Behavioral Ecology and Sociobiology

, Volume 70, Issue 5, pp 659–672 | Cite as

The relationship between testosterone and long-distance calling in wild male chimpanzees

  • Pawel FedurekEmail author
  • Katie E. Slocombe
  • Drew K. Enigk
  • Melissa Emery Thompson
  • Richard W. Wrangham
  • Martin N. MullerEmail author
Original Article


Long-distance calling is a common behaviour in animals, which has various important social functions. At a physiological level, calling is often mediated by gonadal hormones such as testosterone (T), particularly when its function is linked to intra-sexual competition for mates or territory. T also plays an important role in the development of vocal characteristics associated with dominance in humans. However, the few available studies of T and vocal behaviour in non-human primates suggest that in primates, T has less influence on call production than in other animals. We tested this hypothesis by studying the relationship between T concentrations and pant-hooting in wild male chimpanzees (Pan troglodytes schweinfurthii) of the Kanyawara community in the Kibale National Park, Uganda. We found three kinds of correlation. Hourly T averages were positively associated with hourly rates of pant-hooting. Monthly T levels were likewise correlated with monthly rates of pant-hooting after controlling for other influences such as fission-fusion rates. Finally, males with high T levels had higher peak frequency at the start of the call climax. These results suggest that T affects the production of pant-hoots in chimpanzees. This implies that the pant-hoot call plays a role in male-male competition. We propose that even in cognitively sophisticated species, endocrine mechanisms can contribute to regulating vocal production.

Significance statement

Many animals produce long-distance calls. The production of these calls is often modulated by gonadal hormones such as testosterone, especially if the calls are involved in competition between males for mates or territory. However, comparatively little is known about the influence of testosterone over the vocal behaviour of non-human primates, especially among great apes. In this study, we examined the relationship between testosterone and pant-hooting in wild male chimpanzees. We found that testosterone levels were associated with pant-hoot rates and one acoustic feature of the call. More specifically, males pant-hooted more often and produced pant-hoots with higher peak frequencies during periods of elevated testosterone levels. These results imply that gonadal hormones are involved in regulating vocal behaviour in chimpanzees and support the view that pant-hoots play a role in male-male competition.


Chimpanzee Testosterone Vocal behaviour Pant-hooting Acoustic structure 



Permission to conduct the study was granted by the Uganda Wildlife Authority and the Uganda National Council for Science and Technology. We would like to thank the KCP field manager Emily Otali and KCP field assistants Francis Mugurusi, Solomon Musana, James Kyomuhendo, Wilberforce Tweheyo, Sunday John and Christopher Irumba, who were extremely helpful during the fieldwork. We thank Hugh Notman for his insightful comments and suggestions that considerably improved the paper. This work was supported by a BBSRC studentship, an American Society of Primatologists General Small Grant, a NSF Graduate Research Fellowship, NSF grants no. 0849380 and no. 1355014, the Leakey Foundation and the Wenner-Gren Foundation. Research reported in this publication was also supported by the National Institute on Aging of the National Institutes of Health under Award Number R01AG049395. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Compliance with ethical standards

Ethical standards

Permission to conduct the study was granted by the Uganda Wildlife Authority and the Uganda National Council for Science and Technology. The study complied with the current laws of Uganda. This study was approved by, and carried out in accordance with, the Department of Psychology Ethics Committee at the University of York.

Supplementary material

265_2016_2087_MOESM1_ESM.docx (28 kb)
ESM 1 (DOCX 28 kb)


  1. Adkins-Regan E (2005) Hormones and animal behavior. Princeton University Press, PrincetonGoogle Scholar
  2. Apicella CL, Feinberg DR (2009) Voice pitch alters mate-choice-relevant perception in hunter–gatherers. Proc R Soc Lond B 276:1077–1082CrossRefGoogle Scholar
  3. Archer J (2006) Testosterone and human aggression: an evaluation of the challenge hypothesis. Neurosci Biobehav Rev 30:319–345CrossRefPubMedGoogle Scholar
  4. Aureli F, Schaffner CM, Boesch C, Bearder SK, Call J et al (2008) Fission-fusion dynamics: new research frameworks. Curr Anthropol 49:627–654CrossRefGoogle Scholar
  5. Bailey WJ (2003) Insect duets: underlying mechanisms and their evolution. Physiol Entomol 28:157–174CrossRefGoogle Scholar
  6. Barelli C, Mundry R, Heistermann M, Hammerschmidt K (2013) Cues to androgen and quality in male gibbon songs. PLoS ONE 8:e82748CrossRefPubMedPubMedCentralGoogle Scholar
  7. Basabose AK (2002) Diet composition of chimpanzees inhabiting the montane forest of Kahuzi, Democratic Republic of Congo. Am J Primatol 58:1–21CrossRefPubMedGoogle Scholar
  8. Beani L, Panzica G, Briganti F, Persichella P, Dessì-Fulgheri F (1995) Testosterone-induced changes of call structure, midbrain and syrinx anatomy in partridges. Physiol Behav 58:1149–1157CrossRefPubMedGoogle Scholar
  9. Beani L, Briganti F, Campanella G, Lupo C, Dessi-Fulgheri F (2000) Effect of androgenes on structure and rate of crowing in the Japanese quail Coturnix japonica. Behaviour 137:417–435CrossRefGoogle Scholar
  10. Boseret G, Carere C, Ball GF, Balthazart J (2006) Social context affects testosterone-induced singing and the volume of song control nuclei in male canaries (Serinus canaria). J Neurobiol 66:1044–1060CrossRefPubMedGoogle Scholar
  11. Bygott JD (1979) Agonistic behavior, dominance, and social structure in wild chimpanzees of the Gombe National Park. In: Hamburg D, McKown EA (eds) The Great Apes. Benjamin-Cummings, Menlo Park, pp 405–427Google Scholar
  12. Chapman CA, Wrangham RW (1993) Range use of the forest chimpanzees of Kibale: implications of the understanding of chimpanzee social organization. Am J Primatol 31:263–273CrossRefGoogle Scholar
  13. Chapman CA, Wrangham RW, Chapman LJ (1995) Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 36:59–70CrossRefGoogle Scholar
  14. Clark AP, Wrangham RW (1994) Chimpanzee arrival pant-hoots: do they signify food or status? Int J Primatol 15:185–205CrossRefGoogle Scholar
  15. Conklin-Brittain NL, Wrangham RW, Hunt KD (1998) Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. II. Macronutrients. Int J Primatol 19:971–998CrossRefGoogle Scholar
  16. Cynx J, Bean NJ, Rossman I (2005) Testosterone implants alter the frequency range of zebra finch songs. Horm Behav 47:446–451CrossRefPubMedGoogle Scholar
  17. Dabbs JM, Mallinger A (1999) High testosterone levels predict low voice pitch among men. Personal Individ Differ 27:801–804CrossRefGoogle Scholar
  18. de Vries H (1993) Matman: a program for the analysis of sociometric matrices and behavioural transition matrices. Behaviour 125:157–175CrossRefGoogle Scholar
  19. de Vries H (1995) An improved test of linearity in dominance hierarchies containing unknown or tied relationships. Anim Behav 50:1375–1389CrossRefGoogle Scholar
  20. Delgado RA (2006) Sexual selection in the loud calls of male primates: signal content and function. Int J Primatol 27:5–25CrossRefGoogle Scholar
  21. Emerson SB, Boyd SK (1999) Mating vocalizations of female frogs: control and evolutionary mechanisms. Brain Behav Evol 53:187–197CrossRefPubMedGoogle Scholar
  22. Emery Thompson M, Muller MN, Wrangham RW, Lwanga JS, Potts KB (2009) Urinary C-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees. Horm Behav 55:299–305CrossRefPubMedGoogle Scholar
  23. Evans S, Neave N, Wakelin D, Hamilton C (2008) The relationship between testosterone and vocal frequencies in human males. Physiol Behav 93:783–788CrossRefPubMedGoogle Scholar
  24. Fedurek P, Machanda Z, Schel AM, Slocombe KE (2013a) Pant hoot chorusing and social bonds in male chimpanzees. Anim Behav 86:189–196CrossRefGoogle Scholar
  25. Fedurek P, Schel A, Slocombe KE (2013b) The acoustic structure of chimpanzee pant-hooting facilitates chorusing. Behav Ecol Sociobiol 67:1781–1789CrossRefGoogle Scholar
  26. Fedurek P, Donnellan E, Slocombe K (2014) Social and ecological correlates of long-distance pant hoot calls in male chimpanzees. Behav Ecol Sociobiol 68:1345–1355CrossRefGoogle Scholar
  27. Fischer J, Kitchen DM, Seyfarth RM, Cheney DL (2004) Baboon loud calls advertise male quality: acoustic features and their relation to rank, age, and exhaustion. Behav Ecol Sociobiol 56:140–148CrossRefGoogle Scholar
  28. Fitch WT, Reby D (2001) The descended larynx is not uniquely human. Proc R Soc Lond B 268:1669–1675CrossRefGoogle Scholar
  29. Floody OR (1981) The hormonal control of ultrasonic communication in rodents. Am Zool 21:129–142CrossRefGoogle Scholar
  30. Floody OR, Walsh C, Flanagan MT (1979) Testosterone stimulates ultrasound production by male hamsters. Horm Behav 12:164–171CrossRefPubMedGoogle Scholar
  31. Furmankiewicz J, Ruczynski I, Urban R, Jones G (2001) Social calls provide tree-dwelling bats with information about the location of conspecifics at roosts. Ethology 117:480–489CrossRefGoogle Scholar
  32. Fusani L, Beani L, Dessi-Fulgheri F (1994) Testosterone affects the acoustic structure of the male call in the grey partridge (Perdix perdix). Behaviour 128:301–310CrossRefGoogle Scholar
  33. Garcia M, Charlton BD, Wyman MT, Fitch WT, Reby D (2013) Do red deer stags Cervus elaphus use roar fundamental frequency (F0) to assess rivals? PLoS ONE 8:e83946CrossRefPubMedPubMedCentralGoogle Scholar
  34. Geissmann T (1999) Duet songs of the siamang Hylobates syndactylus: II. Testing the pair-bonding hypothesis during a partner exchange. Behaviour 136:1005–1039CrossRefGoogle Scholar
  35. Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, CambridgeGoogle Scholar
  36. Hall ML (2009) A review of vocal duetting in birds. Adv Stud Behav 40:67–121CrossRefGoogle Scholar
  37. Harding CF (1991) Neuroendocrine integration of social behaviour in male songbirds. In: Archer T, Hansen S (eds) Behavioral biology: neuroendocrine axis. Hillsdale, New York, pp 53–66Google Scholar
  38. Hodges-Simeon CR, Gurven M, Puts DA, Gaulin SJC (2014) Vocal fundamental and formant frequencies are honest signals of threat potential in peripubertal males. Behav Ecol 25:984–988CrossRefPubMedPubMedCentralGoogle Scholar
  39. Isabirye-Basuta G (1987) Feeding ecology of chimpanzees in the Kibale Forest. In: Heltne PG, Marquardt LA (eds) Understanding chimpanzees. Harvard University Press, Cambridge, pp 116–127Google Scholar
  40. Kapusta J, Pochroń E (2011) Effect of gonadal hormones and sexual experience on vocalizations and behavior of male bank voles (Myodes glareolus). Can J Zool 89:1117–1127CrossRefGoogle Scholar
  41. Ketterson ED, Jr VN, Wolf L, Ziegenfus C (1992) Testosterone and avian life histories: effects of experimentally elevated testosterone on behavior and correlates of fitness in the dark-eyed junco (Junco hyemalis). Am Nat 140:980–999CrossRefGoogle Scholar
  42. Knott CD (2009) Orangutans: sexual coercion without sexual violence. In: Muller MN, Wrangham RW (eds) Sexual coercion in primates and humans: an evolutionary perspective on male aggression against females. Harvard University Press, Cambridge, pp 112–127Google Scholar
  43. Kojima S, Izumi A, Ceugniet M (2003) Identification of vocalizers by pant hoots, pant grunts and screams in a chimpanzee. Primates 44:225–230CrossRefPubMedGoogle Scholar
  44. Marler P, Hobbett L (1975) Individuality in a long-range vocalization of wild chimpanzee. Z Tierpsychol 38:97–109CrossRefGoogle Scholar
  45. Marler CA, Ryan MJ (1996) Energetic constraints and steroid hormone correlates of male calling behaviour in the túngara frog. J Zool 240:397–409CrossRefGoogle Scholar
  46. McComb KE (1991) Female choice for high roaring rates in red deer, Cervus elaphus. Anim Behav 41:79–88CrossRefGoogle Scholar
  47. McDonald PG, Buttemer WA, Astheimer LB (2001) The influence of testosterone on territorial defence and parental behavior in male free-living rufous whistlers, Pachycephala rufiventris. Horm Behav 39:185–194CrossRefPubMedGoogle Scholar
  48. Mitani JC (2009) Male chimpanzees form enduring and equitable social bonds. Anim Behav 77:633–640CrossRefGoogle Scholar
  49. Mitani JC, Gros-Louis J (1998) Chorusing and call convergence in chimpanzees: tests of three hypotheses. Behaviour 135:1041–1064CrossRefGoogle Scholar
  50. Mitani JC, Nishida T (1993) Contexts and social correlates of long-distance calling by male chimpanzees. Anim Behav 45:735–746CrossRefGoogle Scholar
  51. Mitani JC, GrosLouis J, Macedonia JM (1996) Selection for acoustic individuality within the vocal repertoire of wild chimpanzees. Int J Primatol 17:569–583CrossRefGoogle Scholar
  52. Moore FL, Boyd SK, Kelley DB (2005) Historical perspective: hormonal regulation of behaviors in amphibians. Horm Behav 48:373–383CrossRefPubMedGoogle Scholar
  53. Muehlenbein M, Watts D (2010) The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees. Biopsychosoc Med 4:1–12CrossRefGoogle Scholar
  54. Muller MN, Lipson SF (2003) Diurnal patterns of urinary steroid excretion in wild chimpanzees. Am J Primatol 60:161–166CrossRefPubMedGoogle Scholar
  55. Muller MN, Mitani JC (2005) Conflict and cooperation in wild chimpanzees. Adv Stud Behav 35:275–331CrossRefGoogle Scholar
  56. Muller MN, Wrangham RW (2004) Dominance, aggression and testosterone in wild chimpanzees: a test of the ‘challenge hypothesis’. Anim Behav 67:113–123CrossRefGoogle Scholar
  57. Nelson RJ (2000) An introduction to behavioural endocrinology. Sinauer, SunderlandGoogle Scholar
  58. Neumann C, Assahad G, Hammerschmidt K, Perwitasari-Farajallah D, Engelhardt A (2010) Loud calls in male crested macaques, Macaca nigra: a signal of dominance in a tolerant species. Anim Behav 79:187–193CrossRefGoogle Scholar
  59. Notman H (2003) The meaning, structure and function of chimpanzee pant hoots from the Budongo Forest, Uganda. PhD thesis. University of Calgary, CalgaryGoogle Scholar
  60. Notman H, Rendall D (2005) Contextual variation in chimpanzee pant hoots and its implications for referential communication. Anim Behav 70:177–190CrossRefGoogle Scholar
  61. Nowicki S, Ball GF (1989) Testosterone induction of song in photosensitive and photorefractory male sparrows. Horm Behav 23:514–525CrossRefPubMedGoogle Scholar
  62. Pasch B, George AS, Hamlin HJ, Guillette LJ Jr, Phelps SM (2011) Androgens modulate song effort and aggression in Neotropical singing mice. Horm Behav 59:90–97CrossRefPubMedGoogle Scholar
  63. Puts DA, Doll LM, Hill AK (2014) Sexual selection on human voices. In: Weekes-Shackelford V, Shackelford TK (eds) Evolutionary perspectives on human sexual psychology and behavior. Springer, New York, pp 69–86CrossRefGoogle Scholar
  64. Rangel-Negrín A, Dias PAD, Chavira R, Canales-Espinosa D (2011) Social modulation of testosterone levels in male black howlers (Alouatta pigra). Horm Behav 59:159–166CrossRefPubMedGoogle Scholar
  65. Reby D, McComb K (2003) Anatomical constraints generate honesty: acoustic cues to age and weight in the roars of red deer stags. Anim Behav 65:519–530CrossRefGoogle Scholar
  66. Reby D, Charlton BD, Locatelli Y, McComb K (2010) Oestrous red deer hinds prefer male roars with higher fundamental frequencies. Proc R Soc Lond B 277:2747–2753CrossRefGoogle Scholar
  67. Riede T, Arcadi AC, Owren MJ (2007) Nonlinear acoustics in the pant hoots of common chimpanzees (Pan troglodytes): vocalizing at the edge. J Acoust Soc Am 121:1758–1767CrossRefPubMedGoogle Scholar
  68. Ritschard M, Laucht S, Dale J, Brumm H (2011) Enhanced testosterone levels affect singing motivation but not song structure and amplitude in Bengalese finches. Physiol Behav 102:30–35CrossRefPubMedGoogle Scholar
  69. Sidak Z (1967) Rectangular confidence regions for the means of multivariate normal distributions. J Am Stat Assoc 62:626–633Google Scholar
  70. Solis R (1994) Factores moduladores de las interacciones sociales acusticasde Pleurodema thaul. PhD thesis, Universidad de ChileGoogle Scholar
  71. Solís R, Penna M (1997) Testosterone levels and evoked vocal responses in a natural population of the frog Batrachyla taeniata. Horm Behav 31:101–109CrossRefPubMedGoogle Scholar
  72. Struhsaker TT (1975) The red colobus monkey. University of Chicago Press, ChicagoGoogle Scholar
  73. Taylor AM, Reby D (2010) The contribution of source–filter theory to mammal vocal communication research. J Zool 280:221–236CrossRefGoogle Scholar
  74. Titze IR (1989) On the relation between subglottal pressure and fundamental frequency in phonation. J Acoust Soc Am 85:901–906CrossRefPubMedGoogle Scholar
  75. Titze IR (1994) Principles of voice production. Prentice Hall, Englewood CliffsGoogle Scholar
  76. Titze IR, Riede T (2010) A cervid vocal fold model suggests greater glottal efficiency in calling at high frequencies. PLoS Comput Biol 6:e1000897CrossRefPubMedPubMedCentralGoogle Scholar
  77. Townsend DS, Moger WH (1987) Plasma androgen levels during male parental care in a tropical frog (Eleutherodactylus). Horm Behav 21:93–99CrossRefPubMedGoogle Scholar
  78. Van Duyse E, Pinxten R, Eens M (2002) Effects of testosterone on song, aggression, and nestling feeding behavior in male great tits, Parus major. Horm Behav 41:178–186CrossRefPubMedGoogle Scholar
  79. Waser MS (1977) Individual recognition, intragroup cohesion, and intergroup spacing: evidence from sound playback to forest monkeys. Behaviour 60:28–74CrossRefGoogle Scholar
  80. Watts DP (2002) Reciprocity and interchange in the social relationships of wild male chimpanzees. Behaviour 139:343–370CrossRefGoogle Scholar
  81. Wich SA, van der Post DJ, Heistermann M, Möhle U, van Hooff JARAM, Sterck EHM (2003) Life-phase related changes in male loud call characteristics and testosterone levels in wild Thomas langurs. Int J Primatol 24:1251–1265CrossRefGoogle Scholar
  82. Wilczynski W, Lynch KS, O’Bryant EL (2005) Current research in amphibians: studies integrating endocrinology, behavior, and neurobiology. Horm Behav 48:440–450CrossRefPubMedPubMedCentralGoogle Scholar
  83. Wilson ML, Kahlenberg SM, Wells M, Wrangham RW (2012) Ecological and social factors affect the occurrence and outcomes of intergroup encounters in chimpanzees. Anim Behav 83:277–291CrossRefGoogle Scholar
  84. Wrangham RW (2002) The cost of sexual attraction: is there a trade-off in female Pan between sex appeal and received coercion? In: Boesch C, Hohmann G, Marchant L (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, Cambridge, pp 204–215CrossRefGoogle Scholar
  85. Wrangham RW, Clark AP, Isabirye-Basuta G (1992) Female social relationships and social organization of Kibale Forest chimpanzees. In: Nishida T, McGrew WC, Marler P, Pickford M, de Waal FBM (eds) Human origins. The University of Tokyo Press, Tokyo, pp 81–98Google Scholar
  86. Zahavi A (1975) Mate selection- selection for a handicap. J Theor Biol 53:205–214CrossRefPubMedGoogle Scholar
  87. Zahavi A (1977) The cost of honesty (further remarks on handicap principle). J Theor Biol 67:603–605CrossRefPubMedGoogle Scholar
  88. Zimmermann E (1996) Castration affects the emission of an ultrasonic vocalization in a nocturnal primate, the grey mouse lemur (Microcebus murinus). Physiol Behav 60:693–697CrossRefPubMedGoogle Scholar
  89. Zuberbühler K (2001) Predator-specific alarm calls in Campbell’s guenons. Behav Ecol Sociobiol 50:414–422CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Pawel Fedurek
    • 1
    Email author
  • Katie E. Slocombe
    • 2
  • Drew K. Enigk
    • 3
  • Melissa Emery Thompson
    • 3
  • Richard W. Wrangham
    • 4
  • Martin N. Muller
    • 3
    Email author
  1. 1.Institute of BiologyUniversity of NeuchâtelNeuchâtelSwitzerland
  2. 2.Department of PsychologyUniversity of YorkYorkUK
  3. 3.Department of AnthropologyUniversity of New MexicoAlbuquerqueUSA
  4. 4.Department of Human Evolutionary BiologyHarvard UniversityCambridgeUSA

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