Behavioral Ecology and Sociobiology

, Volume 67, Issue 9, pp 1457–1469 | Cite as

Signaling in multiple modalities in male rhesus macaques: sex skin coloration and barks in relation to androgen levels, social status, and mating behavior

  • James P. Higham
  • Dana Pfefferle
  • Michael Heistermann
  • Dario Maestripieri
  • Martin Stevens
Original Paper


The past decade has seen an increasing shift in animal communication towards more studies that incorporate aspects of signaling in multiple modalities. Although nonhuman primates are an excellent group for studying the extent to which different aspects of condition may be signaled in different modalities, and how such information may be integrated during mate choice, very few studies of primate species have incorporated such analyses. Here, we present data from free-ranging male rhesus macaques on sex skin coloration (modeled to receiver perception), bark vocal signals, androgen levels, morphometric variables, dominance status, and female mate choice. We show that, consistent with data on females, most intra- and interindividual variation in sex skin appearance occurs in luminance rather than color. Sex skin luminance was significantly correlated across different skin regions. Sex skin luminance did not correlate with the majority of bark parameters, suggesting the potential for the two signals to convey different information. Sex skin appearance was not related to androgen levels although we found some evidence for links between androgen levels and bark parameters, several of which were also related to morphometric variables. We found no evidence that either signal was related to male dominance rank or used in female mate choice, though more direct measures of female proceptive behavior are needed. Overall, the function of male sex skin coloration in this species remains unclear. Our study is among the first nonhuman primate studies to incorporate measurements of multiple signals in multiple modalities, and we encourage other authors to incorporate such analyses into their work.


Coloration Luminance Vocal signals Multimodal Primate Rhesus macaques 



We thank Doreen Hess, Jenna Goldfein, Maria Rakhovskaya, and the staff of the Caribbean Primate Research Center for logistical support in the field and assistance with animal capturing and handling. We are extremely grateful to Andrea Heistermann and Petra Kiesel for analyzing the fecal samples and to Tara Mandalaywala and the Caribbean Primate Research Center for assisting with their transportation to Germany. We are also most grateful to John Addicott for first helping us to develop our behavioral data parser and Access database. We additionally thank Kurt Hammerschmidt for making his LMA sound analysis program available. Eileen Hebets and two anonymous reviewers provided constructive and helpful comments on the manuscript. This research was supported by NIH grant R21-AG029862 to D.M. M.S. was supported by a Biotechnology and Biological Sciences Research Council David Phillips Research Fellowship (BB/G022887/1). This publication was made possible by grant number CM-5-P40RR003640 from the NIH National Center for Research Resources (NCRR) to the Caribbean Primate Research Center of the University of Puerto Rico. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of NCRR or NIH.

Ethical standards

This study was conducted in accordance with the NIH Guide for the Care and Use of Laboratory Animals and conformed to all laws of Puerto Rico, the USA, and Germany. The protocol for this study was approved by the Institutional Animal Care and Use Committee, Medical Sciences Department, University of Puerto Rico.

Conflict of interest

The authors declare no conflict of interest.


  1. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  2. Berard JD, Nürnberg P, Epplen JT, Schmidtke J (1994) Alternative reproductive tactics and reproductive success in male rhesus macaques. Behaviour 129:177–201CrossRefGoogle Scholar
  3. Bergman TJ, Beehner JC (2008) A simple method for measuring colour in wild animals: validation and use on chest patch colour in geladas (Theropithecus gelada). Biol J Linn Soc 94:231–240CrossRefGoogle Scholar
  4. Bergman TJ, Ho L, Beehner JC (2009) Chest color and social status in male geladas (Theropithecus gelada). Int J Primatol 30:791–806CrossRefGoogle Scholar
  5. Boulet M, Charpentier MJE, Drea CM (2009) Decoding an olfactory mechanism of kin recognition and inbreeding avoidance in primates. BMC Evol Biol 9:281PubMedCrossRefGoogle Scholar
  6. Bowmaker JK, Dartnall HJA, Lythgoe JN, Mollon JD (1978) The visual pigments of rods and cones in the rhesus monkey Macaca mulatta. J Physiol 274:329–348PubMedGoogle Scholar
  7. Bradley BJ, Mundy NI (2008) The primate palette: the evolution of primate coloration. Evol Anthropol 17:97–111CrossRefGoogle Scholar
  8. Campbell BC, Gerald MS (2004) Body composition, age and fertility among free-ranging female rhesus macaques (Macaca mulatta). J Med Primatol 33:70–77Google Scholar
  9. Cerda-Molina AL, Hernández-López L, Rojas-Maya S, Murcia-mejía C, Mondragón-Ceballos R (2006) Male-induced sociosexual behavior by vaginal secretions in Macaca arctoides. Int J Primatol 27:791–807CrossRefGoogle Scholar
  10. Charpentier MJE, Crawford J, Boulet M, Drea CM (2010) Message ‘scent’: lemurs detect the genetic relatedness and quality of conspecifics via olfactory cues. Anim Behav 80:101–108CrossRefGoogle Scholar
  11. Clarke PM, Barrett L, Henzi SP (2009) What role do olfactory cues play in baboon mating? Am J Primatol 71:493–502PubMedCrossRefGoogle Scholar
  12. Dartnall HJA, Bowmaker JK, Mollon JD (1983) Human visual pigments: microspectrophotometric results from the eyes of seven persons. Proc R Soc Lond B 220:115–130PubMedCrossRefGoogle Scholar
  13. Darwin C (1871) The descent of man and selection in relation to sex. John Murray, LondonCrossRefGoogle Scholar
  14. Darwin C (1872) The expression of the emotions in man and animals. John Murray, LondonCrossRefGoogle Scholar
  15. Darwin C (1876) Sexual selection in relation to monkeys. Nature 15:18–19CrossRefGoogle Scholar
  16. Deschner T, Heistermann M, Hodges K, Boesch C (2004) Female sexual swelling size, timing of ovulation and male behavior in wild West African chimpanzees. Horm Behav 46:204–215PubMedCrossRefGoogle Scholar
  17. Dixson AF (2012) Primate sexuality: comparative studies of prosimians, monkeys, apes, and human beings (2nd edn). Oxford University Press, OxfordGoogle Scholar
  18. Dubuc C, Brent LJN, Accamando AK, Gerald MS, MacLarnon A, Semple S, Heistermann M, Engelhardt A (2009) Sexual skin color contains information about the timing of the fertile phase in free-ranging rhesus macaques. Int J Primatol 30:777–789CrossRefGoogle Scholar
  19. Dubuc C, Muniz L, Heistermann M, Engelhardt A, Widdig A (2011) Testing the priority-of-access model in a seasonally breeding primate species Macaca mulatta). Behav Ecol Sociobiol 65:1615–1627PubMedCrossRefGoogle Scholar
  20. Emery MA, Whitten PL (2003) Size of sexual swellings reflects ovarian function in chimpanzees (Pan troglodytes). Behav Ecol Sociobiol 54:340–351CrossRefGoogle Scholar
  21. Endler JA, Mielke PW (2005) Comparing entire colour patterns as birds see them. Biol J Linn Soc 86:405–431Google Scholar
  22. Engelhardt A, Fischer J, Neumann C, Pfeifer J-B, Heistermann M (2012) Information content of female copulation calls in wild long-tailed macaques (Macaca fascicularis). Behav Ecol Sociobiol 66:121–134PubMedCrossRefGoogle Scholar
  23. Fant G (1960) Acoustic theory of speech production. Mouton & Co, The HagueGoogle Scholar
  24. Fitch WT (1997) Vocal tract length and formant frequency dispersion correlate with body size in rhesus macaques. J Acoust Soc Am 102:1213–1222PubMedCrossRefGoogle Scholar
  25. Gerald MS (2001) Primate colour predicts social status and aggressive outcome. Anim Behav 61:559–566CrossRefGoogle Scholar
  26. Gerritsma EJ, Brocaar MP, Hakkesteegt MM, Birkenhager JC (1994) Virilization of the voice in postmenopausal women due to the anabolic-steroid Nandrolone Decanoate (Decadurabolin)—the effects of medication for one-year. Clin Otolaryngol 19:79–84PubMedCrossRefGoogle Scholar
  27. Gesquiere LR, Wango EO, Alberts SC, Altmann J (2007) Mechanisms of sexual selection: sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons. Horm Behav 51:114–125PubMedCrossRefGoogle Scholar
  28. Ghazanfar AA, Maier JX, Hoffman KL, Logothetis NK (2005) Multisensory integration of dynamic faces and voices in primate auditory cortex. Journal of Neuroscience 25:5004–5012Google Scholar
  29. Ghazanfar AA, Turesson HK, Maier JX, van Dinther R, Patterson RD, Logothetis NK (2007) Vocal tract resonances as indexical cues in rhesus monkeys. Curr Biol 17:425–430PubMedCrossRefGoogle Scholar
  30. Girard-Buttoz C, Heistermann M, Krummel S, Engelhardt A (2009) Seasonal and social influences on fecal androgen and glucocorticoid excretion in wild male long-tailed macaques (Macaca fascicularis). Physiol Behav 98:168–175PubMedCrossRefGoogle Scholar
  31. Gustison ML, le Roux A, Bergman TJ (2012) Derived vocalisations of geladas (Theropithecus gelada) and the evolution of vocal complexity in primates. Philos Trans R Soc B 367:1847–1859CrossRefGoogle Scholar
  32. Hammerschmidt K (1990) Individuelle Lautmuster bei Berberaffen (Macaca sylvanus): Ein Ansatz zum Verständnis ihrer vokalen Kommunikation. Diss Freie Universtät, BerlinGoogle Scholar
  33. Hauser MD (1992) Costs of deception: cheaters are punished in rhesus monkeys (Macaca mulatta). P Natl Acad Sci U S A 89:12137–12139CrossRefGoogle Scholar
  34. Hauser MD (1993) Rhesus monkey copulation calls: honest signals for female choice? Proc R Soc Lond B 254:93–96CrossRefGoogle Scholar
  35. Hauser MD, Evans CS, Marler P (1993) The role of articulation in the production of rhesus monkey, Macaca mulatta, vocalizations. Anim Behav 45:423–433CrossRefGoogle Scholar
  36. Hebets EA, Papaj DR (2005) Complex signal function: developing a testable framework for testable hypotheses. Behav Ecol Sociobiol 57:197–214CrossRefGoogle Scholar
  37. Hebets EA, Uetz GW (1999) Female responses to isolated signals from multimodal male courtship displays in the wolf spider genus Schizocosa (Araneae: Lycosidae). Anim Behav 57:865–872PubMedCrossRefGoogle Scholar
  38. Heistermann M, Finke M, Hodges JK (1995) Assessment of female reproductive status in captive-housed Hanuman langurs (Presbytis entellus) by measurement of urinary and fecal steroid excretion patterns. Am J Primatol 37:275–284CrossRefGoogle Scholar
  39. Heymann EW (2006a) Introduction: the neglected sense—olfaction in primate behaviour, ecology, and evolution. Am J Primatol 68:519–524PubMedCrossRefGoogle Scholar
  40. Heymann EW (2006b) Scent marking strategies of New World primates. Am J Primatol 68:650–661PubMedCrossRefGoogle Scholar
  41. Higham JP (2006) The reproductive ecology of female olive baboons (Papio hamdryas anubis) at Gashaka-Gumti National Park, Nigeria. PhD thesis, Roehampton University, LondonGoogle Scholar
  42. Higham JP (2009) Primate coloration: an introduction to the special issue. Int J Primatol 30:749–751CrossRefGoogle Scholar
  43. Higham JP, Maestripieri D (2010) Revolutionary coalitions in male rhesus macaques. Behaviour 147:1889–1908CrossRefGoogle Scholar
  44. Higham JP, MacLarnon AM, Ross C, Heistermann M, Semple S (2008) Baboon sexual swellings: Information content of size and color. Horm Behav 53:452–462PubMedCrossRefGoogle Scholar
  45. Higham JP, Brent LJN, Dubuc C, Accamando AK, Engelhardt A, Gerald MS, Heistermann M, Stevens M (2010) Color signal information content and the eye of the beholder: a case study in the rhesus macaque. Behav Ecol 21:739–746PubMedCrossRefGoogle Scholar
  46. Higham JP, Hughes KD, Brent LJN, Dubuc C, Engelhardt A, Heistermann M, Maestripieri D, Santos LR, Stevens M (2011a) Familiarity affects assessment of facial signals of female fertility by free-ranging male rhesus macaques. Proc R Soc Lond B 278:3452–3458CrossRefGoogle Scholar
  47. Higham JP, Heistermann M, Maestripieri D (2011b) The energetics of male–male endurance rivalry in rhesus macaques. Anim Behav 81:1001–1007CrossRefGoogle Scholar
  48. Higham JP, Heistermann M, Saggau C, Agil M, Perwitasari-Farajallah D, Engelhardt A (2012) Sexual signaling in the crested macaque and the evolution of primate fertility signals. BMC Evol Biol 12:89PubMedCrossRefGoogle Scholar
  49. Higham JP, Heistermann M, Maestripieri D (2013) The endocrinology of male rhesus macaque social and reproductive status: a test of the challenge and social stress hypotheses. Behav Ecol Sociobiol 67:19–30CrossRefGoogle Scholar
  50. Hodges JK, Heistermann M (2011) Field endocrinology: monitoring hormonal changes in free-ranging primates. In: Setchell JM, Curtis DJ (eds) Field and laboratory methods in primatology, 2nd edn. Cambridge University Press, Cambridge, pp 282–294Google Scholar
  51. Hoffman CL, Ruiz-Lambides AV, Davila E, Maldonado E, Gerald MS, Maestripieri D (2008) Sex differences in survival costs of reproduction in a promiscuous primate. Behav Ecol Sociobiol 62:1711–1718PubMedCrossRefGoogle Scholar
  52. Khan SA, Levine WJ, Dobson SD, Kralik JD (2011) Red signals dominance in male rhesus macaques. Psychol Sci 22:1001–1003PubMedCrossRefGoogle Scholar
  53. Manson JH (1995) Do female rhesus macaques choose novel males? Am J Primatol 37:285–296CrossRefGoogle Scholar
  54. Manson JH (1996) Rhesus macaque copulation calls: re-evaluating the “honest signal” hypothesis. Primates 37:145–154CrossRefGoogle Scholar
  55. Marty JS, Higham JP, Gadsby EL, Ross C (2009) Dominance, coloration and social and sexual behavior in male drills (Mandrillus leucophaeus). Int J Primatol 30:807–823CrossRefGoogle Scholar
  56. Michael RP, Keverne EB (1968) Pheromones in the communication of sexual status in primates. Nature 218:746–749PubMedCrossRefGoogle Scholar
  57. Möhle U, Heistermann M, Palme R, Hodges JK (2002) Characterization of urinary and fecal metabolites of testosterone and their measurement for assessing gonadal endocrine function in male nonhuman primates. Gen Comp Endocrinol 129:135–145PubMedCrossRefGoogle Scholar
  58. Neumann C, Assahad G, Hammerschmidt K, Farajallah DP, Engelhardt A (2010) Loud calls in male Macaca nigra—a signal of dominance in a tolerant primate species. Anim Behav 79:187–193CrossRefGoogle Scholar
  59. Newman SR, Butler J, Hammond EH, Gray SD (2000) Preliminary report on hormone receptors in the human vocal fold. J Voice 14:72–81PubMedCrossRefGoogle Scholar
  60. Osorio D, Vorobyev M (1996) Colour vision as an adaptation to frugivory in primates. Proc R Soc Lond B 263:593–599CrossRefGoogle Scholar
  61. Osorio D, Vorobyev M (2005) Photoreceptor spectral sensitivities in terrestrial animals: adaptations for luminance and colour vision. Proc R Soc Lond B 272:1745–1752CrossRefGoogle Scholar
  62. Osorio D, Smith AC, Vorobyev M, Buchanan-Smith HM (2004) Detection of fruit and the selection of primate visual pigments for color vision. Am Nat 164:696–708CrossRefGoogle Scholar
  63. Palme R, Möstl E (1994) Biotin–streptavidin enzyme immunoassay for the determination of oestrogens and androgens in boar faeces. In: Görög S (ed) Advances in steroid analysis. Akadémiai Kiadó, Budapest, pp 11–117Google Scholar
  64. Partan SR (2002) Signal and multichannel signal composition: facial expressions and vocalizations of rhesus macaques (Macaca mulatta). Behaviour 139:993–1028CrossRefGoogle Scholar
  65. Partan SR, Marler P (1999) Communication goes multimodal. Science 283:1272–1273PubMedCrossRefGoogle Scholar
  66. Partan SR, Marler P (2005) Issues in the classification of multisensory communication signals. Am Nat 166:231–245PubMedCrossRefGoogle Scholar
  67. Partan SR, Yelda S, Price V, Shimizu T (2005) Female pigeons, Columba livia, respond to multisensory audio-video playbacks of male courtship behaviour. Anim Behav 70:957–966CrossRefGoogle Scholar
  68. Pfefferle D, Fischer J (2006) Sounds and size: identification of acoustic variables that reflect body size in hamadryas baboons, Papio hamadryas. Anim Behav 72:43–51CrossRefGoogle Scholar
  69. Pfefferle D, West PM, Grinnell J, Packer C, Fischer J (2007) Do acoustic features of lion, Panthera leo, roars reflect sex and male condition? J. Acoust Soc Am 121:3947–3953Google Scholar
  70. Pfefferle D, Brauch K, Heistermann M, Hodges JK, Fischer J (2008a) Female Barbary macaque (Macaca sylvanus) copulation calls do not reveal the fertile phase but influence mating outcome. Proc R Soc B 275:571–578PubMedCrossRefGoogle Scholar
  71. Pfefferle D, Heistermann M, Hodges JK, Fischer J (2008b) Male Barbary macaques eavesdrop on mating outcome: a playback study. Anim Behav 75:1885–1891CrossRefGoogle Scholar
  72. Pfefferle D, Heistermann M, Pirow R, Hodges JK, Fischer J (2011) Estrogen and progestogen correlates of the structure of female copulation calls in semi-free-ranging Barbary macaques (Macaca sylvanus). Int J Primatol 32:992–1006PubMedCrossRefGoogle Scholar
  73. Plavcan JM (2001) Sexual dimorphism in primate evolution. Am J Phys Anthropol 116:25–53CrossRefGoogle Scholar
  74. Rawlins RG, Kessler MJ (1986) The Cayo Santiago macaques: history, behavior, and biology. SUNY Press, AlbanyGoogle Scholar
  75. 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
  76. Rhodes L, Argersinger ME, Gantert LT, Friscino BH, Hom G, Pikounis B, Hess DL, Rhodes WL (1997) Effects of administration of testosterone, dihydrotestosterone, oestrogen and fadrozole, and aromatase inhibitor, on sex skin colour in intact male rhesus macaques. J Reprod Fertil 111:51–57PubMedCrossRefGoogle Scholar
  77. Rowe C, Guilford T (1999) Novelty in a multimodal warning signal. Anim Behav 57:341–346PubMedCrossRefGoogle Scholar
  78. Rowe C, Guilford T (2001) The evolution of multimodal warning signals. Evol Ecol 13:655–671CrossRefGoogle Scholar
  79. Rowell TE, Hinde RA (1962) Vocal communication by the rhesus monkey (Macaca mulatta). Proc Zool Soc Lond 138:279–294Google Scholar
  80. Saez S, Sakai F (1976) Androgen receptors in human pharyngo-laryngeal mucosa and pharyngo-laryngeal epithelioma. J Steroid Biochem Mol Biol 7:919–921Google Scholar
  81. Schneider B, Cohen E, Stani J, Kolbus A, Rudas M, Horvat R, van Trotsenburg M (2007) Towards the expression of sex hormone receptors in the human vocal fold. J Voice 21:502–507PubMedCrossRefGoogle Scholar
  82. Schrader L, Hammerschmidt K (1997) Computer-aided analysis of acoustic parameters in animal vocalisations: a multi-parametric approach. Bioacoustics 7:247–265CrossRefGoogle Scholar
  83. Semple S, McComb K (2000) Perception of female reproductive state from vocal cues in a mammal species. Proc R Soc Lond B 267:707–712CrossRefGoogle Scholar
  84. Semple S, McComb K, Alberts SC, Altmann J (2002) Information content of female copulation calls in yellow baboons. Am J Primatol 56:43–56PubMedCrossRefGoogle Scholar
  85. Setchell JM, Dixson AF (2001) Changes in the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status. Horm Behav 39:177–184PubMedCrossRefGoogle Scholar
  86. Setchell JM, Wickings EJ (2005) Dominance, status signals and coloration in male mandrills (Mandrillus sphinx). Ethology 111:25–50CrossRefGoogle Scholar
  87. Setchell JM, Vaglio S, Abbott KM, Moggi-Cecchi J, Boscaro F, Pieraccini G, Knapp LA (2011) Odour signals major histocompatibility complex genotype in an Old World monkey. Proc R Soc Lond B 278:274–280CrossRefGoogle Scholar
  88. Seyfarth RM, Cheney DL, Marler P (1980) Vervey monkey alarm calls: semantic communication in a free-ranging primate. Anim Behav 28:1070–1094CrossRefGoogle Scholar
  89. Siddiqi A, Cronin TW, Loew ER, Vorobyev M, Summers K (2004) Interspecific and intraspecific views of color signals in the strawberry poison frog Dendrobates pumilio. J Exp Biol 207:2471–2485Google Scholar
  90. Slocombe K, Waller B, Liebal K (2011) The language void: the need for multimodality in primate communication research. Anim Behav 81:919–924CrossRefGoogle Scholar
  91. Smith WJ (1977) The behavior of communicating: an ethological approach. Harvard University Press, CambridgeGoogle Scholar
  92. Smith CL, Evans CS (2008) Multimodal signaling in fowl Gallus gallus. J Exp Biol 211:2052–2057PubMedCrossRefGoogle Scholar
  93. Stevens M, Párraga CA, Cuthill IC, Partridge JC, Troscianko T (2007) Using digital photography to study animal coloration. Biol J Linn Soc 90:211–237Google Scholar
  94. Stevens M, Stoddard MC, Higham JP (2009) Studying primate color: towards visual system-dependent methods. Int J Primatol 30:893–917CrossRefGoogle Scholar
  95. Taylor RC, Buchanan BW, Doherty JL (2007) Sexual selection in the squirrel treefrog Hyla squirella: the role of multimodal cue assessment in female choice. Anim Behav 74:1753–1763CrossRefGoogle Scholar
  96. Taylor RC, Klein BA, Stein J, Ryan MJ (2008) Faux frogs: multi-modal signalling and the value of robotics in animal behavior. Anim Behav 76:1089–1097CrossRefGoogle Scholar
  97. Taylor RC, Klein BA, Stein J, Ryan MJ (2011) Multimodal signal variation in space and time: how important is matching a signal with its signaler? J Exp Biol 214:815–820PubMedCrossRefGoogle Scholar
  98. Thompson JT, Bissell AN, Martins EP (2008) Inhibitory interactions between multimodal behavioral responses may influence the evolution of complex signals. Anim Behav 76:113–121CrossRefGoogle Scholar
  99. Tung J, Barreiro LB, Johnson ZP, Hansen KD, Michopoulous V, Toufexis D, Michelini KM, Wilson ME, Gilad Y (2012) Social environment is associated with gene regulatory variation in the rhesus macaque immune system. P Natl Acad Sci U S A 109:6490–6495CrossRefGoogle Scholar
  100. Uetz GW, Roberts JA (2002) Multisensory cues and multimodal communication in spiders: insights from video/audio playback studies. Brain Behav Evol 59:222–230PubMedCrossRefGoogle Scholar
  101. Uetz GW, Roberts JA, Taylor PW (2009) Multimodal communication and mate choice in wolf spiders: female response to multimodal versus unimodal signals. Anim Behav 78:299–305CrossRefGoogle Scholar
  102. Uy JAC, Moyle R, Filardi CR (2009) Plumage color and song differences mediate species recognition between incipient flycatcher species of the Solomon Islands. Evolution 63:153–164PubMedCrossRefGoogle Scholar
  103. van Noordwijk MA, van Schaik CP (2004) Sexual selection and the careers of primate males: paternity concentration, dominance-acquisition tactics and transfer decisions. In: Kappeler P, van Schaik CP (eds) Sexual selection in primates. Cambridge University Press, Cambridge, pp 208–229CrossRefGoogle Scholar
  104. Voelter C, Kleinsasser N, Joa P, Nowak I, Martinez R, Hagen R, Voelker HU (2008) Detection of hormone receptors in the human vocal fold. Eur Arch Otorhinolaryngol 265:1239–1244PubMedCrossRefGoogle Scholar
  105. Vorobyev M, Osorio D (1998) Receptor noise as a determinant of colour thresholds. Proc R Soc Lond B 265:351–358CrossRefGoogle Scholar
  106. Waitt C, Little AC, Wolfensohn S, Honess P, Brown AP, Buchanan-Smith HM, Perrett DI (2003) Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice. Proc R Soc Lond B B270:S144–S146CrossRefGoogle Scholar
  107. Waitt C, Gerald MS, Little AC, Kraiselburd E (2006) Selective attention toward female secondary sexual color in male rhesus macaques. Am J Primatol 68:738–744PubMedCrossRefGoogle Scholar
  108. Widdig A, Bercovitch FB, Streich WJ, Nürnberg P, Krawczak M (2004) A longitudinal analysis of reproductive skew in male rhesus macaques. Proc R Soc Lond B 271:819–826CrossRefGoogle Scholar
  109. Ziegler TE, Epple G, Snowdon CT, Porter TA, Belcher AM, Kuderling I (1993) Detection of the chemical signals of ovulation in the cotton-top tamarin, Saguinus oedipus. Anim Behav 45:313–322CrossRefGoogle Scholar
  110. Zuberbühler K, Noë R, Seyfarth RM (1997) Diana monkey long-distance calls: messages for conspecifics and predators. Anim Behav 53:589–604CrossRefGoogle Scholar
  111. Zuckerman S, Parkes AS (1939) Observations on the secondary sexual characteristics in monkeys. J Endocrinol 1:430–439CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • James P. Higham
    • 1
    • 2
  • Dana Pfefferle
    • 3
    • 4
  • Michael Heistermann
    • 5
  • Dario Maestripieri
    • 1
  • Martin Stevens
    • 6
  1. 1.Institute for Mind and BiologyUniversity of ChicagoChicagoUSA
  2. 2.Department of AnthropologyNew York UniversityNew YorkUSA
  3. 3.Behavioural Ecology Research Group, Institute of BiologyUniversity of LeipzigLeipzigGermany
  4. 4.Junior Research Group of Primate Kin Selection, Department of PrimatologyMax-Planck Institute for Evolutionary AnthropologyLeipzigGermany
  5. 5.Endocrinology LaboratoryGerman Primate CentreGöttingenGermany
  6. 6.Department of ZoologyUniversity of CambridgeCambridgeUK

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