Audience drives male songbird response to partner's voice

Abstract

According to the social intelligence hypothesis, social context represents an important force driving the selection of animal cognitive abilities such as the capacity to estimate the nature of the social relationships between other individuals1,2,3,4. Despite this importance, the influence of this force has been assessed only in primates and never in other animals showing social interactions5,6,7. In this way, avian communication generally takes place in a network of signallers and receivers, which represents an audience altering individual signalling behaviours8,9. Indeed, vocal amplitude10 and repertoire11 are known to be socially regulated and the attitude towards the opposite sex may change depending on the audience8,12,13. This ‘audience effect’8,14,15,16 provides support for the reality of social awareness in some bird species. However no evidence has yet been found to suggest that birds are able to estimate the characteristics of the social relationships between group-mates. Here we show that the male of a gregarious songbird species—the zebra finch (Taeniopygia guttata)—pays attention to the mating status of conspecific pairs, and uses this information to control its behaviour towards its female partner.

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Figure 1: Acoustic structure of the distance call of the female zebra finch.
Figure 2: Discriminant analysis on the 17 acoustic parameters of the female call.
Figure 3: Response of male to female voices as a function of the mating status of the audience.

References

  1. 1

    Barton, R. A. & Dunbar, R. I. M. in Machiavellian Intelligence II: Extensions and Evaluations (eds Whiten, A. & Byrne, R. W.) 240–263 (Cambridge Univ. Press, Cambridge, 1997)

    Google Scholar 

  2. 2

    Byrne, R. W. & Whiten, A. Machiavellian Intelligence: Social Expertise and the Evolution of Intellect in Monkeys, Apes and Humans (Clarendon, Oxford, 1988)

    Google Scholar 

  3. 3

    Dunbar, R. I. M. The social brain hypothesis. Evol. Anthropol. 6, 178–190 (1998)

    Article  Google Scholar 

  4. 4

    Adolphs, R. Cognitive neuroscience of human social behaviour. Nature Rev. Neurosci. 4, 165–178 (2003)

    CAS  Article  Google Scholar 

  5. 5

    Perry, S., Barrett, C. & Manson, J. H. White-faced capuchin monkeys show triadic awareness in their choice of allies. Anim. Behav. 67, 165–170 (2004)

    Article  Google Scholar 

  6. 6

    Jolly, A. Lemur social behaviour and primate intelligence. Science 153, 501–506 (1966)

    ADS  CAS  Article  Google Scholar 

  7. 7

    Tomasello, M. & Call, J. Primate Cognition (Oxford Univ. Press, Oxford, 1997)

    Google Scholar 

  8. 8

    Baltz, A. P. & Clark, A. B. Extra-pair courtship behaviour of male budgerigars and the effect of an audience. Anim. Behav. 53, 1017–1024 (1997)

    Article  Google Scholar 

  9. 9

    McGregor, P. K., Otter, K. & Peake, T. M. in Animal Signals: Signalling and Signal Design in Animal Communication (eds Espmark, Y., Amundsen, T. & Rosenqvist, G.) 329–340 (Tapir Academic, Trondheim, Norway, 2000)

    Google Scholar 

  10. 10

    Cynx, J. & Gell, C. Social mediation of vocal amplitude in a songbird, Taeniopygia guttata. Anim. Behav. 67, 451–455 (2004)

    Article  Google Scholar 

  11. 11

    Zann, R. The Zebra Finch: a Synthesis of Field and Laboratory Studies 196–213 (Oxford Univ. Press, Oxford, 1996)

    Google Scholar 

  12. 12

    Evans, C. S. & Evans, L. Chicken food calls are functionally referential. Anim. Behav. 58, 307–319 (1999)

    CAS  Article  Google Scholar 

  13. 13

    Evans, C. S. & Marler, P. Food calling and audience effects in male chickens, Gallus gallus: their relationships to food availability, courtship and social facilitation. Anim. Behav. 47, 1159–1170 (1994)

    Article  Google Scholar 

  14. 14

    Marler, P., Dufty, A. & Pickert, R. Vocal communication in the domestic chicken: II. Is a sender sensitive to the presence and nature of a receiver? Anim. Behav. 34, 194–198 (1986)

    Article  Google Scholar 

  15. 15

    Striedter, G. F., Freibott, L., Hile, A. G. & Burley, N. T. For whom the male calls: an effect of audience on contact call rate and repertoire in budgerigars, Melopsittacus undulatus. Anim. Behav. 65, 875–882 (2003)

    Article  Google Scholar 

  16. 16

    Johnstone, A. R. Eavesdropping and animal conflict. Proc. Natl Acad. Sci. USA 98, 9177–9180 (2001)

    ADS  CAS  Article  Google Scholar 

  17. 17

    Miller, D. B. The acoustic basis of mate recognition by female zebra finches (Taeniopygia guttata). Anim. Behav. 27, 376–380 (1979)

    Article  Google Scholar 

  18. 18

    Charrier, I., Mathevon, N. & Jouventin, P. Mother's voice recognition by seal pups. Nature 412, 873 (2001)

    ADS  CAS  Article  Google Scholar 

  19. 19

    Belin, P., Fecteau, S. & Bédard, C. Thinking the voice: neural correlates of voice perception. Trends Cogn. Sci. 8, 129–135 (2004)

    Article  Google Scholar 

  20. 20

    Insley, S. J. Long-term recognition in the northern fur seal. Nature 406, 404–405 (2000)

    ADS  CAS  Article  Google Scholar 

  21. 21

    Hessler, N. A. & Doupe, A. J. Social context modulates singing-related neural activity in the songbird forebrain. Nature Neurosci. 2, 209–211 (1999)

    CAS  Article  Google Scholar 

  22. 22

    Jarvis, E. D., Scharff, C. & Grossman, M. R. For whom the bird sings: context-dependent gene expression. Neuron 21, 775–788 (1998)

    CAS  Article  Google Scholar 

  23. 23

    Aubin, T. Syntana: a software for the synthesis and analysis of animal sounds. Bioacoustics 6, 80–81 (1994)

    Google Scholar 

  24. 24

    Sokal, R. R. & Rohlf, F. J. Biometry 57–58 & 443 (Freeman, New York, 1995)

    Google Scholar 

  25. 25

    Robinson, P., Aubin, T. & Brémond, J. C. Individuality in the voice of emperor penguin Aptenodytes forsteri: adaptation to a noisy environment. Ethology 94, 279–290 (1993)

    Article  Google Scholar 

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Acknowledgements

This research was supported by the Interdisciplinary Program “Cognition and Information Processing” of the Centre National de la Recherche Scientifique (CNRS). C.V. is supported by the French Ministry of National Education. We thank C. Bouchut, M. Rabearinaivo and S. Tisseur for their help during the work, L. Bloomfield for improving the English, and I. Charrier for her advice on previous drafts of the manuscript.

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Correspondence to Nicolas Mathevon.

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Vignal, C., Mathevon, N. & Mottin, S. Audience drives male songbird response to partner's voice. Nature 430, 448–451 (2004). https://doi.org/10.1038/nature02645

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