Individual vs. non-individual acoustic signalling in African woodland dormice (Graphiurus murinus)
Abstract
Animals that live in cohesive groups often use social calls for long-distance communication, particularly in low-visibility habitats, whereas other call types are only used to communicate over short distances. According to the “distance-communication hypothesis” only the former should encode individual information while the latter should not because individuals are in visual or olfactory contact when calls are broadcast. We used the African woodland dormouse Graphiurus murinus, a social rodent whose vocal repertoire is still poorly known, as a model species to test the hypothesis that long-range but not shortrange calls will structurally differ across individuals. By conducting controlled video- and audio recordings in captivity, we associated calls to non-vocal behaviours in G. murinus and selected two call types (contact and aggressive calls) that clearly served long- and short-range communication respectively. In agreement with the distance-communication hypothesis, only contact but not aggressive calls differed significantly among subjects. Although we did not test the actual function of such variation, the latter provides a structural basis for the transmission of individual information. This is the first time this hypothesis is tested in a small non-volant mammal. Our study also provides the first description of acoustic behaviour in G. murinus.
Keywords
Communication Dormouse Individual discrimination Rodent Vocal signaturePreview
Unable to display preview. Download preview PDF.
References
- Ancillotto, L., Russo, D., 2014. Selective aggressiveness in European free-tailed bats (Tadarida teniotis): influence of familiarity, age and sex, Naturwissenschaften 101, 221–228.PubMedCrossRefGoogle Scholar
- Ancillotto, L, Sozio, G., Mortelliti, A., Russo, D., 2014. Ultrasonic communication in Gliridae (Rodentia): the hazel dormouse (Muscardinus avellanarius) as a case study, Bioacoustics 23, 129–141, https://doi.org/10.1080/09524622.2013. 838146.CrossRefGoogle Scholar
- Ancillotto, L, Mori, E., Sozio, G., Solano, E., Bertolino, S., Russo, D., 2016. A novel approach to field identification of cryptic Apodemus wood mice: calls differ more than morphology. Mammal Rev., https://doi.org/10.1111/mam.12076.Google Scholar
- Arriaga, G., Jarvis, E.D., 2013. Mouse vocal communication system: are ultrasounds learned or innate? Brain Lang. 124, 96–116, https://doi.org/10.1016/j.bandl. 2012.10.002.Google Scholar
- Boratynski, P., Rachwald, A., Nowakowski, W., 1999. Ultrasound communication calls in forest dormouse (Dryomys nitedula). In: IVth Int. Conf. Dormice, Rodentia, Gliridae.Google Scholar
- Bouchet, H., Blois-Heulin, C., Pellier, A.S., Zuberbühler, K., Lemasson, A., 2012. Acoustic variability and individual distinctiveness in the vocal repertoire of red-capped mangabeys (Cercocebus torquatus), J. Comp. Psychol. 126, 45–56.PubMedCrossRefGoogle Scholar
- Bouchet, H., Blois-Heulin, C., Lemasson, A., 2013. Social complexity parallels vocal complexity: a comparison of three non-human primate species. Front. Psychol. 4.Google Scholar
- Boughman, J., Wilkinson, G., 1998. Greater spear-nosed bats discriminate group mates by vocalizations. Anim. Behav. 55, 1717–1732, https://doi.org/10.1006/anbe.1997.0721.CrossRefGoogle Scholar
- Cornec, C, Hingrat, Y., Rybak, F., 2014. Individual signature in a lekking species: visual and acoustic courtship parameters may help discriminating conspecifics in the houbara bustard, Ethology 120, 726–737.CrossRefGoogle Scholar
- Ellis, J.M., 2008. Decay of apparent individual distinctiveness in the begging calls of adult female white-throated magpie-jays, Condor 110, 648–657.CrossRefGoogle Scholar
- Freeberg, T.M., Dunbar, R.I., Ord, T.J., 2012. Social complexity as a proximate and ultimate factor in communicative complexity, Philos. Trans. Soc. Lond. B Biol. Sci. 367, 1785–1801.CrossRefGoogle Scholar
- Hare, J.F., 1998. Juvenile Richardson’s ground squirrels, Spermophilus richardsonii, discriminate among individual alarm callers, Anim. Behav. 55, 451–460.PubMedCrossRefGoogle Scholar
- Hogstedt, G., 1983. Adaptation unto death: function of fear screams. Am. Nat., 562–570.Google Scholar
- Holy, T.E., Guo, Z., 2005. Ultrasonic songs of male mice. PLoS Biol. 3, e386, https://doi.org/10.1371/journal.pbio.0030386.CrossRefGoogle Scholar
- Hutson, C.L., Lee, K.N., Abel, J., Carroll, D.S., Montgomery, J.M., Olson, V.A., Li, Y., Davidson, W., Hughes, C, Dillon, M., Spurlock, P., et al., 2007. Monkeypox zoonotic associations: insights from laboratory evaluation of animals associated with the multistate US outbreak, Am. J. Trop. Med. Hyg. 76, 757–767.PubMedCrossRefPubMedCentralGoogle Scholar
- Hutterer, R., Peter, G., 2001. The vocal repertoIre of Graphiurus parvus, and comparisons with other species of dormice, Trak. Univ. J. Sci. Res. Ser. B 2, 69–74.Google Scholar
- Janik, V.M., Sayigh, L.S., 2013. Communication in bottlenose dolphins: 50 years of signature whistle research, J. Comp. Physiol. 199, 479–489.CrossRefGoogle Scholar
- Juskaitis, R., 2008. The Common Dormouse Muscardinus avellanarius: Ecology, Population Structure and Dynamics. Institute of Ecology of Vilnius University Publishers, Vilnius.Google Scholar
- Jurczyszyn, M., 1994. Population density of Myoxus glis (L.) in some forest biotops, Hystrix Ital. J. Mammal. 6, 265–271.Google Scholar
- Kalcounis-Rueppell, M.C., Petric, R., Briggs, J.R., Carney, C, Marshall, M.M., Willse, J.T., Rueppell, O., Ribble, D.O., Crossland, J.P., 2010. Differences in ultrasonic vocalizations between wild and laboratory California mice (Peromyscus californicus). PLoS One 5, e9705, https://doi.org/10.1371/journal.pone 0009705.CrossRefGoogle Scholar
- Kastenmayer, R.J., Moak, H.B., Jeffress, E.J., Elkins, W.R., 2010. Management and care of African dormice (Graphiurus kelleni), J. Am. Assoc. Lab. Anim. Sci. 49, 173–176.PubMedPubMedCentralGoogle Scholar
- Kremers, D., Lemasson, A., Almunia, J., Wanker, R., 2012. Vocal sharing and individual acoustic distinctiveness within a group of captive orcas (Orcinus orca). J. Comp. Psychol. 126, 433.CrossRefGoogle Scholar
- Krystufek, B., Haberl, W., Baxter, R.M., Zima, J., 2004. Morphology and karyology of two populations of the woodland dormouse Graphiurus murinus in the Eastern Cape, South Africa, Folia Zool. 53, 339–350.Google Scholar
- Macedonia, J.M., 1986. Individuality in a contact call of the ringtailed lemur (Lemur catta), Am. J. Primatol. 11, 163–179.CrossRefGoogle Scholar
- Madikiza, Z.J.K., 2010. Population biology and aspects of the socio-spatial organisation of the Woodland dormouse Graphiurus murinus (Desmaret, 1822) in the Great fish river Reserve, South Africa. In: Ph.D Thesis. University of Fort Hare, South Africa.Google Scholar
- Madikiza, Z.J.K., Bertolino, S., Baxter, R.M., Do Linh San, E., 2010. Nest box use by woodland dormice (Graphiurus murinus): the influence of life cycle and nest box placement. Eur. J. Wildl. Res. 56, 735–743, https://doi.org/10.1007/ s10344-010-0369-x.Google Scholar
- Madikiza, Z.J.K., Bertolino, S., Do Linh San, E., 2011. Female in space, or female in space and time? First data on the socio-spatial organization and mating system of the woodland dormouse (Graphiurus murinus). J. Ethol. 29, 375–380, https://doi.org/10.1007/s10164-010-0249-6.CrossRefGoogle Scholar
- Matrosova, V.A., Blumstein, D.T., Volodin, I.A., Volodina, E.V., 2011. The potential to encode sex, age, and individual identity in the alarm calls of three species of Marmotinae, Naturwissenschaften 98, 181–192.PubMedPubMedCentralCrossRefGoogle Scholar
- Maynard Smith, J., Harper, D., 2003. Animal Signals. Oxford University Press, Oxford, UK, pp. 208.Google Scholar
- McCowan, B., Hooper, S.L., 2002. Individual acoustic variation in Belding’s ground squirrel alarm chirps in the High Sierra Nevada, J. Acoust. Soc. Am. 111, 1157–1160.PubMedCrossRefGoogle Scholar
- Miller, J.R., Engstrom, M.D., 2010. Stereotypic vocalizations in harvest mice (Reithrodontomys): harmonic structure contains prominent and distinctive audible, ultrasonic, and non-linear elements. J. Acoust. Soc. Am. 128, 1501–1510, https://doi.org/10.1121/1.3455855.Google Scholar
- Mitani,J.C, Gros-Louis, J., Macedonia, J.M., 1996. Selection for acoustic individuality within the vocal repertoire of wild chimpanzees, Int. J. Primatol. 17, 569–583.CrossRefGoogle Scholar
- Montgelard, C, Matthee, C.A., Robinson, T.J., 2003. Molecular systematics of dormice (Rodentia: Gliridae) and the radiation of Graphiurus in Africa. Proc. R. Soc. B. Biol. Sci. 270, 1947–1955, https://doi.org/10.1098/rspb.2003.2458.Google Scholar
- Mumm, C.A.S., Urrutia, M.C., Knörnschild, M., 2014. Vocal individuality in cohesion calls of giant otters, Pteronura brasiliensis, Anim. Behav. 88, 243–252, https://doi.org/10.1016/j.anbehav.2013.12.005.CrossRefGoogle Scholar
- Nousek, A.E., Slater, P.J., Wang, C, Miller, P.J., 2006. The influence of social affiliation on individual vocal signatures of northern resident killer whales (Orcinus orca), Biol. Lett. 2, 481–484.PubMedPubMedCentralCrossRefGoogle Scholar
- Pfalzer, G., Kusch, J., 2003. Structure and variability of bat social calls: implications for specificity and individual recognition, J. Zool. 261, 21–33, https://doi.org/10.1017/S0952836903003935.CrossRefGoogle Scholar
- Pollard, K.A., Blumstein, D.T., 2012. Evolving communicative complexity: insights from rodents and beyond. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 1869–1878, https://doi.org/10.1098/rstb.2011.0221.Google Scholar
- Searby, A., Jouventin, P., Aubin, T., 2004. Acoustic recognition in macaroni penguins: an original signature system, Anim. Behav. 67, 615–625.CrossRefGoogle Scholar
- Sousa-Lima, R.S., Paglia, A.P., Da Fonseca, G.A., 2002. Signature information and individual recognition in the isolation calls of Amazonian manatees, Trichechus inunguis (Mammalia: Sirenia), Anim. Behav. 63, 301–310.CrossRefGoogle Scholar
- Suckow, M.A., Stevens, K.A., Wilson, R.P., 2012. The Laboratory Rabbit, Guinea Pig, Hamster, and Other Rodents. Academic Press/Elsevier, Waltham, MA.Google Scholar
- Terryn, L, Wendelen, W., Leirs, H., Lenglet, G., Verheyen, E., 2007. African Rodentia. https://doi.org/projects.biodiversity.be/africanrodentia.
- Tyack, P.L., 2000. Dolphins whistle a signature tune. Science 289, 1310.Google Scholar
- Wanker, R., Fischer, J., 2001. Intra-and interindividual variation in the contact calls of spectacled parrotlets (Forpus conspicillatus), Behaviour 138, 709–726.CrossRefGoogle Scholar
- Webb, P.I., Skinner, J.D., 1994. The dormice (Myoxidae) of Southern Africa, Hystrix Ital. J. Mammal. 6, 287–293.Google Scholar
- Wiley, R.H., Richards, D.G., 1978. Physical constraints on acoustic communication in the atmosphere: implications for the evolution of animal vocalizations, Behav. Ecol. Sociobiol. 3, 69–94.CrossRefGoogle Scholar
- Wright, S.L., Brown, R.E., 2004. Sex differences in ultrasonic vocalizations and coordinated movement in the California mouse (Peromyscus californicus), Behav. Processes 65, 155–162, https://doi.org/10.1016/j.beproc.2003.09.004.PubMedCrossRefGoogle Scholar