Primates

, Volume 58, Issue 1, pp 83–91 | Cite as

Testing for links between face color and age, dominance status, parity, weight, and intestinal nematode infection in a sample of female Japanese macaques

  • Lucie Rigaill
  • Andrew J. J. MacIntosh
  • James P. Higham
  • Sandra Winters
  • Keiko Shimizu
  • Keiko Mouri
  • Takafumi Suzumura
  • Takeshi Furuichi
  • Cécile Garcia
Original Article

Abstract

Studies of the role of secondary sexual ornaments in mate choice tend to focus on colorful traits in males, but females of many animal species express colorful ornamentation too. Among non-human primates, investigations into the role of female secondary sexual traits as indicators of life history characteristics, reproductive success, and health status have mostly focused on sexual swellings, whereas only few studies have been conducted on the role of facial color. Recent studies on rhesus macaques and mandrills suggested that female ornamentation might provide information about female life history characteristics, but not on disease resistance factors and parasite infection, which have been shown to affect male ornamentation in some non-primate species. In Japanese macaques (Macaca fuscata), females have brightly colored faces that are indicative of their reproductive status. Here, we aimed to determine whether female facial color might also convey information about age, dominance rank, parity, weight, and intestinal nematode infection in free-ranging individuals. We analyzed whether female facial parameters (luminance and redness) were linked to these individual characteristics, using digital photography and data on intestinal parasite infection collected systematically during 1 month for each of seven free-ranging females. We found no evidence to suggest that female facial color is an indicator of any of these measures in Japanese macaques. Considering our small data set, it is still preliminary to draft any clear conclusions. Future studies combining digital, hormonal, parasitological and behavioral data are needed to assess the possible role of female face color on male preferences and mating choice in Japanese macaques.

Keywords

Sexual selection Secondary sexual ornaments Signaling Macaca fuscata 

Notes

Acknowledgments

We thank the Cooperative Research Program of Kyoto University’s Wildlife Research Center for research permits and use of the Koshima field station. Thanks also to Akiko Takahashi and Julie Duboscq for their help in the field, and to Louise Ducroix for her help with the preparation of images and samples. We thank Prof. Fred Bercovitch for comments on the manuscript. The comments of Dr Joanna Setchell and an anonymous reviewer also greatly improved an earlier draft of this paper. The research protocol was reviewed and approved by the Wildlife Research Center of Kyoto University and was in agreement with the Guidelines for the Care and Use of Nonhuman Primates of the Kyoto University Primate Research Institute. Financial support was provided by the Centre National de la Recherche Scientifique (France), Projet International de Coopération Scientifique n°06274 (to C. Garcia) and the Japan Society for the Promotion of Science (to A. J. J. MacIntosh).

References

  1. Amundsen T (2000) Why are female birds ornamented? Trends Ecol Evol 15:149–155. doi: 10.1016/S0169-5347(99)01800-5 CrossRefPubMedGoogle Scholar
  2. Amundsen T, Forsgren E (2001) Male mate choice selects for female coloration in a fish. Proc Natl Acad Sci 98:13155–13160. doi: 10.1073/pnas.211439298 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Andersson MB (1994) Sexual selection. Princeton University PressGoogle Scholar
  4. Arizono N, Yamada M, Tegoshi T, Onishi K (2012) Molecular identification of Oesophagostomum and Trichuris eggs isolated from wild Japanese macaques. Korean J Parasitol 50:253–257. doi: 10.3347/kjp.2012.50.3.253 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw. doi: 10.18637/jss.v067.i01 Google Scholar
  6. Behboodi E, Katz DF, Samuels SJ, Tell L, Hendrickx AG, Lasley BL (1991) The use of a urinary estrone conjugates assay for detection of optimal mating time in the cynomolgus macaque (Macaca fascicularis). J Med Primatol 20:229–234PubMedGoogle Scholar
  7. Bercovitch FB (1996) Testicular function and scrotal coloration in patas monkeys. J Zool 239:93–100. doi: 10.1111/j.1469-7998.1996.tb05439.x CrossRefGoogle Scholar
  8. Bergman TJ, Ho L, Beehner JC (2009) Chest color and social status in male geladas (Theropithecus gelada). Int J Primatol 30:791–806. doi: 10.1007/s10764-009-9374-x CrossRefGoogle Scholar
  9. Brauch K, Pfefferle D, Hodges K et al (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. Horm Behav 52:375–383. doi: 10.1016/j.yhbeh.2007.06.001 CrossRefPubMedGoogle Scholar
  10. Burnham KP, Anderson DR (eds) (2004) Model selection and multimodel inference. Springer, New YorkGoogle Scholar
  11. Clutton-Brock TH (2004) What is sexual selection? In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 24–36Google Scholar
  12. Danzy Cramer J, Gaetano T, Gray JP et al (2013) Variation in scrotal color among widely distributed vervet monkey populations (Chlorocebus aethiops pygerythrus and Chlorocebus aethiops sabaeus). Am J Primatol 75:752–762. doi: 10.1002/ajp.22156 CrossRefGoogle Scholar
  13. Darwin C (1871) The descent of man, and selection in relation to sex. Murray, LondonCrossRefGoogle Scholar
  14. David P, Heeb P (2009) Parasites and sexual selection. In: Thomas F, Guégan JF, Renaud F (eds) Ecology and evolution of parasitism. Oxford University Press, Oxford, pp 31–47Google Scholar
  15. de Vries H, Stevens JMG, Vervaecke H (2006) Measuring and testing the steepness of dominance hierarchies. Anim Behav 71:585–592. doi: 10.1016/j.anbehav.2005.05.015 CrossRefGoogle 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 46:204–215. doi: 10.1016/j.yhbeh.2004.03.013 CrossRefPubMedGoogle Scholar
  17. Doutrelant C, Grégoire A, Grnac N et al (2008) Female coloration indicates female reproductive capacity in blue tits. J Evol Biol 21:226–233. doi: 10.1111/j.1420-9101.2007.01451.x PubMedGoogle Scholar
  18. Dubuc C, Allen WL, Maestripieri D, Higham JP (2014a) Is male rhesus macaque red color ornamentation attractive to females? Behav Ecol Sociobiol 68:1215–1224CrossRefPubMedPubMedCentralGoogle Scholar
  19. Dubuc C, Winters S, Allen WL et al (2014b) Sexually selected skin colour is heritable and related to fecundity in a non-human primate. Proc R Soc Lond B Biol Sci 281:20141602. doi: 10.1098/rspb.2014.1602 CrossRefGoogle Scholar
  20. Dubuc C, Allen WL, Cascio J, et al (2015) Who cares? Experimental attention biases provide new insights into a mammalian sexual signal. Behav Ecol arv117. doi:  10.1093/beheco/arv117
  21. Emery MA, Whitten PL (2003) Size of sexual swellings reflects ovarian function in chimpanzees (Pan troglodytes). Behav Ecol Sociobiol 54:340–351. doi: 10.1007/s00265-003-0648-6 CrossRefGoogle Scholar
  22. Engelhardt A, Pfeifer J-B, Heistermann M et al (2004) Assessment of female reproductive status by male longtailed macaques, Macaca fascicularis, under natural conditions. Anim Behav 67:915–924. doi: 10.1016/j.anbehav.2003.09.006 CrossRefGoogle Scholar
  23. Fooden J, Aimi M (2003) Birth-season variation in Japanese macaques, Macaca fuscata. Primates 44:109–117. doi: 10.1007/s10329-002-0011-y PubMedGoogle Scholar
  24. Fooden J, Aimi M (2005) Systematic review of Japanese macaques, Macaca fuscata (Gray, 1870). Fieldiana Zool 104:1–198Google Scholar
  25. Fujita S (2010) Interaction between male and female mating strategies and factors affecting reproductive outcome. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Springer, Tokyo, pp 221–239CrossRefGoogle Scholar
  26. 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. Am J Primatol 53:167–176. doi: 10.1002/ajp.3 CrossRefPubMedGoogle Scholar
  27. Fujita S, Sugiura H, Shimizu K, Mitsunaga F (2004) Hormone profiles and reproductive characteristics in wild female Japanese macaques (Macaca fuscata). Am J Primatol 64:367–375. doi: 10.1002/ajp.20086 CrossRefPubMedGoogle Scholar
  28. Furuichi T (1985) Inter-male associations in a wild Japanese macaque troop on Yakushima Island, Japan. Primates 26:219–237. doi: 10.1007/BF02382399 CrossRefGoogle Scholar
  29. 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). Am J Primatol 71:868–879. doi: 10.1002/ajp.20717 CrossRefPubMedGoogle Scholar
  30. Ghai RR, Fugère V, Chapman CA et al (2015) Sickness behaviour associated with non-lethal infections in wild primates. Proc R Soc B 282:20151436. doi: 10.1098/rspb.2015.1436 CrossRefPubMedCentralGoogle Scholar
  31. Gillespie TR (2006) Noninvasive assessment of gastrointestinal parasite infections in free-ranging primates. Int J Primatol 27:1129–1143. doi: 10.1007/s10764-006-9064-x CrossRefGoogle Scholar
  32. Go M (2009) Seasonal changes in food resource distribution and feeding sites selected by Japanese macaques on Koshima Islet, Japan. Primates 51:149–158. doi: 10.1007/s10329-009-0179-5 CrossRefPubMedGoogle Scholar
  33. Gotoh S (2000) Regional differences in the infection of wild Japanese macaques by gastrointestinal helminth parasites. Primates 41:291–298. doi: 10.1007/BF02557598 CrossRefGoogle Scholar
  34. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387CrossRefPubMedGoogle Scholar
  35. Heistermann M, Brauch K, Möhle U et al (2007) Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Am J Primatol 70:44–53. doi: 10.1002/ajp.20455 CrossRefGoogle Scholar
  36. Higham JP (2013) How does honest costly signaling work? Behav Ecol art097. doi:  10.1093/beheco/art097
  37. Higham JP, MacLarnon AM, Ross C et al (2008) Baboon sexual swellings: information content of size and color. Horm Behav 53:452–462. doi: 10.1016/j.yhbeh.2007.11.019 CrossRefPubMedGoogle Scholar
  38. Higham JP, Brent LJN, Dubuc C et al (2010) Color signal information content and the eye of the beholder: a case study in the rhesus macaque. Behav Ecol 21:739–746. doi: 10.1093/beheco/arq047 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Higham JP, Pfefferle D, Heistermann M et al (2013) Signaling in multiple modalities in male rhesus macaques: sex skin coloration and barks in relation to androgen levels, social status, and mating behavior. Behav Ecol Sociobiol 67:1457–1469. doi: 10.1007/s00265-013-1521-x CrossRefPubMedPubMedCentralGoogle Scholar
  40. Horii Y, Imada I, Yanagida T et al (1982) Parasite changes and their influence on the body weight of Japanese monkeys (Macaca fuscata fuscata) of the Koshima troop. Primates 23:416–431. doi: 10.1007/BF02381324 CrossRefGoogle Scholar
  41. Huchard E, Benavides JA, Setchell JM et al (2009) Studying shape in sexual signals: the case of primate sexual swellings. Behav Ecol Sociobiol 63:1231–1242. doi: 10.1007/s00265-009-0748-z CrossRefGoogle Scholar
  42. Huffman MA (1991) Mate selection and partner preferences in female Japanese macaques. Monkeys Arashiyama Thirty-Five Years Res Jpn West 101–122Google Scholar
  43. Huffman MA (1992) Influences of female partner preference on potential reproductive outcome in Japanese macaques. Folia Primatol 59:77–88CrossRefPubMedGoogle Scholar
  44. Isbell LA (1995) Seasonal and social correlates of changes in hair, skin, and scrotal condition in vervet monkeys (Cercopithecus aethiops) of Amboseli National Park, Kenya. Am J Primatol 36:61–70. doi: 10.1002/ajp.1350360105 CrossRefGoogle Scholar
  45. Iwamoto T (1982) Food and nutritional condition of free ranging Japanese monkeys on Koshima Islet during winter. Primates 23:153–170. doi: 10.1007/BF02381158 CrossRefGoogle Scholar
  46. Krief S, Jamart A, Mahé S et al (2008) Clinical and pathologic manifestation of oesophagostomosis in African great apes: does self-medication in wild apes influence disease progression? J Med Primatol 37:188–195. doi: 10.1111/j.1600-0684.2008.00285.x CrossRefPubMedGoogle Scholar
  47. Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292–305. doi: 10.2307/2407393 CrossRefGoogle Scholar
  48. MacIntosh AJJ, Huffman MA (2010) Toward understanding the tole of diet in host–parasite interactions: the case for Japanese macaques. In: Nakagawa N, Nakamichi M, Sugiura H (eds) The Japanese macaques. Springer, Tokyo, pp 323–344CrossRefGoogle Scholar
  49. MacIntosh AJJ, Hernandez AD, Huffman MA (2010) Host age, sex, and reproductive seasonality affect nematode parasitism in wild Japanese macaques. Primates 51:353–364. doi: 10.1007/s10329-010-0211-9 CrossRefPubMedGoogle Scholar
  50. MacIntosh AJJ, Alados CL, Huffman MA (2011) Fractal analysis of behaviour in a wild primate: behavioural complexity in health and disease. J R Soc Interface 8:1497–1509. doi: 10.1098/rsif.2011.0049 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Marty JS, Higham JP, Gadsby EL, Ross C (2009) Dominance, coloration, and social and sexual behavior in male drills Mandrillus leucophaeus. Int J Primatol 30:807–823. doi: 10.1007/s10764-009-9382-x CrossRefGoogle Scholar
  52. Møller AP, Christe P, Lux E (1999) Parasitism, host immune function, and sexual selection. Q Rev Biol 74:3–20CrossRefPubMedGoogle Scholar
  53. Mori A (1979) Analysis of population changes by measurement of body weight in the Koshima troop of Japanese monkeys. Primates 20:371–397. doi: 10.1007/BF02373390 CrossRefGoogle Scholar
  54. Muller MN, Emery Thompson M, Wrangham RW (2006) Male chimpanzees prefer mating with old females. Curr. Biol 16:2234–2238CrossRefPubMedGoogle Scholar
  55. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. doi: 10.1111/j.2041-210x.2012.00261.x CrossRefGoogle Scholar
  56. Neumann C, Duboscq J, Dubuc C et al (2011) Assessing dominance hierarchies: validation and advantages of progressive evaluation with Elo-rating. Anim Behav 82:911–921. doi: 10.1016/j.anbehav.2011.07.016 CrossRefGoogle Scholar
  57. Rigaill L, MacIntosh AJJ, Higham JP et al (2015) Multimodal advertisement of pregnancy in free-ranging female Japanese macaques (Macaca fuscata). PLoS ONE 10:e0135127. doi: 10.1371/journal.pone.0135127 CrossRefPubMedPubMedCentralGoogle Scholar
  58. Roberts JL, Swan RA (1981) Quantitative studies of ovine haemonchosis. I. Relationship between faecal egg counts and total worm counts. Vet Parasitol 8:165–171. doi: 10.1016/0304-4017(81)90044-3 CrossRefGoogle Scholar
  59. Roulin A, Jungi TW, Pfister H, Dijkstra C (2000) Female barn owls (Tyto alba) advertise good genes. Proc R Soc Lond B Biol Sci 267:937–941. doi: 10.1098/rspb.2000.1093 CrossRefGoogle Scholar
  60. Roulin A, Riols C, Dijkstra C, Ducrest A-L (2001) Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba). Behav Ecol 12:103–110CrossRefGoogle Scholar
  61. Seivwright LJ, Redpath SM, Mougeot F (2004) Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus. J Helminthol 78:69–76. doi: 10.1079/JOH2003220 CrossRefPubMedGoogle Scholar
  62. 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 39:177–184. doi: 10.1006/hbeh.2000.1628 CrossRefPubMedGoogle Scholar
  63. Setchell JM, Wickings JE (2004) Sexual swelling in mandrills (Mandrillus sphinx): a test of the reliable indicator hypothesis. Behav Ecol 15:438–445. doi: 10.1093/beheco/arh027 CrossRefGoogle Scholar
  64. Setchell JM, Wickings EJ (2005) Dominance, status signals and coloration in male mandrills (Mandrillus sphinx). Ethology 111:25–50. doi: 10.1111/j.1439-0310.2004.01054.x CrossRefGoogle Scholar
  65. Setchell JM, Wickings JE (2006) Mate choice in male mandrills (Mandrillus sphinx). Ethology 112(1):91–99. doi: 10.1111/j.1439-0310.2006.01128.x CrossRefGoogle Scholar
  66. Setchell JM, Charpentier MJE, Bedjabaga I-B et al (2006a) Secondary sexual characters and female quality in primates. Behav Ecol Sociobiol 61:305–315. doi: 10.1007/s00265-006-0260-7 CrossRefGoogle Scholar
  67. Setchell JM, Wickings EJ, Knapp LA (2006b) Signal content of red facial coloration in female mandrills (Mandrillus sphinx). Proc Biol Sci 273:2395–2400. doi: 10.1098/rspb.2006.3573 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Setchell JM, Charpentier MJE, Abbott KM et al (2009) Is brightest best? Testing the Hamilton-Zuk hypothesis in mandrills. Int J Primatol 30:825–844. doi: 10.1007/s10764-009-9371-0 CrossRefGoogle Scholar
  69. Shimizu K, Udono T, Tanaka C, Narushima E, Yoshihara M, Takeda M, Tanahashi A, van Elsackar L, Hayashi M, Takenaka O (2003) Comparative study of urinary reproductive hormones in great apes. Primates 44:183–190PubMedGoogle Scholar
  70. Shimizu K (2005) Studies on reproductive endocrinology in non-human primates: application of non-invasive methods. J Reprod Dev 51:1–13CrossRefPubMedGoogle Scholar
  71. Stear MJ, Bishop SC, Duncan JL et al (1995) The repeatability of faecal egg counts, peripheral eosinophil counts, and plasma pepsinogen concentrations during deliberate infections with Ostertagia circumcincta. Int J Parasitol 25:375–380. doi: 10.1016/0020-7519(94)00136-C CrossRefPubMedGoogle Scholar
  72. Stevens M, Stoddard MC, Higham JP (2009) Studying primate color: towards visual system-dependent methods. Int J Primatol 30:893–917. doi: 10.1007/s10764-009-9356-z CrossRefGoogle Scholar
  73. Street SE, Cross CP, Brown GR (2016) Exaggerated sexual swellings in female nonhuman primates are reliable signals of female fertility and body condition. Anim Behav 112:203–212. doi: 10.1016/j.anbehav.2015.11.023 CrossRefGoogle Scholar
  74. Számadó S, Penn DJ (2015) Why does costly signalling evolve? Challenges with testing the handicap hypothesis. Anim Behav 110:e9–e12. doi: 10.1016/j.anbehav.2015.06.005 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Takahata Y, Suzuki S, Agetsuma N et al (1998) Reproduction of wild Japanese macaque females of Yakushima and Kinkazan Islands: a preliminary report. Primates 39:339–349. doi: 10.1007/BF02573082 CrossRefGoogle Scholar
  76. Terio KA, Lonsdorf EV, Kinsel MJ et al (2016) Oesophagostomiasis in non-human primates of Gombe National Park. Am J Primatol, Tanzania. doi: 10.1002/ajp.22572 Google Scholar
  77. Waitt C, Little AC, Wolfensohn S et al (2003) Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice. Proc R Soc B Biol Sci 270:S144–S146. doi: 10.1098/rsbl.2003.0065 CrossRefGoogle Scholar
  78. Watanabe K, Mori A, Kawai M (1992) Characteristic features of the reproduction of Koshima monkeys, Macaca fuscata fuscata: a summary of thirty-four years of observation. Primates 33:1–32. doi: 10.1007/BF02382760 CrossRefGoogle Scholar
  79. Weiss SL (2002) Reproductive signals of female lizards: pattern of trait expression and male response. Ethology 108:793–813. doi: 10.1046/j.1439-0310.2002.00819.x CrossRefGoogle Scholar
  80. Weiss SL (2006) Female-specific color is a signal of quality in the striped plateau lizard (Sceloporus virgatus). Behav Ecol 17:726–732. doi: 10.1093/beheco/arl001 CrossRefGoogle Scholar
  81. Wilcox AJ, Weingberg CR, Baird DD (1995) Timing of sexual intercourse in relation to ovulation: effects on the probability of conception, survival of the pregnancy and sex of the baby. N Engl J Med 333:189–194CrossRefGoogle Scholar
  82. Young KH, Bullock SL, Melvin DM, Spruill CL (1979) Ethyl acetate as a substitute for diethyl ether in the formalin-ether sedimentation technique. J Clin Microbiol 10:852–853PubMedPubMedCentralGoogle Scholar
  83. Zahavi A (1975) Mate selection-a selection for a handicap. J Theor Biol 53:205–214CrossRefPubMedGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan 2016

Authors and Affiliations

  • Lucie Rigaill
    • 1
  • Andrew J. J. MacIntosh
    • 1
    • 2
  • James P. Higham
    • 3
  • Sandra Winters
    • 3
  • Keiko Shimizu
    • 4
  • Keiko Mouri
    • 1
  • Takafumi Suzumura
    • 2
  • Takeshi Furuichi
    • 1
  • Cécile Garcia
    • 5
  1. 1.Social Systems Evolution Section, Department of Ecology and Social Behaviors, Primate Research InstituteKyoto UniversityInuyamaJapan
  2. 2.Wildlife Research CenterKyoto UniversityKyotoJapan
  3. 3.Department of Anthropology, Center for the Study of Human OriginsNew York UniversityNew YorkUSA
  4. 4.Department of Zoology, Faculty of ScienceOkayama University of ScienceOkayama CityJapan
  5. 5.CNRS-Muséum National d’Histoire NaturelleParisFrance

Personalised recommendations