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Deer Mothers Are Sensitive to Infant Distress Vocalizations of Diverse Mammalian Species

Susan Lingle and Tobias Riede
The American Naturalist
Vol. 184, No. 4 (October 2014), pp. 510-522
DOI: 10.1086/677677
Stable URL:
Page Count: 13
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AbstractAcoustic structure, behavioral context, and caregiver responses to infant distress vocalizations (cries) are similar across mammals, including humans. Are these similarities enough for animals to respond to distress vocalizations of taxonomically and ecologically distant species? We show that mule deer (Odocoileus hemionus) and white-tailed deer (Odocoileus virginianus) mothers approach a speaker playing distress vocalizations of infant marmots (Marmota flaviventris), seals (Neophoca cinerea and Arctocephalus tropicalis), domestic cats (Felis catus), bats (Lasionycteris noctivagans), humans (Homo sapiens), and other mammals if the fundamental frequency (F0) falls or is manipulated to fall within the frequency range in which deer respond to young of their own species. They did not approach to predator sounds or to control sounds having the same F0 but a different structure. Our results suggest that acoustic traits of infant distress vocalizations that are essential for a response by caregivers, and a caregiver’s sensitivity to these acoustic traits, may be shared across diverse mammals.

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This item contains 67 references.

Literature Cited
  • ['Aitkin, L., J. Nelson, and R. Shepherd. 1996. Development of hearing and vocalization in a marsupial, the northern quoll Dasyurus hallucatus. Journal of Experimental Zoology 276:394–402.']
  • ['Andics, A., M. Gácsi, T. Faragó, A. Kis, and Á. Miklósi. 2014. Voice-sensitive regions in the dog and human brain are revealed by comparative fMRI. Current Biology 24:574–578.']
  • ['Aubin, T. 1991. Why do distress calls evoke interspecific responses? an experimental study applied to some species of birds. Behavioural Processes 23:103–111.']
  • ['Aubin, T., and J. C. Bremond. 1992. Perception of distress call harmonic structure by the starling Sturnus vulgaris. Behaviour 120:151–163.']
  • ['August, P. V., and J. G. T. Anderson. 1987. Mammal sounds and motivation-structural rules: a test of the hypothesis. Journal of Mammalogy 68:1–9.']
  • ['Barnet, A., M. Bazelon, and M. Zapella. 1966. Visual and auditory function in an hydranencephalic infant. Brain Research 2:351–360.']
  • ['Bass, A. H., E. H. Gilland, and R. Baker. 2008. Evolutionary origins for social vocalization in a vertebrate hindbrain-spinal compartment. Science 321:417–421.']
  • ['Bass, A. H., and J. R. McKibben. 2003. Neural mechanisms and behaviors for acoustic communication in teleost fish. Progress in Neurobiology 69:1–26.']
  • ['Belin, P., S. Fecteau, I. Charest, N. Nicastro, M. D. Hauser, and J. L. Armory. 2008. Human cerebral response to animal affective vocalizations. Proceedings of the Royal Society B: Biological Sciences 275:473–481.']
  • ['Benedict, L. 2007. Offspring discrimination without recognition: California towhee responses to chick distress calls. Condor 109:79–87.']
  • ['Blumstein, D. T., D. T. Richardson, L. Cooley, J. Winternitz, and J. C. Daniel. 2008. The structure, meaning and function of yellow-bellied marmot pup screams. Animal Behaviour 76:1055–1064.']
  • ['Boersma, P., and D. Weenink. 2011. Praat: doing phonetics by computer. Version 5.2.22.']
  • ['Bohn, K. M., C. F. Moss, and G. S. Wilkinson. 2006. Correlated evolution between hearing sensitivity and social calls in bats. Biology Letters 2:561–564.']
  • ['Briefer, E. F. 2012. Vocal expression of emotions in mammals: mechanisms of production and evidence. Journal of Zoology 288:1–20.']
  • ['Carter, C. S. 2014. Oxytocin pathways and the evolution of human behavior. Annual Review of Psychology 65:17–39. doi:10.1146/annurev-psych-010213-115110.']
  • ['Carter, C. S., A. J. Grippo, H. Pournajafi-Nazarloo, M. G. Ruscio, and S. W. Porges. 2008. Oxytocin, vasopressin and social behavior. Progress in Brain Research 170:331–336.']
  • ['Chaiken, M. 1992. Individual recognition of nestling distress screams by European starlings Sturnus vulgaris. Behaviour 120:139–150.']
  • ['Charrier, I., N. Mathevon, and P. Jouventin. 2002. How does a fur seal mother recognize the voice of her pup? an experimental study of Arctocephalus tropicalis. Journal of Experimental Biology 205:603–612.']
  • ['Chittka, L., P. Skorupski, and N. E. Raine. 2009. Speed-accuracy tradeoffs in animal decision making. Trends in Ecology and Evolution 24:400–407.']
  • ['Clutton-Brock, J. 1999. A natural history of domesticated mammals. 2nd ed. Cambridge University Press, Cambridge.']
  • ['Curio, E. 1978. The adaptive significance of mobbing. I. Teleonomic hypotheses and predictions. Zeitschrift für Tierpsychologie 48:175–183.']
  • ['Custance, D., and J. Mayer. 2012. Empathic-like responding by domestic dogs (Canis familiaris) to distress in humans: an exploratory study. Animal Cognition 15:851–859. doi:10.1007/s10071-012-0510-1.']
  • ['Druzhkova, A. S., O. Thalmann, V. A. Trifonov, J. A. Leonard, N. V. Vorobieva, N. D. Ovodov, A. S. Graphodatsky, and R. K. Wayne. 2013. Ancient DNA analysis affirms the canid from Altai as a primitive dog. PLoS ONE 8:e57754. doi:10.1371/journal.pone.0057754.']
  • ['Ehret, G. 1992. Categorical perception of mouse-pup ultrasounds in the temporal domain. Animal Behaviour 43:409–416.']
  • ['Ehret, G., and B. Haack. 1981. Categorical perception of mouse pup ultrasound by lactating females. Naturwissenschaften 68:208–209.']
  • ['Fallow, P. M., B. J. Pitcher, and R. D. Magrath. 2013. Alarming features: birds use specific acoustic properties to identify heterospecific alarm calls. Proceedings of the Royal Society B: Biological Sciences 280:20122539. doi:10.1098/rspb.2012.2539.']
  • ['Faragó, T., A. Andics, V. Devecseri, A. Kis, M. Gácsi, and Á. Miklósi. 2014. Humans rely on the same rules to assess emotional valence and intensity in conspecific and dog vocalizations. Biology Letters 10:20130926.']
  • ['Gillooly, J. F., and A. G. Ophir. 2010. The energetic basis of acoustic communication. Proceedings of the Royal Society B: Biological Sciences 277:1325–1331. doi:10.1098/rspb.2009.2134.']
  • ['Gustafsson, E., D. Levréro, D. Reby, and N. Mathevon. 2013. Fathers are just as good as mothers at recognizing the cries of their baby. Nature Communication 4:1698. doi:10.1038/ncomms2713.']
  • ['Hauser, M. D. 1997. The evolution of communication. MIT Press, Cambridge, MA.']
  • ['Insley, S. J., A. V. Phillips, and I. Charrier. 2003. A review of social recognition in pinnipeds. Aquatic Mammals 29:181–201.']
  • ['Kyuhou, S., and H. Gemba. 1998. Two vocalization-related subregions in the midbrain periaqueductal gray of the guinea pig. Neuroreport 9:1607–1610.']
  • ['Levréro, F., L. Durand, C. Vignal, A. Blanca, and N. Mathevon. 2009. Begging calls support offspring individual identity and recognition by zebra finch parents. Comptes Rendus Biologies 332:579–589.']
  • ['Lingle, S., D. Rendall, and S. M. Pellis. 2007a. Altruism and recognition in the predator defence of deer: species and individual variation in fawn distress calls. Animal Behaviour 73:897–905.']
  • ['Lingle, S., D. Rendall, W. F. Wilson, R. W. DeYoung, and S. M. Pellis. 2007b. Altruism and recognition in the predator defence of deer: why mule deer help nonoffspring fawns. Animal Behaviour 73:907–916.']
  • ['Lingle, S., and T. Riede. 2014. Data from: Deer mothers are sensitive to infant distress vocalizations of diverse mammalian species. American Naturalist, Dryad Digital Repository,']
  • ['Lingle, S., M. T. Wyman, R. Kotrba, L. J. Teichroeb, and C. A. Romanow. 2012. What makes a cry a cry? a review of infant distress vocalizations. Current Zoology 58:698–726.']
  • ['Liu, R. C., K. D. Miller, M. M. Merzenich, and C. E. Schreiner. 2003. Acoustic variability and distinguishability among mouse ultrasound vocalizations. Journal of the Acoustical Society of America 114:3412–3422.']
  • ['McComb, K., A. M. Taylor, C. Wilson, and B. D. Charlton. 2009. The cry embedded within the purr. Current Biology 19:R507–R508.']
  • ['McNeilly, A. S., I. Robinson, M. J. Houston, and P. W. Howie. 1983. Release of oxytocin and prolactin in response to suckling. British Medical Journal 286:257–259.']
  • ['Middlemis-Brown, J. E., E. D. Johnson, and M. S. Blumberg. 2005. Separable brainstem and forebrain contributions to ultrasonic vocalizations in infant rats. Behavioral Neuroscience 119:1111–1117.']
  • ['Morton, E. S. 1977. On the occurrence and significance of motivation-structural rules in some birds and mammal sounds. American Naturalist 111:855–869.']
  • ['Nelson, E. E., and J. Panksepp. 1998. Brain substrates of infant-mother attachment: contributions of opioids, oxytocin, and norepinephrine. Neuroscience and Biobehavioral Reviews 22:437–452.']
  • ['Newman, J. D. 2004. The primate isolation call: a comparison with precocial birds and non-primate mammals. Pages 171–187 in L. J. Rogers and G. Kaplan, eds. Comparative vertebrate cognition: are primates superior to non-primates? Kluwer Academic/Plenum, New York.']
  • ['———. 2007. Neural circuits underlying crying and cry responding in mammals. Behavioural Brain Research 182:155–165.']
  • ['Nielsen, J. M., and R. P. Sedgwick. 1949. Instincts and emotions in an anencephalic monster. Journal of Nervous and Mental Disease 110:387–394.']
  • ['Owren, M. J., and D. Rendall. 2001. Sound on the rebound: bringing form and function back to the forefront in understanding nonhuman primate vocal signaling. Evolutionary Anthropology 10:58–71.']
  • ['Panksepp, J., and L. Biven. 2012. The archaeology of mind: neuroevolutionary origins of human emotions. Norton, New York.']
  • ['Parsons, C. E., K. S. Young, E. Parson, A. Stein, and M. L. Kringelbach. 2012. Listening to infant distress vocalizations enhances effortful motor performance. Acta Paediatrica 101:189–191.']
  • ['Reby, D. D., B. D. Charlton, Y. Locatelli, and K. McComb. 2010. Oestrous red deer hinds prefer male roars with higher fundamental frequencies. Proceedings of the Royal Society B: Biological Sciences 277:2747–2753.']
  • ['Rendall, D., M. J. Owren, and M. J. Ryan. 2009. What do animal signals mean? Animal Behaviour 78:233–240.']
  • ['Riem, M. M. E., M. J. Bakermans-Kranenburg, S. Pieper, M. Tops, M. A. S. Boksem, R. R. J. M. Vermeiren, M. H. van IJzendoorn, and S. A. R. B. Rombouts. 2011a. Oxytocin modulates amygdala, insula, and inferior frontal gyrus responses to infant crying: a randomized controlled trial. Biological Psychiatry 70:291–297.']
  • ['Riem, M. M. E., S. Pieper, D. Out, M. J. Bakermans-Kranenburg, and M. H. van IJzendoorn. 2011b. Oxytocin receptor gene and depressive symptoms associated with physiological reactivity to infant crying. Social Cognitive and Affective Neuroscience 6:294–300.']
  • ['Springer, M. S., W. J. Murphy, E. Eizirik, and S. J. O’Brien. 2003. Placental mammal diversification and the Cretaceous-Tertiary boundary. Proceedings of the National Academy of Sciences of the USA 100:1056–1061.']
  • ['Stallings, J., A. S. Fleming, C. Corter, C. Worthman, and M. Steiner. 2001. The effects of infant cries and odors on sympathy, cortisol, and autonomic responses in new mothers and nonpostpartum women. Parenting: Science and Practice 1:71–100.']
  • ['Tallet, C., P. Linhart, R. Policht, K. Hammerschmidt, P. Šimeček, P. Kratinova, and M. Špinka. 2013. Encoding of situations in the vocal repertoire of piglets (Sus scrofa): a comparison of discrete and graded classifications. PLoS ONE 8:e71841. doi:10.1371/journal.pone.0071841.']
  • ['Tallet, C., M. Špinka, I. Maruščáková, and P. Šimeček. 2010. Human perception of vocalizations of domestic piglets and modulation by experience with domestic pigs Sus scrofa. Journal of Comparative Psychology 124:81–91.']
  • ['Teichroeb, L. J., T. Riede, R. Kotrba, and S. Lingle. 2013. Fundamental frequency is key to response of female deer to juvenile distress calls. Behavioural Processes 92:15–23.']
  • ['Tops, M., M. H. van IJzendoorn, M. M. E. Riem, M. A. S. Boksem, and M. J. Bakermans-Kranenburg. 2011. Oxytocin receptor gene associated with the efficiency of social auditory processing. Frontiers in Psychiatry 2:1–4. doi:10.3389/fpsyt.2011.00060.']
  • ['Torriani, M. V. G., E. Vannoni, and A. G. McElligott. 2006. Mother-young recognition in an ungulate hider species: a unidirectional process. American Naturalist 168:412–420.']
  • ['Trimmer, P. C., A. I. Houston, J. A. R. Marshall, R. Bogacz, E. S. Paul, M. R. Mendl, and J. M. McNamara. 2008. Mammalian choices: combining fast-but-inaccurate and slow-but-accurate decision-making systems. Proceedings of the Royal Society B: Biological Sciences 275:2353–2361.']
  • ['Vergne, A. L., T. Aubin, P. Taylor, and N. Mathevon. 2011. Acoustic signals of baby black caimans. Zoology 114:313–320.']
  • ['Vergne, A. L., A. Avril, S. Martin, and N. Mathevon. 2007. Parent-offspring communication in the Nile crocodile Crocodylus niloticus: do newborns’ calls show an individual signature? Naturwissenschaften 94:49–54.']
  • ['Wiesenfeld, A. R., C. Z. Malatesta, and L. L. Deloach. 1981. Differential parental responses to familiar and unfamiliar infant distress signals. Infant Behavior and Development 4:281–295. doi:10.1016/S0163-6383(81)80030-6.']
  • ['Zeifman, D. M. 2001. An ethological analysis of human infant crying: answering Tinbergen’s four questions. Developmental Psychobiology 39:265–285.']
  • ['Zeskind, P. S. 2013. Infant crying and the synchrony of arousal. Pages 155–172 in E. Altenmüller, S. Schmidt, and E. Zimmermann, eds. Evolution of emotional communication: from sounds in nonhuman mammals to speech and music in man. Series in Affective Science. Oxford University Press, Oxford.']
  • ['Zimmermann, E., L. Leliveld, and S. Schehka. 2013. Toward the evolutionary roots of affective prosody in human acoustic communication: a comparative perspective. Pages 116–132 in E. Altenmüller, S. Schmidt, and E. Zimmermann, eds. Evolution of emotional communication: from sounds in nonhuman mammals to speech and music in man. Series in Affective Science. Oxford University Press, Oxford.']