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Conserved alarm calls but rapid auditory learning in monkey responses to novel flying objects

Abstract

To evaluate the flexibility in vocal production and comprehension in a non-human primate, we presented a drone to West African green monkeys, Chlorocebus sabaeus. Calls given in response to the drone were clearly distinct from those given to other predators, but highly similar to the aerial alarm calls of the East African vervet monkey, Chlorocebus pygerythrus, suggesting that call structure is conserved. To probe how rapidly the animals attached meaning to the sound of the drone, we played back the drone sound after one to three exposures. Subjects immediately scanned the sky and ran for cover. In contrast to vocal production, comprehension learning was rapid and open-ended.

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Fig. 1: Structure and discriminability of green and vervet monkey alarm calls.
Fig. 2: Response to drone and control playbacks.

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Data availability

Data are available at https://doi.org/10.17605/OSF.IO/F4UTP.

Code availability

Code is available at https://doi.org/10.17605/OSF.IO/F4UTP.

References

  1. Fischer, J. Psychon. Bull. Rev. 24, 72–78 (2017).

    Article  Google Scholar 

  2. Fitch, W. T. The Evolution of Language (Cambridge University Press, 2010).

  3. Zuberbühler, K. Adv. Study Behav. 33, 265–307 (2003).

    Article  Google Scholar 

  4. Townsend, S. W. & Manser, M. B. Ethology 119, 1–11 (2013).

    Article  Google Scholar 

  5. Manser, M. B. Proc. R. Soc. B 268, 2315–2324 (2001).

    Article  CAS  Google Scholar 

  6. Gill, S. A. & Bierema, A. M.-K. Ethology 119, 449–461 (2013).

    Article  Google Scholar 

  7. Arnold, K. & Zuberbühler, K. Curr. Biol. 18, 202–203 (2008).

    Article  Google Scholar 

  8. Schamberg, I., Cheney, D. L., Clay, Z., Hohmann, G. & Seyfarth, R. M. Anim. Behav. 122, 109–116 (2016).

    Article  Google Scholar 

  9. Coye, C., Ouattara, K., Arlet, M. E., Lemasson, A. & Zuberbühler, K. Anim. Behav. 141, 171–181 (2018).

    Article  Google Scholar 

  10. ten Cate, C. Psychon. Bull. Rev. https://doi.org/10.3758/s13423-016-1091-9 (2016).

    Article  PubMed Central  Google Scholar 

  11. Seyfarth, R. M., Cheney, D. L. & Marler, P. Anim. Behav. 28, 1070–1094 (1980).

    Article  Google Scholar 

  12. Seyfarth, R. M., Cheney, D. L. & Marler, P. Science 210, 801–803 (1980).

    Article  CAS  Google Scholar 

  13. Struhsaker, T. T. in Social Communication among Primates (ed. Altmann, S.) 281–324 (University of Chicago Press, 1967).

  14. Price, T. et al. Sci. Rep. 5, 13220 (2015).

    Article  CAS  Google Scholar 

  15. Price, T. & Fischer, J. Anim. Cogn. 17, 277–286 (2014).

    Article  Google Scholar 

  16. Arnold, K., Pohlner, Y. & Zuberbühler, K. Behav. Ecol. Sociobiol. 62, 549–559 (2008).

    Article  Google Scholar 

  17. Mundry, R. & Sommer, C. Anim. Behav. 74, 965–976 (2007).

    Article  Google Scholar 

  18. Seyfarth, R. M. & Cheney, D. L. Anim. Behav. 34, 1640–1658 (1986).

    Article  Google Scholar 

  19. Price, T., Ndiaye, O. & Fischer, J. Behav. Ecol. Sociobiol. 68, 815–825 (2014).

    Article  Google Scholar 

  20. Hammerschmidt, K., Freudenstein, T. & Jürgens, U. Behaviour 138, 1179–1204 (2001).

    Article  Google Scholar 

  21. Winter, P. P., Handley, D. & Schott, D. Behaviour 47, 230–239 (1973).

    Article  CAS  Google Scholar 

  22. Owren, M. J., Dieter, J. A., Seyfarth, R. M. & Cheney, D. L. Dev. Psychobiol. 26, 389–406 (1993).

    Article  CAS  Google Scholar 

  23. Gultekin, Y. B. & Hage, S. R. Nat. Commun. 8, 14046 (2017).

    Article  CAS  Google Scholar 

  24. Takahashi, D. Y., Liao, D. A. & Ghazanfar, A. A. Curr. Biol. 27, 1844–1852.e6 (2017).

    Article  CAS  Google Scholar 

  25. Watson, S. K. et al. Curr. Biol. 25, 495–499 (2015).

    Article  CAS  Google Scholar 

  26. Fischer, J., Wheeler, B. C. & Higham, J. P. Curr. Biol. 25, R1028–R1029 (2015).

    Article  CAS  Google Scholar 

  27. Seyfarth, R. M. & Cheney, D. L. in Social influences on Vocal Development (eds Snowdon, C. T. & Hausberger, M.) 249–273 (Cambridge University Press, 1997).

  28. Fischer, J., Cheney, D. L. & Seyfarth, R. M. Proc. R. Soc. B 267, 2317–2321 (2000).

    Article  CAS  Google Scholar 

  29. Fischer, J. & Price, T. Neurosci. Biobehav. Rev. 82, 22–31 (2017).

    Article  Google Scholar 

  30. Hauser, M. D. Behaviour 105, 187–201 (1988).

    Article  Google Scholar 

  31. Zuberbühler, K. Proc. R. Soc. B 267, 713–718 (2000).

    Article  Google Scholar 

  32. Scott, B. H. & Mishkin, M. Brain Res. 1640, 264–277 (2016).

    Article  CAS  Google Scholar 

  33. Fischer, J., Wegdell, F. L. & Hammerschmidt, K. Conserved alarm calls but rapid auditory learning in monkey responses to novel flying objects – Data Set https://doi.org/10.17605/OSF.IO/F4UTP (2019).

  34. Schrader, L. & Hammerschmidt, K. Bioacoustics 7, 247–265 (1997).

    Article  Google Scholar 

  35. Fischer, J., Noser, R. & Hammerschmidt, K. Am. J. Primatol. 75, 643–663 (2013).

    Article  Google Scholar 

  36. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2017).

  37. Baayen, R. H., Davidson, D. J. & Bates, D. M. J. Mem. Lang. 59, 390–412 (2008).

    Article  Google Scholar 

  38. Barr, D. J., Levy, R., Scheepers, C. & Tily, H. J. Random effects structure for confirmatory hypothesis testing: keep it maximal. J. Mem. Lang. 68, 255–278 (2013).

  39. Simmons, J. P., Nelson, L. D. & Simonsohn, U. Psychol. Sci. 22, 1359–1366 (2011).

    Article  Google Scholar 

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Acknowledgements

We thank R. Seyfarth, D. Cheney and T. Struhsaker for sharing their recordings and insights into vervet monkey communication. Approval and research permission were granted by the Direction des Parcs Nationaux and the Ministère de l’Environnement et de la Protection de la Nature de la République du Sénégal (research permit Nos. 0373/10/3/2012 and 1480/11/11/2016). Research was conducted within the regulations set by Senegalese agencies. We thank Equipe Simenti for assistance with the data collection and L. Ehrenreich for logistic support and help with compilation of Fig. 1. Funding from the Leibniz ScienceCampus Primate Cognition is gratefully acknowledged.

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Contributions

F.W., K.H. and J.F. conceived the study. F.W. conducted the experiment. F.W., K.H. and J.F. conducted the acoustic and statistical analyses. J.F. wrote the paper with input from all authors.

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Correspondence to Julia Fischer.

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Supplementary Information

Supplementary Figs. 1–4 and Supplementary Tables 1–6

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Supplementary Video

Response of green monkey female to the playback of the drone sound

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Wegdell, F., Hammerschmidt, K. & Fischer, J. Conserved alarm calls but rapid auditory learning in monkey responses to novel flying objects. Nat Ecol Evol 3, 1039–1042 (2019). https://doi.org/10.1038/s41559-019-0903-5

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