communication. Sinauer, Sunderland, MA. Search in Google Scholar

Bramley, G.N. and Waas, J.R. (2001). Laboratory and field evaluation of predator odors as repellents for kiore (Rattus exulans) and ship rats (Rattus rattus). J. Chem. Ecol. 27: 1029–1047, Search in Google Scholar

Chaline, J., Brunet-Lecomte, P., Montuire, S., Viriot, L., and Courant, F. (1999). Anatomy of the arvicoline radiation (Rodentia): palaeogeographical, palaeoecological history and evolutionary data. Ann. Zool. Fenn. 36: 239–267. Search in Google Scholar

Cochran, G.R. and Solomon, N.G. (2000). Effects of food supplementation on the social organization of prairie voles (Microtus ochrogaster). J. Mammal. 81: 746–757, Search in Google Scholar

Desy, E.A. and Batzli, G.O. (1989). Effects of food availability and predation on prairie vole demography: a field experiment. Ecology 70: 411–421, Search in Google Scholar

Dickman, C.R. (1992). Predation and habitat shift in the house mouse, Mus domesticus. Ecology 73: 313–322, Search in Google Scholar

Dickman, C.R. (1993). Raiders of the last ark: cats in inland Australia. Aust. Nat. Hist. 24: 44–52. Search in Google Scholar

Dickman, C.R. (1996). Overview of the impacts of feral cats on Australian native fauna. Australian Nature Conservation Agency, Canberra, ACT, Australia. Search in Google Scholar

Dielenberg, R.A. and McGregor, I.S. (1999). Habituation of the hiding response to predatory odor in rats (Rattus norvegicus). J. Comp. Psychol. 113: 376–387, Search in Google Scholar

Drickamer, L.C., Mikesic, D.G., and Shaffer, K.S. (1992). Use of odor baits in traps to test reactions to intra- and interspecific cues in house mice living in outdoor enclosures. J. Chem. Ecol. 18: 2223–2250, Search in Google Scholar

Epple, G., Mason, J., Nolte, D., and Campbell, D. (1993). Effects of predator odors on feeding in the mountain beaver Aplodontia rufa. J. Mammal. 74: 715–722, Search in Google Scholar

Esparza-Carlos, J.P., Íñiguez-Dávalos, L.I., and Laundré, J. (2018). Microhabitat and presence of top predators affect prey apprehension in a subtropical mountain forest. J. Mammal. 99: 596–607, Search in 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, Search in Google Scholar

Ferkin, M.H., Mech, S.G., and Paz-y-Miño, C.G. (2001). Scent marking in meadow voles and prairie voles: a test of three hypotheses. Behaviour 138: 1319–1336, Search in Google Scholar

File, S.E., Zangrossi, H.Jr, Sanders, F.L., and Mabbutt, P.S. (1993). Dissociation between behavioral and corticosterone responses on repeated exposures to cat odor. Physiol. Behav. 54: 1109–1111, Search in Google Scholar

Fletcher, Q.E. and Boonstra, R. (2006). Do captive male meadow voles experience acute stress in response to weasel odour?. Can. J. Zool. 84: 583–588, Search in Google Scholar

Gail, B.G. and Mathis, A. (2010). Innate predator recognition and the problem of introduced trout. Ethology 116: 47–58, Search in Google Scholar

Getz, L.L. (1985). Habitats, pp. 286–309. In: Tamarin, R.H. (Ed.), Biology of Microtus. Special Publication No. 8. American Society of Mammalogists, Shippensburg University, Shippensburg, PA, p. 893. Search in Google Scholar

Getz, L.L., McGuire, B., Pizzuto, T., Hofmann, J.E., and Frase, B. (1993). Social organization of the prairie vole (Microtus ochrogaster). J. Mammal. 74: 44–58, Search in Google Scholar

Getz, L.L., Hofmann, J.E., McGuire, B., and Dolan, T.W. (2001). Twenty-five years of population fluctuations of Microtus ochrogaster and M. pennsylvanicus in three habitats in east-central Illinois. J. Mammal. 82: 22–34, Search in Google Scholar

George, G.W. (1974). Domestic cats as predators and factors in winter shortages of raptor prey. Wilson Bull. 86: 384–396. Search in Google Scholar

Hegab, I.M., Jin, Y., Ye, M., Wang, A., Yin, B., Yang, S., and Wei, W. (2014). Defensive responses of Brandti’s voles (Lasiopodomys brandtii) to stored cat feces. Physiol. Behav. 123: 193–199, Search in Google Scholar

Hutchings, M. R. and White, P.C.L. (2000). Mustelid scent-marking in managed ecosystems: implications for population management. Mamm Rev. 30: 157–169., Search in Google Scholar

Jêdrzejewski, W. and Jêdrzejewska, B. (1990). Effect of a predatoris’s visit on the spatial distribution of bank voles: experiments with weasels. Can. J. Zool. 68: 660–666, Search in Google Scholar

Jike, L., Batzli, G.O., and Getz, L.L. (1988). Home ranges of prairie voles as determined by radiotracking and powdertracking. J. Mammal. 69: 183–186, Search in Google Scholar

Johnston, R.E. (2003). Chemical communication in rodents: from pheromones to individual recognition. J. Mammal. 84: 1141–1162, Search in Google Scholar

Kats, L.B. and Dill, L.M. (1998). The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5: 361–394, Search in Google Scholar

Keane, B., Castelli, F.R., Davis, H., Crist, T.O., and Solomon, N.G. (2017). Effects of avpr1a length polymorphism on male social behavior and reproduction in semi-natural populations of prairie voles (Microtus ochrogaster). Ethology 123: 675–688, Search in Google Scholar

Koehler, G.M. and Hornocker, M.G. (1991). Seasonal resource use among mountain lions, bobcats, and coyotes. J. Mammal. 72: 391–396, Search in Google Scholar

Kovacs, E.K., Crowther, M.S., Webb, J.K., and Dickman, C.R. (2012). Population and behavioural responses of native prey to alien predation. Oecologia 168: 947–957, Search in Google Scholar

Kwak, J., Grigsby, C.C., Preti, G., Rizki, M.M., Yamazaki, K., and Beauchamp, G.K. (2013). Changes in volatile compounds of mouse urine as it ages: their interactions with water and urinary proteins. Physiol. Behav. 120: 211–219, Search in Google Scholar

Liberg, O. (1984). Food habits and prey impact by feral house-based domestic cats in a rural area in southern Sweden. J. Mammal. 65: 424–432, Search in Google Scholar

Lima, S.L. and Dill, L.M. (1990). Behavioural decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68: 619–640, Search in Google Scholar

Lin, Y.K. and Batzli, G.O. (1995). Predation on voles: an experimental approach. J. Mammal. 76: 1003–1012, Search in Google Scholar

Loss, S.R., Will, T., and Marra, P.P. (2013). The impact of free-ranging domestic cats on wildlife of the United States. Nat. Commun. 4: 1396, Search in Google Scholar

Lucia, K.E. and Keane, B. (2015). Alternate mating strategy compensates for inbreeding depression in male prairie voles. Behav. Ecol. 26: 1060–1070, Search in Google Scholar

Masini, C.V., Sauer, S., and Campeau, S. (2005). Ferret odor as a processive stress model in rats: neurochernical, behavioral, and endocrine evidence. Behav. Neurosci. 119: 280–292, Search in Google Scholar

McGuire, B. and Getz, L.L. (1998). The nature and frequency of social interactions among free-living prairie voles (Microtus ochrogaster). Behav. Ecol. Sociobiol. 43: 271–279, Search in Google Scholar

Medina, F.M., Bonnuad, E., Vidal, E., Tershy, B.R., Zavaleta, E.S., Donlan, C.J., Keitt, B.S., Le Corre, M., Horwath, S.V., and Nogales, M. (2011). A global review of the impacts of invasive cats on island endangered vertebrates. Global Change Biol. 17: 3503–3510, Search in Google Scholar

Meek, P.D. (1998). Food items brought home by domestic cats Felis catus (L) living in Booderee National Park, Jervis Bay. Proc. Linn. Soc. N. S. W. 120: 43–47. Search in Google Scholar

Merkins, M., Harestad, A.S., and Sullivan, T.P. (1991). Cover and efficacy of predator based repellants for Townsend’s vole, Microtus townsendii. J. Chem. Ecol. 17: 401–412. Search in Google Scholar

Monclús, R, Rödel, H.G., Palme, R, Von Holst, D., and de Miguel, J. (2006). Non-invasive measurement of the physiological stress response of wild rabbits to the odour of a predator. Chemoecology 16: 25–29, Search in Google Scholar

Orrock, J.L., Danielson, B.J., and Brinkerhoff, R.J. (2004). Rodent foraging is affected by indirect, but not by direct, cues of predation risk. Behav. Ecol. 15: 433–437, Search in Google Scholar

Owen, M.B., Lambert, C.T., Keane, B., and Solomon, N.G. (2019). Influence of vegetation characteristics at and near nests on female prairie vole (Microtus ochrogaster) survival and reproductive success. Am. Mid. Natl. 180: 170–182, Search in Google Scholar

Pearson, O.P. (1985). Predation, pp. 535–566. In: Tamarin, R.H. (Ed.), Biology of Microtus. Special Publication No. 8. American Society of Mammalogists, Shippensburg University, Shippensburg, PA, pp. 893. Search in Google Scholar

Polo-Cavia, N., Gonzalo, A., López, P., and Martín, J. (2010). Predator recognition of native but not invasive turtle predators by naïve anuran tadpoles. Anim. Behav. 80: 461–466, Search in Google Scholar

Powell, F., and Banks, P.B. (2004). Do house mice modify their foraging behaviour in response to predator odours and habitat?. Anim. Behav. 67: 753–759, Search in Google Scholar

Rosell, F. and Czech, A. (2000). Responses of foraging Eurasian beaver (Castor fiber) to predator odours. Wildl. Biol. 6: 13–21, Search in Google Scholar

Sikes, R.S., Bryan, J.A., Byman, D., Danielson, B.J., Eggleston, J., Gannon, M.R., Gannon, W.L., Hale, D.W., Jesmer, B.R., Odell, D.K., et al. (2016). 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J. Mammal. 97: 663–688, Search in Google Scholar

Slade, N.A. and Swihart, R.K. (1983). Home range indices for the hispid cotton rat (Sigmodon hispidus) in northeastern Kansas. J. Mammal. 64: 580–590, Search in Google Scholar

Slade, N.A. and Russell, L.A. (1998). Distances as indices to movements and home-range size from trapping records of small mammals. J. Mammal. 79: 346–351, Search in Google Scholar

Solomon, N.G. (1991). Age of pairing affects reproduction in prairie voles. Lab. Anim. 25: 232–235, Search in Google Scholar

Solomon, N.G., Christiansen, A.M., Kirk Lin, Y., and Hayes, L.D. (2005). Factors affecting nest location of prairie voles (Microtus ochrogaster). J. Mammal. 86: 555–560,[555:fanlop];2. Search in Google Scholar

Solomon, N.G., Richmond, A.R., Harding, P.A., Fries, A., Jacquemin, S., Schaefer, R.L., Lucia, K.E., and Keane, B. (2009). Polymorphism at the avpr1a locus in male prairie voles correlated with genetic but not social monogamy in field populations. Mol. Ecol. 18: 4680–4695, Search in Google Scholar

Sorge, E.R, Martin, L.J., Isbester, K.A., Sotocinal, S.G., Rosen, S., Tuttle, A.H., Wieskopf, J.S., Acland, E.L., Dokova, A., Kadoura, B., et al. (2014). Olfactory exposure to males, including men, causes stress and related analgesia in rodents. Nat. Methods 11: 629–632, Search in Google Scholar

Spencer, E.E., Crowther, M.S., and Dickman, C.R. (2014). Risky business: do native rodents use habitat and odor cues to manage predation risk in Australian deserts?. PloS One 9: e90566, Search in Google Scholar

Stoddart, D.M. (1976). Effect of the odor of weasels (Mustela nivalis L.) on trapped samples of their prey. Oecologia 22: 439–441, Search in Google Scholar

Story, J.D., Galbraith, W.J., and Kithings, J.T. (1982). Food habits of bobcats in eastern Tennessee. J. Tenn. Acad. Sci. 57: 29–32. Search in Google Scholar

Sullivan, T.P., Crump, D.R., and Sullivan, D.S. (1988). Use of predator odors as repellents to reduce feeding damage by herbivores. III. Montane and meadow voles (Microtus montanus and Microtus pennsylvanicus). J. Chem. Ecol. 14: 363–377, Search in Google Scholar

Sullivan, T.P., Nordstrom, L., and Sullivan, D.S. (1985). Use of predator odors as repellents to reduce feeding damage by herbivores: II. Black-tailed deer (Odocoileus hemionus columbianus). J. Chem. Ecol. 11: 921–935, Search in Google Scholar

Swihart, R.K. (1991). Modifying scent-marking behavior to reduce woodchuck damage to fruit trees. Ecol. Appl. 1: 98–103, Search in Google Scholar

Swihart, R.K., Mattina, M.J.I., and Pignatello, J.J. (1997). Repellency of predator urine to woodchucks and meadow voles. In: Mason, J.R. (Ed.). Repellents in wildlife management: Proceedings of a symposium. National Wildlife Research Center, Ft. Collins, Denver, CO, pp. 271–284. Search in Google Scholar

Takahashi, L.K., Nakashima, B.R., Hong, H., and Watanabe, K. (2005). The smell of danger: a behavioral and neural analysis of predator odor-induced fear. Neurosci. Biobehav. Rev. 29: 1157–1167, Search in Google Scholar

Tinbergen, N. (1963). On aims and methods of ethology. Z. Tierpsychol. 20: 410–433. Search in Google Scholar

Turner, D.C. and Bateson, P. (2000). The domestic cat: the biology of its behaviour. Cambridge University Press, Cambridge, p. 256. Search in Google Scholar

Ward, J.F., MacDonald, D.W., Doncaster, C.P., and Mauget, C. (1996). Physiological response of the European hedgehog to predator and nonpredator odor. Physiol. Behav. 60: 1469–1472, Search in Google Scholar

Werdelin, L., Yamaguchi, N., Johnson, W.E., and O’Brien, S.J. (2010). Phylogeny and evolution of cats (Felidae), pp. 59–82. In: MacDonald, D.W. and Loveridge, A.J. (Eds.), Biology and conservation of wild felids. Oxford University Press, Oxford, p. 784. Search in Google Scholar

Wolff, J.O. (2004). Scent marking by voles in response to predation risk: a field-laboratory validation. Behav. Ecol. 15: 286–289, Search in Google Scholar

Zangrossi, H. and File, S.E. (1992). Behavioral consequences in animal tests of anxiety and exploration of exposure to cat odor. Brain Res. Bull. 29: 381–388, Search in Google Scholar

Zöttl, M., Lienert, R., Clutton-Brock, T., Millesi, E., and Manser, M.B. (2013). The effects of recruitment to direct predator cues on predator responses in meerkats. Behav. Ecol. 24: 198–204, Search in Google Scholar

Received: 2020-02-08
Accepted: 2020-06-02
Published Online: 2020-08-03
Published in Print: 2021-01-27

© 2020 Walter de Gruyter GmbH, Berlin/Boston