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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

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

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. 1.

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

    Article  Google Scholar 

  2. 2.

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

  3. 3.

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

    Article  Google Scholar 

  4. 4.

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

    Article  Google Scholar 

  5. 5.

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

    CAS  Article  Google Scholar 

  6. 6.

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

    Article  Google Scholar 

  7. 7.

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

    Article  Google Scholar 

  8. 8.

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

    Article  Google Scholar 

  9. 9.

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

    Article  Google Scholar 

  10. 10.

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

    Article  PubMed Central  Google Scholar 

  11. 11.

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

    Article  Google Scholar 

  12. 12.

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

    CAS  Article  Google Scholar 

  13. 13.

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

  14. 14.

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

    CAS  Article  Google Scholar 

  15. 15.

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

    Article  Google Scholar 

  16. 16.

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

    Article  Google Scholar 

  17. 17.

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

    Article  Google Scholar 

  18. 18.

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

    Article  Google Scholar 

  19. 19.

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

    Article  Google Scholar 

  20. 20.

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

    Article  Google Scholar 

  21. 21.

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

    CAS  Article  Google Scholar 

  22. 22.

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

    CAS  Article  Google Scholar 

  23. 23.

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

    CAS  Article  Google Scholar 

  24. 24.

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

    CAS  Article  Google Scholar 

  25. 25.

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

    CAS  Article  Google Scholar 

  26. 26.

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

    CAS  Article  Google Scholar 

  27. 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. 28.

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

    CAS  Article  Google Scholar 

  29. 29.

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

    Article  Google Scholar 

  30. 30.

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

    Article  Google Scholar 

  31. 31.

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

    Article  Google Scholar 

  32. 32.

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

    CAS  Article  Google Scholar 

  33. 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. 34.

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

    Article  Google Scholar 

  35. 35.

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

    Article  Google Scholar 

  36. 36.

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

  37. 37.

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

    Article  Google Scholar 

  38. 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. 39.

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

    Article  Google Scholar 

Download references

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.

Author information

Affiliations

Authors

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.

Corresponding author

Correspondence to Julia Fischer.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

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

Reporting Summary

Supplementary Video

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Further reading

Search

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing