Individual facial coloration in male Eulemur fulvus rufus: A condition-dependent ornament?

International Journal of Primatology

Volumn 30, Issue 6, 2009, Pages 859-875

  Clough, Dagmar ^a,b   Heistermann, Michael ^a   Kappeler, Peter M ^a,b  

^a GERMAN PRIMATE CENTER   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Androgen; Coloration; Condition dependent trait; Eulemur fulvus rufus; Facial hair

Indexed keywords

ANDROGEN; COLOR; CONDITION FACTOR; DIGITAL IMAGE; FECES; HAIR; MALE BEHAVIOR; ORNAMENTATION; PRIMATE; REPRODUCTIVE SUCCESS; SIGNALING; SKIN;

KIRINDY FOREST; MADAGASCAR; TOLIARA;

EULEMUR FULVUS RUFUS; LEMUR; LEMURIDAE; PRIMATES; STREPSIRHINI;

EID: 77952742857     PISSN: 01640291     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10764-009-9379-5     Document Type: Article

References (72)

1. Andersson, M. (1994). Sexual selection. Princeton, NJ: Princeton University Press.
2. Asa, C. S., Porton, I. J., & Junge, R. (2007). Reproductive cycles and contraception of black lemurs (Eulemur macaco macaco) with depot medroxyprogesterone acetate during the breeding season. Zoo Biology, 26, 289-298.
3. Barthold, J., Fichtel, C., & Kappeler, P. M. (2008). What is it going to be? Pattern and potential function of natal coat change in sexually dichromatic redfronted lemurs (Eulemur fulvus rufus). American Journal of Physical Anthropology, 138, 1-10.
4. 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.
5. Bradley, B. J., Irwin, M., Kappeler, P. M., Moisson, P., & Morelli, T. L. (2008). & Pastorini, J. The proximate is key to the ultimate: Identifying the genetic bases of primate pigmentation. In Congress of the International Primatological Society XXII.
6. Bradley, B. J., & Mundy, N. I. (2008). The primate palette: The evolution of primate coloration. Evolutionary Anthropology, 17, 97-111.
7. Brown, C., & Mosteller, F. (1991). Components of variance. In D. C. Hoaglin, F. Mosteller & J. W. Tukey (Eds.), Fundamentals of explanatory analysis of variance (pp. 193-251). New York: John Wiley & Sons.
8. Buchholz, R. (1995). Female choice, parasite load and male ornamentation in wild turkeys. Animal Behaviour, 50, 929-943.
9. Castanet, J., & Ortonne, J.-P. (1996). Hair melanin and hair color. In P. Jollès, H. Zahn & H. Höcker (Eds.), Formation and structure of human hair: Biology and structure (pp. 209-226). Basel: Birkhäuser.
10. Cooper, V. J., & Hosey, G. R. (2003). Sexual dichromatism and female preference in Eulemur fulvus subspecies. International Journal of Primatology, 24, 1177-1188.
11. Cotton, S., Fowler, K., & Pomiankowski, A. (2004). Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis? Proceedings of the Royal Society B: Biological Sciences, 271, 771-783.
12. Dale, J. (2000). Ornamental plumage does not signal male quality in red-billed queleas. Proceedings of the Royal Society B: Biological Sciences, 267, 2143-2149.
13. Dale, J., Lank, D. B., & Reeve, H. K. (2001). Signaling individual identity versus quality: A model and case studies with ruffs, queleas, and house finches. American Naturalist, 158, 75-86.
14. Dixson, A. (1998). Primate sexuality. Oxford: Oxford University Press.
15. Endler, J. A. (1993). The color of light in forests and its implications. Ecological Monographs, 63, 1-27.
16. Folstad, I., & Karter, A. J. (1992). Parasites, bright males, and the immunocompetence handicap. American Naturalist, 139, 603-622.
17. Gerald, M. S. (2001). Primate colour predicts social status and aggressive outcome. Animal Behaviour, 61, 559-566.
18. Gerald, M. S. (2003). How color may guide the primate world: Possible relationships between sexual selection and sexual dichromatism. In C. B. Jones (Ed.), Sexual selection and reproductive competition in primates: New perspectives and directions (pp. 141-171). Norman: The American Society of Primatologists.
19. Gerald, M. S., Bernstein, J., Hinkson, R., & Fosbury, R. A. E. (2001). Formal method for objective assessment of primate colour. American Journal of Primatology, 53, 79-85.
20. Gerald, M. S., Waitt, C., Little, A. C., & Kraiselburd, E. (2007). Females pay attention to female secondary sexual color: An experimental study in Macaca mulatta. International Journal of Primatology, 28, 1-7.
21. Hamilton, W. D., & Zuk, M. (1982). Heritable true fitness and bright birds: A role for parasites? Science, 218, 384-387.
22. Hauser, M. (1996). The evolution of communication. Cambridge, MA: Bradford/MIT Press.
23. Hausfater, G., Gerhardt, H. C., & Klump, G. M. (1990). Parasites and mate choice in gray treefrogs, Hyla versicolor. American Naturalist, 30, 299-311.
24. Hearing, V. J. (1999). Biochemical control of melanogenesis and melanosomal organization. Journal of Investigative Dermatology Symposium Proceedings, 4, 24-28.
25. 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.
26. Hill, G. E. (1991). Plumage coloration is a sexually selected indicator of male quality. Nature, 350, 337-339.
27. Izard, K., Epps, B., & Simons, E. (1995). Reproduction in the brown lemur (Eulemur fulvus fulvus). American Journal of Primatology, 36, 129.
28. Jacobs, G. H. (1993). The distribution and nature of colour vision among the mammals. Biological Reviews of the Cambridge Philosophical Society, 68, 413-471.
29. Jacobs, G. H. (1999). Prospects for trichromatic color vision in male Cebus monkeys. Behavioural Brain Research, 101, 109-112.
30. Kappeler, P. M., & Port, M. (2008). Mutual tolerance or reproductive competition? Patterns of reproductive skew among male redfronted lemurs (Eulemur fulvus rufus). Behavioral Ecology and Sociobiology, 62, 1477-1488.
31. Kraus, C., Heistermann, M., & Kappeler, P. M. (1999). Physiological suppression of sexual function of subordinate males: A subtle form of intrasexual competition among male sifakas (Propithecus verreauxi)? Physiology & Behavior, 66, 855-861.
32. Loy, J. (1974). Changes in facial color associated with pregnancy in patas monkeys. Folia Primatolologica, 22, 251-257.
33. Maynard-Smith, J., & Harper, D. (2003). Animal signals. Oxford: Oxford University Press.
34. Milinski, M., & Bakker, T. C. M. (1990). Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature, 344, 330-333.
35. Mittermeier, R. A., Konstant, W. R., Hawkins, F., Louis, E. E., Langrand, O., Ratsimbazafy, J., et al. (2006). Lemurs of Madagascar. Washington, DC: Conservation International.
36. Ostner, J., & Kappeler, P. M. (1999). Central males instead of multiple pairs in redfronted lemurs, Eulemur fulvus rufus (Primates, Lemuridae)? Animal Behaviour, 58, 1069-1078.
37. Ostner, J., Kappeler, P. M., & Heistermann, M. (2002). Seasonal variation and social correlates of androgen excretion in male redfronted lemurs (Eulemur fulvus rufus). Behavioral Ecology and Sociobiology, 52, 485-495.
38. Ostner, J., Kappeler, P. M., & Heistermann, M. (2008). Androgen and glucocorticoid levels reflect seasonally occurring social challenges in male redfronted lemurs (Eulemur fulvus rufus). Behavioural Ecology and Sociobiology, 62, 627-638.
39. Palmer, A. E., London, W. T., Brown, R. L., & Rice, J. M. (1981). Color changes in the haircoat of patas monkeys (Erythrocebus patas). American Journal of Primatology, 1, 371-378.
40. Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & Team, R-Core. (2008). nlme: Linear and Nonlinear Mixed Effects Models. R-package version, 3, 1-89.
41. R Development Core Team. (2008). R: A language and environment for statistical computing, R Foundation for Statistical Computing. Vienna, Austria, http://www. R-project. org.
42. Randall, V. A. (2000). Androgens: The main regulator of human hair growth. In F. M. Camacho, V. A. Randall & V. H. Price (Eds.), Hair and its disorders. Biology, pathology and management (pp. 69-82). London: Martin Dunitz.
43. Randall, V. A. (2008). Androgens and hair growth. Dermatologic Therapy, 21, 314-328.
44. Ressel, S., & Schall, J. J. (1989). Parasites and showy males: malarial infection and color variation in fence lizards. Oecologica, 78, 158-164.
45. 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, an aromatase inhibitor, on sex skin colour in intact male rhesus macaques. Journal of Reproduction and Fertility, 111, 51-57.
46. Rohwer, S., & Ewald, P. W. (1981). The cost of dominance and advantage of subordination in a badge signaling system. Evolution, 35, 441-454.
47. Roulin, A., Almasi, B., Rossi-Pedruzzi, A., Ducrest, A.-L., Wakamatsu, K., Miksik, I., et al. (2008). Corticosterone mediates the condition-dependent component of melanin-based coloration. Animal Behaviour, 75, 1351-1358.
48. Setchell, J., & Dixson, A. (2001a). Changes in the secondary sexual adornments of male mandrills (Mandrillus sphinx) are associated with gain and loss of alpha status. Hormones and Behavior, 39, 177-184.
49. Setchell, J. M. (2005). Do female mandrills prefer brightly colored males? International Journal of Primatology, 26, 715-735.
50. Setchell, J. M., & Dixson, A. F. (2001b). Circannual changes in the secondary sexual adornments of semifree-ranging male and female mandrills (Mandrillus sphinx). American Journal of Primatology, 53, 109-121.
51. Setchell, J. M., & Kappeler, P. M. (2003). Selection in relation to sex in primates. Advances in the Study of Behaviour, 33, 87-174.
52. Setchell, J. M., Smith, T., Wickings, E. J., & Knapp, L. A. (2008). Social correlates of testosterone and ornamentation in male mandrills. Hormones and Behavior, 54, 365-372.
53. Setchell, J. M., & Wickings, E. (2005). Dominance, status signals and coloration in male mandrills (Mandrillus sphinx). Ethology, 111, 25-50.
54. Setchell, J. M., Wickings, E. J., & Knapp, L. A. (2006). Signal content of red facial colouration in female mandrills (Mandrillus sphinx). Proceedings of the Royal Society B: Biological Sciences, 273, 2395-2400.
55. Slominski, A., & Paus, R. (1993). Melanogenesis is coupled to murine anagen: toward new concepts for the role of melanocytes and the regulation of melanogenesis in hair growth. Journal of Investigative Dermatology, 101, 90S-97S.
56. Slominski, A., Tobin, D. J., Shibahara, S., & Wortsman, J. (2004a). Melanin pigmentation in mammalian skin and its hormonal regulation. Physiological Reviews, 84, 1155-1228.
57. Slominski, A., Wortsman, J., Plonka, P. M., Schallreuter, K. U., Paus, R., & Tobin, D. J. (2004b). Hair follicle pigmentation. Journal of Investigative Dermatology, 124, 13-21.
58. Stevens, M., Párraga, 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.
59. Sumner, P., & Mollon, J. D. (2003). Colors of primate pelage and skin: Objective assessment of conspicuousness. American Journal of Primatology, 59, 67-91.
60. Surridge, A. K., Osorio, D., & Mundy, N. I. (2003). Evolution and selection of trichromatic vision in primates. Trends in Ecology & Evolution, 18, 198-205.
61. Tan, Y., & Li, W.-H. (1999). Trichromatic vision in prosimians. Nature, 402, 36.
62. Vandenbergh, J. G. (1965). Hormonal basis of sex skin in male rhesus monkeys. General and Comparative Endocrinology, 5, 31-34.
63. Veiga, J. P., & Puerta, M. (1996). Nutritional constraints determine the expression of a sexual trait in the house sparrow, Passer domesticus. Proceedings of the Royal Society B: Biological Sciences, 263, 229-234.
64. von Engelhardt, N., Kappeler, P. M., & Heistermann, M. (2000). Androgen levels and female social dominance in Lemur catta. Proceedings of the Royal Society B: Biological Sciences, 267, 1533-1539.
65. Waitt, C., Little, A. C., Wolfensohn, S., Honess, P., Brown, A. P., Buchanan-Smith, H. M., et al. (2003). Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice. Proceedings of the Royal Society B: Biological Sciences (Supplement), 270, S144-S146.
66. Wedekind, C. (1992). Detailed information about parasites revealed by sexual ornamentation. Proceedings of the Royal Society B: Biological Sciences, 247, 169-174.
67. West, P. M., & Packer, C. (2002). Sexual Selection, temperature, and the lion's mane. Science, 297, 1339-1343.
68. Wickings, E. J., & Dixson, A. F. (1992). Testicular function, secondary sexual development, and social status in male mandrills. Physiology & Behavior, 52, 909-916.
69. Wimmer, B., & Kappeler, P. M. (2002). The effects of sexual selection and life history on the genetic structure of redfronted lemur, Eulemur fulvus rufus, groups. Animal Behaviour, 64, 557-568.
70. Zahavi, A. (1975). Mate selection-a selection for a handicap. Journal of Theoretical Biology, 53, 205-214.
71. Ziegler, T., Hodges, K., Winkler, P., & Heistermann, M. (2000). Hormonal correlates of reproductive seasonality in wild female Hanuman langurs (Presbytis entellus). American Journal of Primatology, 51, 119-134.
72. Zuk, M., & Decruyenaere, J. (1994). Measuring individual variation in colour: A comparison of two techniques. Biological Journal of the Linnean Society, 53, 165-173.