Influence of season and social context on male giant panda (Ailuropoda melanoleuca) vocal behaviour

Autoři: Benjamin D. Charlton aff001;  Megan A. Owen aff001;  Xiaoping Zhou aff002;  Hemin Zhang aff002;  Ronald R. Swaisgood aff001
Působiště autorů: Institute for Conservation Research, San Diego Zoo Global, San Diego, California, United States of America aff001;  China Conservation and Research Center for the Giant Panda, Wolong, Sichuan, China aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225772


Documenting the different social and behavioural contexts that vocalisations are produced in remains an important step towards understanding the functional relevance of specific call types in a given species’ vocal repertoire. In this study we investigated whether seasonal differences and the presence or absence of male and female conspecifics influence the production of male giant panda vocal signals. To this end, captive male giant pandas were observed during and outside of the breeding season in three social contexts: only male conspecific neighbours, only female conspecific neighbours, and a context with no neighbours. We found that males were more likely to bleat, chirp, honk and moan during the breeding season, and showed a tendency to growl more outside of the reproductive period. The contextual analysis revealed that bleats were more likely to be produced by males when opposite-sexed conspecifics are in close attendance during the breeding season. Conversely, males were more likely to chirp when neighboured by males than females or no neighbours. In addition, males were more likely to honk in the absence of neighbouring conspecifics during the breeding season, raising the possibility that these calls function to signal location and gain the attention of potential mates. Moans were produced more often when male giant pandas had male than female neighbours during the breeding season, which may reflect mild aggression towards these same-sexed rivals, whereas the production of barks and growls did not vary according to season or the sex of conspecific neighbours. Our findings underscore the importance of male giant panda bleats for coordinating reproduction and promoting contact with potential mating partners in this non-gregarious species, and yield fresh insights into the function of male honks that warrant further investigation. They also provide a basis for comparison with free-ranging giant panda vocal behaviour that could potentially inform conservation efforts.

Klíčová slova:

Acoustic signals – Acoustics – Animal husbandry – Animal sexual behavior – Audio signal processing – Bioacoustics – Giant pandas – Vocalization


1. Charlton B, Ellis W, McKinnon A, Cowin G, Brumm J, Nilsson K, et al. Cues to body size in the formant spacing of male koala (Phascolarctos cinereus) bellows: honesty in an exaggerated trait. J Exp Biol. 2011;214(20):3414–22. doi: 10.1242/jeb.061358 WOS:000295322600014. 21957105

2. Wyman M, Mooring M, McCowan B, Penedo M, Reby D, Hart L. Acoustic cues to size and quality in the vocalizations of male North American bison, Bison bison. Anim Behav. 2012;84(6):1381–91.

3. Reby D, McComb K. Anatomical constraints generate honesty: acoustic cues to age and weight in the roars of red deer stags. Anim Behav. 2003;65:519–30. doi: 10.1006/anbe.2003.2078 ISI:000183484800012.

4. Semple S, McComb K, Alberts S, Altmann J. Information content of female copulation calls in yellow baboons. Am J Primatol. 2002;56(1):43–56. doi: 10.1002/ajp.1062 11793412.

5. Blumstein D, Munos O. Individual, age and sex-specific information is contained in yellow-bellied marmot alarm calls. Anim Behav. 2005.

6. Barelli C, Mundry R, Heistermann M, Hammerschmidt K. Cues to androgens and quality in male gibbon songs. PLoS ONE. 2013;8(12):e82748. doi: 10.1371/journal.pone.0082748 24367551

7. Pasch B, George AS, Campbell P, Phelps SM. Androgen-dependent male vocal performance influences female preference in Neotropical singing mice. Anim Behav. 2011;82(2):177–83. doi: 10.1016/j.anbehav.2011.04.018

8. Koren L, Geffen E. Complex call in male rock hyrax (Procavia capensis): a multi-information distributing channel. Behav Ecol Sociobiol. 2009;63(4):581–90. doi: 10.1007/s00265-008-0693-2

9. Taylor A, Charlton BD, Reby D. Vocal production by terrestrial mammals: source, filter and function. In: Suthers RA, Fitch WT, Fay RR, Popper A, editors. Vertebrate sound production and acoustic communication. Springer Handbook of Auditory Research. Berlin: Springer International Publishing; 2016. p. 229–59.

10. Barros KS, Tokumaru RS, Pedroza JP, Nogueira SSC. Vocal repertoire of captive capybara (Hydrochoerus hydrochaeris): structure, context and function. Ethology. 2010;117(1):83–94. doi: 10.1111/j.1439-0310.2010.01853.x

11. Boinski S, Mitchell CL. Ecological and social factors affecting the vocal behavior of adult female squirrel monkeys. Ethology. 1992;92(4):316–30. doi: 10.1111/j.1439-0310.1992.tb00969.x

12. Bowyer RT, Rachlow JL, Stewart KM, Van Ballenberghe V. Vocalizations by Alaskan moose: female incitation of male aggression. Behav Ecol Sociobiol. 2011;65(12):2251–60. doi: 10.1007/s00265-011-1234-y

13. McShane LJ, Estes JA, Riedman ML, Staedler MM. Repertoire, structure, and individual variation of vocalizations in the sea otter. J Mammal. 1995:414–27.

14. Wong J, Stewart PD, Macdonald DW. Vocal repertoire in the European badger (Meles meles): Structure, context, and function. J Mammal. 1999;80(2):570–88.

15. Minami M, Kawamichi T. Vocal repertoires and classification of the sika deer Cervus nippon. Journal of the Mammalogical Society of Japan. 1992;17(2):71–94. BCI:BCI199395095097.

16. Mitani JC. Sexual selection and adult male orangutan long calls. Anim Behav. 1985;33(FEB):272–83. ISI:A1985ABC1100026.

17. Berger J, Cunningham C. Bellows, copulations, and sexual selection in bison (Bison bison). Behav Ecol. 1991;2(1):1. 5093205576104217131related:Kwq7i3yzrkYJ.

18. McElligott AG, Hayden TJ. Context-related vocalization rates of fallow bucks, Dama dama. Anim Behav. 1999;58:1095–104. ISI:000083929700019. doi: 10.1006/anbe.1999.1237 10564612

19. Seyfarth RM, Cheney DL. Monkey responses to three different alarm calls: Evidence of predator classification and semantic communication. Science. 1980;210:801–3. doi: 10.1126/science.7433999 7433999

20. McComb K, Moss C, Sayialel S, Baker L. Unusually extensive networks of vocal recognition in African elephants. Anim Behav. 2000;59:1103–9. ISI:000088220000004. doi: 10.1006/anbe.2000.1406 10877888

21. Harrington FH, Mech LD. Wolf howling and its role in territory maintenance. Behaviour. 1979;68(3–4):207–49. doi: 10.1163/156853979X00322

22. Sekulic R. The function of howling in red howler monkeys (Alouatta seniculus). Behaviour. 1982;81:38–54. ISI:A1982PJ58500003.

23. Charlton B, Ellis W, Brumm J, Nilsson K, Fitch W. Female koalas prefer bellows in which lower formants indicate larger males. Anim Behav. 2012;84(6):1565–71. doi: 10.1016/j.anbehav.2012.09.034 WOS:000311953200035.

24. Charlton B, Reby D, McComb K. Female red deer prefer the roars of larger males. Biol Lett. 2007;3(4):382–5. doi: 10.1098/rsbl.2007.0244 WOS:000247907000009. 17550876

25. Schaller GB, Hu J, Pan W, Zhu J. The giant pandas of Wolong. Chicago: University of Chicago Press; 1985.

26. Liu X, Skidmore A, Wang T, Yong YG, Prins H. Giant panda movements in Foping Nature Reserve, China. J Wildl Manage. 2002;66(4):1179–88. doi: 10.2307/3802951

27. Connor T, Hull V, Liu J. Telemetry research on elusive wildlife: A synthesis of studies on giant pandas. Integr Zool. 2016;11(4):295–307. doi: 10.1111/1749-4877.12197 26940046

28. Swaisgood RR, Lindburg DG, White AM, Zhou X, Zhang H. Chemical communication in giant pandas: experimentation and application. In: Lindburg DG, Baragona K, editors. Giant pandas: biology and conservation. Berkeley and Los Angeles: University of California Press; 2004. p. 106–20.

29. Gilad O, Swaisgood RR, Owen MA, Zhou X. Giant pandas use odor cues to discriminate kin from nonkin. Curr Zool. 2016;62(4):333–6. doi: 10.1093/cz/zow025 29491921

30. Swaisgood RR, Lindburg DG, Zhou XP. Giant pandas discriminate individual differences in conspecific scent. Anim Behav. 1999;57:1045–53. doi: 10.1006/anbe.1998.1070 ISI:000080285600007. 10328790

31. Swaisgood RR, Lindburg DG, Zhou XP, Owen MA. The effects of sex, reproductive condition and context on discrimination of conspecific odours by giant pandas. Anim Behav. 2000;60:227–37. doi: 10.1006/anbe.2000.1464 10973725

32. Swaisgood RR, Lindburg DG, Zhang H. Discrimination of oestrous status in giant pandas (Ailuropoda melanoleuca) via chemical cues in urine. J Zool. 2002;257:381–6. doi: 10.1017/S0952836902000985

33. White AM, Swaisgood RR, Zhang H. The highs and lows of chemical communication in giant pandas (Ailuropoda melanoleuca): effect of scent deposition height on signal discrimination. Behav Ecol Sociobiol. 2002;51:519–29. doi: 10.1007/s00265-002-0473-3

34. White AM, Swaisgood RR, Zhang H. Chemical communication in giant pandas: The role of signaler and assessor age. J Zool. 2003;259(2):171–8.

35. Peters G. A note on the vocal behaviour of the giant panda, Ailuropoda melanoleuca (David 1869). Z Saugetierkd-Int J Mamm Biol. 1982;47:236–46.

36. Peters G. A comparative survey of vocalization in the giant panda (Ailuropoda melanoleuca, David 1869). Bongo (Berlin). 1985;10:197–208.

37. Charlton BD, Martin-Wintle MS, Owen MA, Zhang H, Swaisgood RR. Vocal behaviour predicts mating success in giant pandas. R Soc open sci. 2018;5(10):181323–15. doi: 10.1098/rsos.181323 30473861

38. Kleiman DG, Karesh WB, Chu PR. Behavioural changes associated with oestrus in the giant panda (Ailuropoda melanoleuca). International Zoo Yearbook. 1979;19:217–23.

39. Kleiman DG, Peters G, editors. Auditory communication in the giant panda: motivation and function. Second International Symposium on the Giant Panda; 1990; Tokyo: Tokyo Zoological Park Society.

40. Charlton BD, Martin-Wintle MS, Owen MA, Zhang H, Swaisgood RR. Vocal behaviour predicts mating success in giant pandas. R Soc open sci. 2018;5:181323–15. doi: 10.1098/rsos.181323 30473861

41. Charlton B, Zhang Z, Snyder R. Vocal cues to identity and relatedness in giant pandas (Ailuropoda melanoleuca). J Acoust Soc Am. 2009;126(5):2721–32. doi: 10.1121/1.3224720 WOS:000271507000066. 19894848

42. Charlton B, Zhihe Z, Snyder R. The information content of giant panda, Ailuropoda melanoleuca, bleats: acoustic cues to sex, age and size. Anim Behav. 2009;78(4):893–8. doi: 10.1016/j.anbehav.2009.06.029 WOS:000270021800016.

43. Charlton BD, Keating JL, Kersey D, Rengui L, Huang Y, Swaisgood RR. Vocal cues to male androgen levels in giant pandas. Biol Lett. 2011;7(1):71–4. doi: 10.1098/rsbl.2010.0582 20810426

44. Charlton BD, Keating JL, Rengui L, Huang Y, Swaisgood RR. The acoustic structure of male giant panda bleats varies according to intersexual context. J Acoust Soc Am. 2015;138(3):1305–12. doi: 10.1121/1.4928606 26428769

45. Charlton B, Huang Y, Swaisgood R. Vocal discrimination of potential mates by female giant pandas (Ailuropoda melanoleuca). Biol Lett. 2009;5(5):597–9. doi: 10.1098/rsbl.2009.0331 WOS:000269699300007. 19535366

46. Charlton B, Zhang Z, Snyder R. Giant pandas perceive and attend to formant frequency variation in male bleats. Anim Behav. 2010;79(6):1221–7. doi: 10.1016/j.anbehav.2010.02.018 WOS:000277933400008.

47. Charlton B, Swaisgood R, Zhihe Z, Snyder R. Giant pandas attend to androgen-related variation in male bleats. Behav Ecol Sociobiol. 2012;66(6):969–74. doi: 10.1007/s00265-012-1345-0 WOS:000304159600015.

48. Kleiman DG. Ethology and reproduction of captive giant pandas (Ailuropoda melanoleuca). Z Tierpsychol. 1983;62(1):1–46. doi: 10.1111/j.1439-0310.1983.tb02139.x WOS:A1983QQ52600001.

49. McGeehan L, Li X, Jackintell L, Huang S, Wang A, Czekala NM. Hormonal and behavioral correlates of estrus in captive giant pandas. Zoo Biology. 2002;21:449–66.

50. Charlton B, Keating J, Li R, Yan H, Swaisgood R. Female giant panda (Ailuropoda melanoleuca) chirps advertise the caller's fertile phase. Proceedings of the Royal Society B-Biological Sciences. 2010;277(1684):1101–6. doi: 10.1098/rspb.2009.1431 WOS:000274858500017. 19955154

51. Owen MA, Swaisgood RR, Zhou X, Blumstein DT. Signalling behaviour is influenced by transient social context in a spontaneously ovulating mammal. Anim Behav. 2016;111:157–65. doi: 10.1016/j.anbehav.2015.10.008

52. MacDonald E, Czekala NM, Wang P, Gual-Sil F, Nakao T. Urinary testosterone and cortisol metabolites in male giant pandas Ailuropoda melanoleuca in relation to breeding, housing, and season. Acta Zoologica Sinica. 2006;52(2):242–9.

53. Nie Y, Zhang Z, Swaisgood R, Wei F. Effects of season and social interaction on fecal testosterone metabolites in wild male giant pandas: implications for energetics and mating strategies. Eur J Wildl Res. 2012;58(1):235–41. doi: 10.1007/s10344-011-0569-z

54. Snyder RJ, Lawson DP, Zhang A, Zhang Z, Luo L, Zhong W, et al. Reproduction in giant pandas: hormones and behaviour. In: Lindburg DG, Baragona K, editors. Giant pandas: biology and conservation. Berkeley and Los Angeles, California: University of California Press; 2004. p. 125–32.

55. Bateson P, Martin P. Recording methods. In: Bateson P, Martin P, editors. Measuring Behaviour: An Introductory Guide. 2 ed. Cambridge: Cambridge University Press; 1993. p. 84–100.

56. Altmann J. Observational study of behaviour: sampling methods. Behaviour. 1974;48:499–509. doi: 10.1163/156853974X00534 4597405

57. O’Hara RB, Kotze DJ. Do not log-transform count data. Methods in Ecology and Evolution. 2010;1(2):118–22. doi: 10.1111/j.2041-210X.2010.00021.x

58. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, et al. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol. 2009;24(3):127–35. doi: 10.1016/j.tree.2008.10.008 19185386

59. Charlton B, McComb K, Reby D. Free-ranging red deer hinds show greater attentiveness to roars with formant frequencies typical of young males. Ethology. 2008;114(10):1023–31. doi: 10.1111/j.1439-0310.2008.01539.x WOS:000259524400010.

60. Charlton B, Reby D. Context-related acoustic variation in male fallow deer (Dama dama) groans. PLoS ONE. 2011;6(6). doi: 10.1371/journal.pone.0021066 WOS:000291663300037. 21695159

61. Nie Y, Swaisgood R, Zhang Z, Liu X, Wei F. Reproductive competition and fecal testosterone in wild male giant pandas (Ailuropoda melanoleuca). Behav Ecol Sociobiol. 2012;66(5):721–30. doi: 10.1007/s00265-012-1320-9

62. Marler P. Characteristics of some animal calls. Nature. 1955;176(4470):6–8. doi: 10.1038/176006a0

63. Owren MJ, Rendall D. Sound on the rebound: bringing form and function back to the forefront in understanding nonhuman primate vocal signaling. Evol Anthropol. 2001;10:58–71.

64. Manser MB. The evolution of auditory communication in suricates Suricata suricatta Cambridge, U.K.: Cambridge; 1998.

65. Reby D, Cargnelutti B, Hewison AJ. Contexts and possible functions of barking in roe deer. Anim Behav. 1999;57(5):1121–8. 10328799. doi: 10.1006/anbe.1998.1056 10328799

66. Yin S, McCowan B. Barking in domestic dogs: context specificity and individual identification. Anim Behav. 2004;68:343–55.

67. Swaisgood R, Wang D, Wei F. Ailuropoda melanoleuca. The IUCN Red List of Threatened Species [Internet]. 2016:[e.T712A121745669 p.].

68. Cohen JA, Fox MW. Vocalizations in wild canids and possible effects of domestication. Behav Processes. 1976;1(1):77–92. doi: 10.1016/0376-6357(76)90008-5 24923546

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