Signaling in multiple modalities in male rhesus macaques: sex skin coloration and barks in relation to androgen levels, social status, and mating behavior
- 870 Downloads
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.
KeywordsColoration 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.
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.
- Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
- 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
- Dixson AF (2012) Primate sexuality: comparative studies of prosimians, monkeys, apes, and human beings (2nd edn). Oxford University Press, OxfordGoogle Scholar
- Endler JA, Mielke PW (2005) Comparing entire colour patterns as birds see them. Biol J Linn Soc 86:405–431Google Scholar
- Fant G (1960) Acoustic theory of speech production. Mouton & Co, The HagueGoogle Scholar
- 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
- Hammerschmidt K (1990) Individuelle Lautmuster bei Berberaffen (Macaca sylvanus): Ein Ansatz zum Verständnis ihrer vokalen Kommunikation. Diss Freie Universtät, BerlinGoogle Scholar
- 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
- 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
- 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
- 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
- Rawlins RG, Kessler MJ (1986) The Cayo Santiago macaques: history, behavior, and biology. SUNY Press, AlbanyGoogle Scholar
- 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
- Rowell TE, Hinde RA (1962) Vocal communication by the rhesus monkey (Macaca mulatta). Proc Zool Soc Lond 138:279–294Google Scholar
- 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
- 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
- Smith WJ (1977) The behavior of communicating: an ethological approach. Harvard University Press, CambridgeGoogle Scholar
- 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
- 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