Abstract
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.
Similar content being viewed by others
References
Adkins-Regan E (2005) Hormones and animal behavior. Princeton University Press, Princeton
Apicella CL, Feinberg DR (2009) Voice pitch alters mate-choice-relevant perception in hunter–gatherers. Proc R Soc Lond B 276:1077–1082
Archer J (2006) Testosterone and human aggression: an evaluation of the challenge hypothesis. Neurosci Biobehav Rev 30:319–345
Aureli F, Schaffner CM, Boesch C, Bearder SK, Call J et al (2008) Fission-fusion dynamics: new research frameworks. Curr Anthropol 49:627–654
Bailey WJ (2003) Insect duets: underlying mechanisms and their evolution. Physiol Entomol 28:157–174
Barelli C, Mundry R, Heistermann M, Hammerschmidt K (2013) Cues to androgen and quality in male gibbon songs. PLoS ONE 8:e82748
Basabose AK (2002) Diet composition of chimpanzees inhabiting the montane forest of Kahuzi, Democratic Republic of Congo. Am J Primatol 58:1–21
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 58:1149–1157
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 137:417–435
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 66:1044–1060
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 405–427
Chapman CA, Wrangham RW (1993) Range use of the forest chimpanzees of Kibale: implications of the understanding of chimpanzee social organization. Am J Primatol 31:263–273
Chapman CA, Wrangham RW, Chapman LJ (1995) Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 36:59–70
Clark AP, Wrangham RW (1994) Chimpanzee arrival pant-hoots: do they signify food or status? Int J Primatol 15:185–205
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 19:971–998
Cynx J, Bean NJ, Rossman I (2005) Testosterone implants alter the frequency range of zebra finch songs. Horm Behav 47:446–451
Dabbs JM, Mallinger A (1999) High testosterone levels predict low voice pitch among men. Personal Individ Differ 27:801–804
de Vries H (1993) Matman: a program for the analysis of sociometric matrices and behavioural transition matrices. Behaviour 125:157–175
de Vries H (1995) An improved test of linearity in dominance hierarchies containing unknown or tied relationships. Anim Behav 50:1375–1389
Delgado RA (2006) Sexual selection in the loud calls of male primates: signal content and function. Int J Primatol 27:5–25
Emerson SB, Boyd SK (1999) Mating vocalizations of female frogs: control and evolutionary mechanisms. Brain Behav Evol 53:187–197
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 55:299–305
Evans S, Neave N, Wakelin D, Hamilton C (2008) The relationship between testosterone and vocal frequencies in human males. Physiol Behav 93:783–788
Fedurek P, Machanda Z, Schel AM, Slocombe KE (2013a) Pant hoot chorusing and social bonds in male chimpanzees. Anim Behav 86:189–196
Fedurek P, Schel A, Slocombe KE (2013b) The acoustic structure of chimpanzee pant-hooting facilitates chorusing. Behav Ecol Sociobiol 67:1781–1789
Fedurek P, Donnellan E, Slocombe K (2014) Social and ecological correlates of long-distance pant hoot calls in male chimpanzees. Behav Ecol Sociobiol 68:1345–1355
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 56:140–148
Fitch WT, Reby D (2001) The descended larynx is not uniquely human. Proc R Soc Lond B 268:1669–1675
Floody OR (1981) The hormonal control of ultrasonic communication in rodents. Am Zool 21:129–142
Floody OR, Walsh C, Flanagan MT (1979) Testosterone stimulates ultrasound production by male hamsters. Horm Behav 12:164–171
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 117:480–489
Fusani L, Beani L, Dessi-Fulgheri F (1994) Testosterone affects the acoustic structure of the male call in the grey partridge (Perdix perdix). Behaviour 128:301–310
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:e83946
Geissmann T (1999) Duet songs of the siamang Hylobates syndactylus: II. Testing the pair-bonding hypothesis during a partner exchange. Behaviour 136:1005–1039
Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge
Hall ML (2009) A review of vocal duetting in birds. Adv Stud Behav 40:67–121
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 53–66
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 25:984–988
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 116–127
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 89:1117–1127
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 140:980–999
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 112–127
Kojima S, Izumi A, Ceugniet M (2003) Identification of vocalizers by pant hoots, pant grunts and screams in a chimpanzee. Primates 44:225–230
Marler P, Hobbett L (1975) Individuality in a long-range vocalization of wild chimpanzee. Z Tierpsychol 38:97–109
Marler CA, Ryan MJ (1996) Energetic constraints and steroid hormone correlates of male calling behaviour in the túngara frog. J Zool 240:397–409
McComb KE (1991) Female choice for high roaring rates in red deer, Cervus elaphus. Anim Behav 41:79–88
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 39:185–194
Mitani JC (2009) Male chimpanzees form enduring and equitable social bonds. Anim Behav 77:633–640
Mitani JC, Gros-Louis J (1998) Chorusing and call convergence in chimpanzees: tests of three hypotheses. Behaviour 135:1041–1064
Mitani JC, Nishida T (1993) Contexts and social correlates of long-distance calling by male chimpanzees. Anim Behav 45:735–746
Mitani JC, GrosLouis J, Macedonia JM (1996) Selection for acoustic individuality within the vocal repertoire of wild chimpanzees. Int J Primatol 17:569–583
Moore FL, Boyd SK, Kelley DB (2005) Historical perspective: hormonal regulation of behaviors in amphibians. Horm Behav 48:373–383
Muehlenbein M, Watts D (2010) The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees. Biopsychosoc Med 4:1–12
Muller MN, Lipson SF (2003) Diurnal patterns of urinary steroid excretion in wild chimpanzees. Am J Primatol 60:161–166
Muller MN, Mitani JC (2005) Conflict and cooperation in wild chimpanzees. Adv Stud Behav 35:275–331
Muller MN, Wrangham RW (2004) Dominance, aggression and testosterone in wild chimpanzees: a test of the ‘challenge hypothesis’. Anim Behav 67:113–123
Nelson RJ (2000) An introduction to behavioural endocrinology. Sinauer, Sunderland
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 79:187–193
Notman H (2003) The meaning, structure and function of chimpanzee pant hoots from the Budongo Forest, Uganda. PhD thesis. University of Calgary, Calgary
Notman H, Rendall D (2005) Contextual variation in chimpanzee pant hoots and its implications for referential communication. Anim Behav 70:177–190
Nowicki S, Ball GF (1989) Testosterone induction of song in photosensitive and photorefractory male sparrows. Horm Behav 23:514–525
Pasch B, George AS, Hamlin HJ, Guillette LJ Jr, Phelps SM (2011) Androgens modulate song effort and aggression in Neotropical singing mice. Horm Behav 59:90–97
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 69–86
Rangel-Negrín A, Dias PAD, Chavira R, Canales-Espinosa D (2011) Social modulation of testosterone levels in male black howlers (Alouatta pigra). Horm Behav 59:159–166
Reby D, McComb K (2003) Anatomical constraints generate honesty: acoustic cues to age and weight in the roars of red deer stags. Anim Behav 65:519–530
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 277:2747–2753
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 121:1758–1767
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 102:30–35
Sidak Z (1967) Rectangular confidence regions for the means of multivariate normal distributions. J Am Stat Assoc 62:626–633
Solis R (1994) Factores moduladores de las interacciones sociales acusticasde Pleurodema thaul. PhD thesis, Universidad de Chile
Solís R, Penna M (1997) Testosterone levels and evoked vocal responses in a natural population of the frog Batrachyla taeniata. Horm Behav 31:101–109
Struhsaker TT (1975) The red colobus monkey. University of Chicago Press, Chicago
Taylor AM, Reby D (2010) The contribution of source–filter theory to mammal vocal communication research. J Zool 280:221–236
Titze IR (1989) On the relation between subglottal pressure and fundamental frequency in phonation. J Acoust Soc Am 85:901–906
Titze IR (1994) Principles of voice production. Prentice Hall, Englewood Cliffs
Titze IR, Riede T (2010) A cervid vocal fold model suggests greater glottal efficiency in calling at high frequencies. PLoS Comput Biol 6:e1000897
Townsend DS, Moger WH (1987) Plasma androgen levels during male parental care in a tropical frog (Eleutherodactylus). Horm Behav 21:93–99
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 41:178–186
Waser MS (1977) Individual recognition, intragroup cohesion, and intergroup spacing: evidence from sound playback to forest monkeys. Behaviour 60:28–74
Watts DP (2002) Reciprocity and interchange in the social relationships of wild male chimpanzees. Behaviour 139:343–370
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 24:1251–1265
Wilczynski W, Lynch KS, O’Bryant EL (2005) Current research in amphibians: studies integrating endocrinology, behavior, and neurobiology. Horm Behav 48:440–450
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 83:277–291
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 204–215
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 81–98
Zahavi A (1975) Mate selection- selection for a handicap. J Theor Biol 53:205–214
Zahavi A (1977) The cost of honesty (further remarks on handicap principle). J Theor Biol 67:603–605
Zimmermann E (1996) Castration affects the emission of an ultrasonic vocalization in a nocturnal primate, the grey mouse lemur (Microcebus murinus). Physiol Behav 60:693–697
Zuberbühler K (2001) Predator-specific alarm calls in Campbell’s guenons. Behav Ecol Sociobiol 50:414–422
Acknowledgements
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.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
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.
Additional information
Communicated by R. I. M. Dunbar
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 28 kb)
Rights and permissions
About this article
Cite this article
Fedurek, P., Slocombe, K.E., Enigk, D.K. et al. The relationship between testosterone and long-distance calling in wild male chimpanzees. Behav Ecol Sociobiol 70, 659–672 (2016). https://doi.org/10.1007/s00265-016-2087-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-016-2087-1