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Behavioral Ecology and Sociobiology

, Volume 69, Issue 11, pp 1749–1759 | Cite as

Post-copulatory grooming: a conditional mating strategy?

  • Ruth S. SonnweberEmail author
  • Jorg J. M. Massen
  • W. Tecumseh Fitch
Original Article

Abstract

Animals of diverse taxa show different conditional mating strategies: they adjust their behaviour according to social and environmental situations, which may bring diverse (fitness) advantages for an individual. Especially in primates, mating is often associated with other social behaviours, such as grooming. Here, we study Barbary macaque post-copulatory grooming: we investigate for the first time whether males and females modify their grooming initiations after mating depending to the type of copulation (i.e. with or without ejaculation) and female lactation state. Our results show that males and females adjust grooming initiations conditional on copulation type, with males initiating grooming after copulations with ejaculation and females after non-ejaculatory mating. Moreover, lactating females tend to start grooming the males they just mated with more than vice versa, whereas there is no such a difference for grooming initiations after copulations with non-lactating females. These data indicate that Barbary macaques show post-mating grooming strategies that vary depending on the type of copulation that occurred and in dependence of female reproductive state. These grooming initiation patterns may reflect sex-specific mating interests and potentially serve to increase fitness: females, in particular lactating females, may benefit from initiating grooming to secure protection for themselves and their offspring and reduce harassment. Males may profit from grooming females after ejaculatory copulation by keeping them from mating with another male and thus potentially decreasing sperm competition.

Keywords

Barbary macaques Mating Ejaculatory copulations Non-ejaculatory copulations Single mount ejaculations 

Notes

Acknowledgments

The authors were supported by ERC Advanced Grant no. 230604 SOMACCA (awarded to WTF), a grant of the Austrian Science Foundation (FWF no. P26806-B22 to JJMM) and an Anniversary Fund 2014 grant from the Austrian Academy of Sciences (awarded to WTF and RSS). We thank the Gibraltar Ornithological and Natural History Society for permission to perform the study, and we are particularly grateful to Eric Shaw, Dale Laguea and Damian Holmes for their continuous support throughout the data collection periods. We thank Mark O’Hara, Andrea Ravignani, Gesche Westphal-Fitch, two anonymous reviewers and Roland Noë for helpful comments on the manuscript and statistics. The manuscript was written in loving memory of our dear colleague Kathrin Brauch, whose initial idea spurred this project.

Ethical standards

All applicable international, national and/or institutional guidelines for the care and use of animals were followed. The nature of the study was purely observational: No invasive methodologies were applied at any point of the study. The Gibraltar Ornithological and Natural History Society (GONHS) approved data collection for the study. All procedures were in accordance with British, Austrian and European Union law.

Supplementary material

265_2015_1987_MOESM1_ESM.doc (41 kb)
ESM 1 (DOC 41 kb)

References

  1. Aho K, DeWayne D, Peterson T (2014) Model selection for ecologists: the worldviews of AIC and BIC. Ecology 95:631–636CrossRefPubMedGoogle Scholar
  2. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267CrossRefPubMedGoogle Scholar
  3. Baldwin JD, Baldwin JI (1997) Gender differences in sexual interest. Arch Sex Behav 26:181–210CrossRefPubMedGoogle Scholar
  4. Bancroft J (2005) The endocrinology of sexual arousal. J Endocrinol 186:411–427CrossRefPubMedGoogle Scholar
  5. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1.1-7, https://cran.r-project.org/web/packages/lme4/index.html
  6. Berard JD, Nurnberg P, Epplen JT, Schmidtke J (1994) Alternative reproductive tactics and reproductive success in male rhesus macaques. Behaviour 129:177–201CrossRefGoogle Scholar
  7. Berenstain L, Wade TD (1983) Intrasexual selection and male mating strategies in baboons and macaques. Int J Powder Metall 4:201–235Google Scholar
  8. Brauch K, Hodges K, Engelhardt A, Fuhrmann K, Shaw E, Heistermann M (2008) Sex-specific reproductive behaviours and paternity in free-ranging Barbary macaques (Macaca sylvanus). Behav Ecol Sociobiol 62:1453–1466CrossRefGoogle Scholar
  9. Brauch K, Pfefferle D, Hodges K, Mohle 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. Horm Behav 52:375–383CrossRefPubMedGoogle Scholar
  10. Bretman A, Gage MJ, Chapman T (2011) Quick-change artists: male plastic behavioural responses to rivals. Trends Ecol Evol 26:467–473CrossRefPubMedGoogle Scholar
  11. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New YorkGoogle Scholar
  12. Burton FD (1972) The integration of biology and behavior in the socialization of Macaca sylvana of Gibraltar. In: Poirier FE (ed) Primate Socialization. Random House, NY, pp 29–62Google Scholar
  13. Carroll SP (1988) Contrasts in reproductive ecology between temperate and tropical populations of Jadera haematoloma, a mate-guarding hemipteran (Rhopalidae). Ann Entomol Soc Am 81:54–63CrossRefGoogle Scholar
  14. Cheney DL, Seyfarth RM (2009) Stress and coping mechanisms in female primates. Adv Study Behav 39:1–44CrossRefGoogle Scholar
  15. Crockford C, Wittig RM, Whitten PL, Seyfarth RM, Cheney DL (2008) Social stressors and coping mechanisms in wild female baboons (Papio hamadryas ursinus). Horm Behav 53:254–265CrossRefPubMedGoogle Scholar
  16. de Vries H, Netto WJ, Hanegraaf PL (1993) Matman: a program for the analysis of sociometric matrices and behavioural transition matrices. Behaviour 125:157–175CrossRefGoogle Scholar
  17. Deag JM (1974) A study of the social behavior and ecology of the wild Barbary macaque (Macaca sylvanus). PhD Thesis, University of BristolGoogle Scholar
  18. Deag JM, Crook JH (1971) Social behaviour and ‘agonistic buffering’ in the wild Barbary macaque Macaca sylvana. L Folia Primatol 15:183–200CrossRefPubMedGoogle Scholar
  19. Dewsbury DA (1972) Patterns of copulatory behavior in male mammals. Q Rev Biol 47:1–33CrossRefPubMedGoogle Scholar
  20. Dewsbury DA (1973) Copulatory behavior of montane voles (Microtus montanus). Behaviour 44:186–202CrossRefGoogle Scholar
  21. Dixson AF (2012) Primate sexuality: comparative studies of the prosimians, monkeys, apes, and humans. Oxford University Press, OxfordCrossRefGoogle Scholar
  22. Dominey WJ (1984) Alternative mating tactics and evolutionarily stable strategies. Am Zool 24:385–396CrossRefGoogle Scholar
  23. Dunbar RIM (1991) Functional significance of social grooming in primates. Folia Primatol 57:121–131CrossRefGoogle Scholar
  24. Furtbauer I, Heistermann M, Schulke O, Ostner J (2011) Concealed fertility and extended female sexuality in a non-human primate (Macaca assamensis). PLoS One 6, e23105PubMedCentralCrossRefPubMedGoogle Scholar
  25. Gabriel W, Luttbeg B, Sih A, Tollrian R (2005) Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses. Am Nat 166:339–353CrossRefPubMedGoogle Scholar
  26. Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge, MAGoogle Scholar
  27. Gross MR (1996) Alternative reproductive strategies and tactics—diversity within sexes. Trends Ecol Evol 11:92–98CrossRefPubMedGoogle Scholar
  28. Gumert MD (2007) Payment for sex in a macaque mating market. Anim Behav 74:1655–1667CrossRefGoogle Scholar
  29. Heistermann M, Brauch K, Mohle U, Pfefferle D, Dittami J, Hodges K (2008) Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Am J Primatol 70:44–53CrossRefPubMedGoogle Scholar
  30. Higham JP, Semple S, MacLarnon A, Heistermann M, Ross C (2009) Female reproductive signaling, and male mating behavior, in the olive baboon. Horm Behav 55:60–67CrossRefPubMedGoogle Scholar
  31. Hughes SM, Kruger DJ (2011) Sex differences in post-coital behaviors in long- and short-term mating: an evolutionary perspective. J Sex Res 48:496–505CrossRefPubMedGoogle Scholar
  32. Jackson R (1992) Conditional strategies and interpopulation variation in the behaviour of jumping spiders. New Zeal J Zool 19:99–111CrossRefGoogle Scholar
  33. Johnstone RA, Reynolds JD, Deutsch JC (1996) Mutual mate choice and sex differences in choosiness. Evolution 50:1382–1391CrossRefGoogle Scholar
  34. Kondo M, Kishi H, Kojima C et al (2003) Lactation-associated infertility in Japanese monkeys (Macaca fuscata) during the breeding season. Zoo Biol 22:65–76CrossRefGoogle Scholar
  35. Koyama NF, Caws C, Aureli F (2012) Supply and demand predict male grooming of swollen females in captive chimpanzees, Pan troglodytes. Anim Behav 84:1419–1425CrossRefGoogle Scholar
  36. Kuester J, Paul A (1984) Female reproductive characteristics in semifree-ranging Barbary macaques (Macaca sylvanus L. 1758). Folia Primatol 43:69–83CrossRefGoogle Scholar
  37. Kuester J, Paul A (1992) Influence of male competition and female mate choice on male mating success in Barbary macaques (Macaca sylvanus). Behaviour 120:192–217CrossRefGoogle Scholar
  38. Kuester J, Paul A (1996) Female-female competition and male mate choice in Barbary macaques (Macaca sylvanus). Behaviour 133:763–790CrossRefGoogle Scholar
  39. Lampiao F (2014) Coitus interruptus: are there spermatozoa in the pre-ejaculate? Int J Med Biomed Res 3:1–4CrossRefGoogle Scholar
  40. Lee HJ, Macbeth AH, Pagani JH, Young WS 3rd (2009) Oxytocin: the great facilitator of life. Prog Neurobiol 88:127–151PubMedCentralPubMedGoogle Scholar
  41. Lemasson A, Palombit R, Jubin R (2008) Friendships between males and lactating females in a free-ranging group of olive baboons (Papio hamadryas anubis): evidence from playback experiments. Behav Ecol Sociobiol 62:1027–1035CrossRefGoogle Scholar
  42. Li BG, Zhao DP (2007) Copulation behavior within one-male groups of wild Rhinopithecus roxellana in the Qinling Mountains of China. Primates 48:190–196CrossRefPubMedGoogle Scholar
  43. Li J, Yin H, Zhou L (2007) Non-reproductive copulation behavior among Tibetan macaques (Macaca thibetana) at Huangshan, China. Primates 48:64–72CrossRefPubMedGoogle Scholar
  44. Maeda KI, Tsukamura H, Ohkura S, Kanaizuka T, Suzuki J (1991) Suppression of ovarian activity during the breeding season in suckling Japanese monkey (Macaca fuscata). J Reprod Fertil 92:371–375CrossRefPubMedGoogle Scholar
  45. Massen JJ, Overduin-de Vries AM, de Vos-Rouweler AJ, Spruijt BM, Doxiadis GG, Sterck EH (2012) Male mating tactics in captive rhesus macaques (Macaca mulatta): the influence of dominance, markets, and relationship quality. Int J Powder Metall 33:73–92Google Scholar
  46. Massen JJ, Sterck EH (2013) Stability and durability of intra-and intersex social bonds of captive rhesus macaques (Macaca mulatta). Int J Powder Metall 34:770–791Google Scholar
  47. Massen JJ, Sterck EH, de Vos H (2010) Close social associations in animals and humans: functions and mechanisms of friendship. Behaviour 147:1379–1412CrossRefGoogle Scholar
  48. Matsumoto-Oda A (1999) Female choice in the opportunistic mating of wild chimpanzees (Pan troglodytes schweinfurthii) at Mahale. Behav Ecol Sociobiol 46:258–266CrossRefGoogle Scholar
  49. McGill TE (1962) Sexual behavior in three inbred strains of mice. Behaviour 19:341–350CrossRefGoogle Scholar
  50. McManus JJ (1967) Observations on sexual behavior of the opossum, Didelphis marsupialis. J Mammal 481:486–487CrossRefGoogle Scholar
  51. Ménard N et al (2001) Is male–infant caretaking related to paternity and/or mating activities in wild Barbary macaques (Macaca sylvanus)? Cr Acad Sci III-Vie 324:601–610CrossRefGoogle Scholar
  52. Mitsunaga F, Nozaki M, Shimizu K (1994) Suppressed copulatory behavior and ovarian function in lactating Japanese monkeys (Macaca fuscata fuscata) during the mating season. Primates 35:79–88CrossRefGoogle Scholar
  53. Nishida T (1997) Sexual behavior of adult male chimpanzees of the Mahale Mountains national park, Tanzania. Primates 38:379–398CrossRefGoogle Scholar
  54. Overduin-de Vries AM, Massen JJ, Spruijt BM, Sterck EH (2012) Sneaky monkeys: an audience effect of male rhesus macaques (Macaca mulatta) on sexual behavior. Am J Primatol 74:217–228CrossRefPubMedGoogle Scholar
  55. Palombit RA, Cheney DL, Seyfarth RM (2001) Female–female competition for male ‘friends’ in wild chacma baboons (Papio cynocephalus ursinus). Anim Behav 61:1159–1171CrossRefGoogle Scholar
  56. Palombit RA, Seyfarth RM, Cheney DL (1997) The adaptive value of ‘friendships’ to female baboons: experimental and observational evidence. Anim Behav 54:599–614CrossRefPubMedGoogle Scholar
  57. Parga JA (2010) Male post-ejaculatory mounting in the ring-tailed lemur (Lemur catta): a behavior solicited by females? Ethology 116:832–842Google Scholar
  58. Paul A, Kuester J, Arnemann J (1996) The sociobiology of male–infant interactions in Barbary macaques, Macaca sylvanus. Anim Behav 51:155–170CrossRefGoogle Scholar
  59. Pazol K, Wilson ME, Wallen K (2004) Medroxyprogesterone acetate antagonizes the effects of estrogen treatment on social and sexual behavior in female macaques. J Clin Endocrinol Metab 89:2998–3006PubMedCentralCrossRefPubMedGoogle Scholar
  60. Pfefferle D, Brauch K, Heistermann M, Hodges JK, Fischer J (2008) Female Barbary macaque (Macaca sylvanus) copulation calls do not reveal the fertile phase but influence mating outcome. Proc R Soc Lond B 275:571–578CrossRefGoogle Scholar
  61. Possamaia CB, Youngb RJ, de Oliveiraa RC, Mendesd SL, Striere KB (2005) Age-related variation in copulations of male northern muriquis. Folia Primatol 76:33–36CrossRefGoogle Scholar
  62. Prentice AM, Prentice A (1988) Energy costs of lactation. Annu Rev Nutr 8:63–79CrossRefPubMedGoogle Scholar
  63. Rao GM (1995) Oxytocin induces intimate behaviors. Indian J Med Sci 49:261–266PubMedGoogle Scholar
  64. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, www.r-project.org/
  65. Ren R, Yan K, Su Y, Qi H, Liang B, Bao W, de Waal FBM (1995) The reproductive behavior of golden monkeys in captivity (Rhinopithecus roxellana roxellana). Primates 36:135–143CrossRefGoogle Scholar
  66. Rowell TE (1963) Behaviour and female reproductive cycles of rhesus macaques. J Reprod Fertil 6:193–203CrossRefPubMedGoogle Scholar
  67. Silk JB (2007a) The adaptive value of sociality in mammalian groups. Philos T Roy Soc B 362:539–559CrossRefGoogle Scholar
  68. Silk JB (2007b) Social components of fitness in primate groups. Science 317:1347–1351CrossRefPubMedGoogle Scholar
  69. Silk JB (2014) Evolutionary perspectives on the links between close social bonds, health, and fitness. In: Weinstein M, Lane MA (eds) Sociality, hierarchy, health comparative biodemography. A collection of papers. National Academies Press, Washington, DC, pp 121–143Google Scholar
  70. Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234CrossRefPubMedGoogle Scholar
  71. Slob AK, Groeneveld WH, van der Werff ten Bosch JJ (1986) Physiological changes during copulation in male and female stumptail macaques (Macaca arctoides). Physiol Behav 38:891–895CrossRefPubMedGoogle Scholar
  72. Small MF (1990a) Alloparental behaviour in Barbary macaques, Macaca sylvanus. Anim Behav 39:297–306CrossRefGoogle Scholar
  73. Small MF (1990b) Promiscuity in Barbary macaques (Macaca sylvanus). Am J Primatol 20:267–282CrossRefGoogle Scholar
  74. Smuts BB (1985) Sex and friendship in baboons. Transaction Publishers, New YorkGoogle Scholar
  75. Soltis J (1999) Measuring male-female relationships during the mating season in wild Japanese macaques (Macaca fuscata yakui). Primates 40:453–467CrossRefGoogle Scholar
  76. Sonnweber R, Ravignani A, Stobbe N, Schiestl G, Wallner B, Fitch WT (2015) Rank-dependent grooming patterns and cortisol alleviation in Barbary macaques. Am J Primatol 77:688–700CrossRefPubMedGoogle Scholar
  77. Stopka P, Graciasová R (2001) Conditional allogrooming in the herb-field mouse. Behav Ecol 12:584–589CrossRefGoogle Scholar
  78. Taub DM (1980) Female choice and mating strategies among wild Barbary macaques (Macaca sylvanus L.). In: Lindburg DG (ed) The macaques: studies in ecology, behavior and evolution. Van Nostrand Reinhold Company, New York, NY, pp 287–344Google Scholar
  79. Taub DM (1982) Sexual behavior of wild Barbary macaque males (Macaca sylvanus). Am J Primatol 2:109–113CrossRefGoogle Scholar
  80. Townsend SW, Deschner T, Zuberbühler K (2008) Female chimpanzees use copulation calls flexibly to prevent social competition. PLoS One 3, e2431PubMedCentralCrossRefPubMedGoogle Scholar
  81. Townsend SW, Zuberbuhler K (2009) Audience effects in chimpanzee copulation calls. Commun Integr Biol 2:282–284PubMedCentralCrossRefPubMedGoogle Scholar
  82. Trivers R (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine-Atherton, Chicago, pp pp 136–pp 179Google Scholar
  83. Tsukahara T (1990) Initiation and solicitation in male-female grooming in a wild Japanese macaque troop on Yakushima Island. Primates 31:147–156CrossRefGoogle Scholar
  84. Van Belle S, Estrada A, Ziegler TE, Strier KB (2009) Sexual behavior across ovarian cycles in wild black howler monkeys (Alouatta pigra): male mate guarding and female mate choice. Am J Primatol 71:153–164CrossRefPubMedGoogle Scholar
  85. Wallis J (1992) Chimpanzee genital swelling and its role in the pattern of sociosexual behavior. Am J Primatol 28:101–113CrossRefGoogle Scholar
  86. Wallner B, Aspernig D, Millesi E, Machatschke IH (2011) Non-lactating versus lactating females: a comparison of sex steroids, sexual coloration, and sexual behavior in Japanese macaques. Primates 52:69–75CrossRefPubMedGoogle Scholar
  87. Wilson ME, Walker ML, Gordon TP (1983) Consequences of first pregnancy in rhesus monkeys. Am J Phys Anthropol 61:103–110CrossRefPubMedGoogle Scholar
  88. Wittig RM, Crockford C, Lehmann J, Whitten PL, Seyfarth RM, Cheney DL (2008) Focused grooming networks and stress alleviation in wild female baboons. Horm Behav 54:170–177PubMedCentralCrossRefPubMedGoogle Scholar
  89. Young C, Hähndel S, Majolo B, Schülke O, Ostner J (2013) Male coalitions and female behaviour affect male mating success independent of dominance rank and female receptive synchrony in wild Barbary macaques. Behav Ecol Sociobiol 67:1665–1677CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Ruth S. Sonnweber
    • 1
    Email author
  • Jorg J. M. Massen
    • 1
  • W. Tecumseh Fitch
    • 1
  1. 1.Department of Cognitive BiologyUniversity of ViennaViennaAustria

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