Sexual skin color contains information about the timing of the fertile phase in free-ranging macaca mulatta

International Journal of Primatology

Volumn 30, Issue 6, 2009, Pages 777-789

  Dubuc, Constance ^a,b   Brent, Lauren J N ^c   Accamando, Amanda K ^d   Gerald, Melissa S ^d,e   MacLarnon, Ann ^c   Semple, Stuart ^c   Heistermann, Michael ^b   Engelhardt, Antje ^b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b GERMAN PRIMATE CENTER   (Germany)

^c UNIVERSITY OF ROEHAMPTON   (United Kingdom)

^d UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^e UNIVERSITY OF PUERTO RICO SCHOOL OF MEDICINE   (Puerto Rico)

Author keywords

Color; Fecal steroids; Fertile phase; Macaca mulatta; Sexual skin

Indexed keywords

COLOR; ENDOCRINOLOGY; FERTILITY; METABOLITE; PRIMATE; SEXUAL BEHAVIOR; SIGNALING; SKIN;

CAYO SANTIAGO; PUERTO RICO;

MACACA; MACACA MULATTA; PRIMATES;

EID: 77952745866     PISSN: 01640291     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10764-009-9369-7     Document Type: Article

References (59)

1. Alvarez, F. (1973). Periodic changes in the bare skin areas of Theropithecus gelada. Primates, 14, 195-199.
2. Aujard, F., Heistermann, M., Thierry, B., & Hodges, J. K. (1998). Functional significance of behavioral, morphological, and endocrine correlates across the ovarian cycle in semifree ranging female tonkean macaques. American Journal of Primatology, 46, 285-309.
3. Barelli, C., Heistermann, M., Boesch, C., & Reichard, U. H. (2007). Sexual swellings in wild white-handed gibbon females (Hylobates lar) indicate the probability of ovulation. Hormones and Behavior, 51, 221-230.
4. Baulu, J. (1976). Seasonal sex skin coloration and hormonal fluctuations in free-ranging and captive monkeys. Hormones and Behavior, 7, 481-494.
5. Behboodi, E., Katz, D. F., Samuels, S. J., Tell, L., Hendrickx, A. G., & Lasley, B. L. (1991). The use of a urinary estrone conjugate assay for detection of optimal mating time in the cynomologus macaque (Macaca fascicularis). Journal of Medical Primatology, 20, 229-234.
6. Bergman, T. J., & Beehner, J. C. (2008). A simple method for measuring colour in wild animals: Validation and use on chest patch colour in geladas (Theropithecus gelada). Biological Journal of the Linnean Society, 94, 231-240.
7. Bernstein, I. S. (1963). Social activities related to rhesus monkey consort behavior. Psychological Reports, 13, 375-379.
8. Bosu, W. T. K., Johansson, E. D. B., & Gemzell, C. (1973). Ovarian steroid patterns in peripheral plasma during the menstrual cycle in the rhesus monkey. Folia Primatologica, 19, 218-234.
9. Bradley, B. J., & Mundy, N. I. (2008). The primate palette: The evolution of primate coloration. Evolutionary Anthropology, 17, 97-111.
10. Brauch, K., Pfefferle, D., Hodges, K., Möhle, U., Fischer, J., & Heistermann, M. (2007). Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Hormones and Behavior, 52, 375-383.
11. Carpenter, C. R. (1942). Sexual behavior of free ranging rhesus monkeys (Macaca mulatta). I. Specimens, procedures and behavioral characteristics of estrus. Journal of Comparative Psychology, 33, 113-142.
12. Changizi, M. A., Zhang, Q., & Shimojo, S. (2006). Bare skin, blood and the evolution of primate colour vision. Biology Letters, 2, 217-221.
13. Cleveland, R., Wilkes, S., & Sabotka, G. (1943). Color measurement of the sexual skin of the Macacus rhesus by the Munsell system of color annotation. Endocrinology, 33, 289-296.
14. Czaja, J. A., Robinson, J. A., Eisele, S. G., Scheffler, G., & Goy, R. W. (1977). Relationship between sexual skin colour of female rhesus monkeys and midcycle plasma levels of oestradiol and progesterone. Journal of Reproduction and Fertility, 49, 147-150.
15. Deaner, R. O., Khera, A. V., & Platt, M. L. (2005). Monkeys pay per view: Adaptive valuation of social images by rhesus macaques. Current Biology, 15, 543-548.
16. Deschner, T., Heistermann, M., Hodges, J. K., & Boesch, C. (2003). Timing and probability of ovulation in relation to sex skin swelling in wild West African chimpanzees, Pan troglodytes verus. Animal Behaviour, 66, 551-560.
17. Deschner, T., Heistermann, M., Hodges, K., & Boesch, C. (2004). Female sexual swelling size, timing of ovulation and male behavior in wild West African chimpanzees. Hormones and Behavior, 46, 204-215.
18. Dixson, A. F. (1983). Observations on the evolution and behavioral significance of 'sexual skin' in female primates. Advances in the Study of Behavior, 13, 63-106.
19. Dixson, A. F. (1998). Primate sexuality: Comparative studies of prosimians, monkeys, apes, and human beings. New York: Oxford University Press.
20. Engelhardt, A., Pfeifer, J.-B., Heistermann, M., Niemitz, C., van Hooff, J. A. R. A. M., & Hodges, J. K. (2004). Assessment of female reproductive status by male longtailed macaques, Macaca fascicularus, under natural conditions. Animal Behaviour, 67, 915-924.
21. Engelhardt, A., Hodges, J. K., Niemitz, C., & Heistermann, M. (2005). Female sexual behaviour, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques (Macaca fascicularis). Hormones and Behavior, 47, 195-204.
22. Fernandez, A. A., & Morris, M. R. (2007). Sexual selection and trichromatic color vision in primates: Statistical support for the preexisting-bias hypothesis. The American Naturalist, 170, 10-20.
23. France, J. T. (1981). Overview of the biological aspects of the fertile period. International Journal of Fertility, 26, 143-152.
24. Fujita, S., Mitsunaga, F., Sugiura, H., & Shimizu, K. (2001). Measurement of urinary and fecal steroid metabolites during the ovarian cycle in captive and wild Japanese macaques, Macaca fuscata. American Journal of Primatology, 53, 167-176.
25. Fujita, S., Sugiura, H., Mitsunaga, F., & Shimizu, K. (2004). Hormone profiles and reproductive characteristics in wild female Japanese macaques (Macaca fuscata). American Journal of Primatology, 64, 367-375.
26. Garcia, C., Shimizu, K., & Huffman, M. (2009). Relationship between sexual interactions and the timing of the fertile phase in captive female Japanese macaques (Macaca fuscata). American Journal of Primatology, 71, 1-12.
27. Gauthier, C. A. (1999). Reproductive parameters and paracallosal skin color changes in captive female Guinea baboons, Papio papio. American Journal of Primatology, 47, 67-74.
28. Gerald, M. S., Waitt, C., & Little, A. C. (2009). Pregnancy coloration in macaques may act as a warning signal to reduce antagonism by conspecifics. Behavioural Processes, 80, 7-11.
29. Gesquiere, L. R., Wango, E. O., Alberts, S. C., & Altmann, J. (2007). Mechanisms of sexual selection: Sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons. Hormones and Behavior, 51, 114-125.
30. Goldstein, S. J., & Richard, A. F. (1989). Ecology of rhesus macaques (Macaca mulatta) in northwest Pakistan. International Journal of Primatology, 10, 531-567.
31. Heistermann, M., Tari, S., & Hodges, J. K. (1993). Measurement of faecal steroids for monitoring ovarian function in New World primates, Callitrichidae. Journal of Reproduction and Fertility, 99, 243-251.
32. Heistermann, M., Finke, M., & Hodges, J. K. (1995). Assessment of female reproductive status in captive-housed Hanuman langurs (Presbytis entellus) by measurement of urinary and fecal steroid excretion patterns. American Journal of Primatology, 37, 275-284.
33. Heistermann, M., Uhrigshardt, J., Husung, A., Kaumanns, A., & Hodges, J. K. (2001). Measurement of faecal steroid metabolites in the lion-tailed macaque (Macaca silenus): A non-invasive tool for assessing female ovarian function. Primate Report, 59, 27-42.
34. Higham, J. P. (2006). The reproductive ecology of female olive baboons (Papio hamadryas anubis) at Gashaka-Gumti National Park, Nigeria. PhD Thesis. Roehampton University.
35. Higham, J. P., MacLarnon, A. M., Ross, C., Heistermann, M., & Semple, S. (2008). Baboon sexual swellings: Information content of size and color. Hormones and Behavior, 53, 452-462.
36. Higham, J. P., Semple, S., MacLarnon, A., Heistermann, M., & Ross, C. (2009). Female reproductive signaling, and male mating behavior, in the olive baboon. Hormones and Behavior, 55, 60-67.
37. Jeffcoate, S. L. (1983). Use of rapid hormone assays in the prediction of ovulation. In S. L. Jeffcoate (Ed.), Ovulation: Methods for its prediction and detection (pp. 67-82). Chichester: John Wiley.
38. Lindburg, D. G. (1977). Feeding behaviour and diet of rhesus monkeys (Macaca mulatta) in a Siwalik forest in north India. In T. H. Clutton-Brock (Ed.), Primate ecology: Studies of feeding and ranging behaviours in lemurs, monkeys and apes (pp. 223-249). New York: Academic Press.
39. Matthews, L. H. (1956). The sexual skin of gelada baboons (Theropithecus gelada). Transactions of the Zoological Society of London, 28, 543-552.
40. Maynard-Smith, J., & Harper, D. (2005). Introduction: What are signals? In J. Maynard-Smith & D. Harper (Eds.), Animal signals (pp. 1-15). Oxford: Oxford University Press.
41. Möhle, U., Heistermann, M., Dittami, J., Reinberg, V., Wallner, B., & Hodges, J. K. (2005). Patterns of anogenital swelling size and their endocrine correlates during ovulatory cycles and early pregnancy in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. American Journal of Primatology, 66, 351-368.
42. Napier, J. R., & Napier, P. H. (1967). A handbook of living primates. London: Academic Press.
43. Nunn, C. (1999). The evolution of exaggerated sexual swellings in primates and the graded signal hypothesis. Animal Behaviour, 58, 229-246.
44. Rhodes, L., Argersinger, M. E., Gantert, L. T., Friscino, B. H., Hom, G., Pikounis, B., et al. (1997). Effects of administration of testosterone, dihydrotestosterone, oestrogen and fadrozole, and aromatase inhibitor, on sex skin colour in intact male rhesus macaques. Journal of Reproduction and Fertility, 111, 51-57.
45. Setchell, J. M., & Wickings, E. J. (2004). Sexual swellings in mandrills (Mandrillus sphinx): A test of the reliable indicator hypothesis. Behavioral Ecology, 15, 438-445.
46. Setchell, J., Wickings, E. J., & Knapp, L. A. (2006). Signal content of red facial coloration in female mandrills (Mandrillus sphinx). Proceedings of the Royal Society B: Biological Sciences, 273, 2395-2400.
47. Seth, P. K., Chopra, P. K., & Seth, S. (2001). Indian rhesus macaque: Habitat, ecology and activity patterns of naturally occurring populations. Envis Bulletin: Wildlife and Protected Areas, 1, 68-80.
48. Shideler, S. E., Orturo, A. M., Moran, F. M., Moorman, E. A., & Lasley, B. L. (1993). Simple extraction and enzyme immunoassays for estrogen and progesterone metabolites in the feces of Macaca fascicularis during non-conceptive and conceptive ovarian cycles. Biology of Reproduction, 48, 1290-1298.
49. Sillén-Tullberg, B., & Møller, A. P. (1993). The relationship between concealed ovulation and mating systems in anthropoid primates: A phylogenetic analysis. The American Naturalist, 141, 1-25.
50. Snowdon, C. T. (2004). Sexual selection and communication. In P. M. Kappeler & C. P. van Schaik (Eds.), Sexual selection in primates: New and comparative perspectives (pp. 57-70). Cambridge, UK: Cambridge University Press.
51. Stevens, M., Parrage, C. A., Cuthill, I. C., Partridge, J. C., & Troscianko, T. S. (2007). Using digital photography to study animal coloration. Biological Journal of the Linnean Society, 90, 211-237.
52. Strum, S. C., & Western, J. D. (1982). Variations in fecundity with age and environment in olive baboons (Papio anubis). American Journal of Primatology, 3, 61-76.
53. Surridge, A. K., Osorio, D., & Mundy, N. I. (2003). Evolution and selection of trichromatic vision in primates. Trends in Ecology and Evolution, 18, 198-205.
54. Thomson, J. A., Hess, D. L., Dahl, K. D., Iliff-Sizemore, S. A., Stouffer, R. L., & Wolf, D. P. (1992). The Sulawesi crested black macaque (Macaca nigra) menstrual cycle: Changes in perineal tumescence and serum estradiol, progesterone, follicle-stimulating hormone, and luteinizing hormone levels. Biology of Reproduction, 46, 879-884.
55. Waitt, C., & Buchanan-Smith, H. M. (2006). Perceptual considerations in the use of colored photographic and video stimuli to study nonhuman primate behavior. American Journal of Primatology, 68, 1054-1067.
56. Waitt, C., Gerald, M. S., Little, A. C., & Krebs, J. R. (2006). Selective attention toward female secondary sexual color in male rhesus macaques. American Journal of Primatology, 68, 738-744.
57. Wilcox, A. J., Weinberg, C. R., & Baird, D. D. (1995). Timing of sexual intercourse in relation to ovulation. New England Journal of Medicine, 333, 1517-1522.
58. Zinner, D. P., van Schaik, C. P., Nunn, C. L., & Kappeler, P. M. (2004). Sexual selection and exaggerated sexual swellings of female primates. In P. M. Kappeler & C. P. van Schaik (Eds.), Sexual selection in primates: New and comparative perspectives (pp. 71-89). Cambridge, UK: Cambridge University Press.
59. Zuckerman, S., van Wagenen, G., & Gardner, R. H. (1938). The sexual skin of the rhesus monkey. Proceedings of the Zoological Society of London, 108, 385-401.