Skip to main content
SpringerLink
Log in

Post-copulatory grooming: a conditional mating strategy?

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aho K, DeWayne D, Peterson T (2014) Model selection for ecologists: the worldviews of AIC and BIC. Ecology 95:631–636

    Article  PubMed  Google Scholar 

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267

    Article  CAS  PubMed  Google Scholar 

  • Baldwin JD, Baldwin JI (1997) Gender differences in sexual interest. Arch Sex Behav 26:181–210

    Article  CAS  PubMed  Google Scholar 

  • Bancroft J (2005) The endocrinology of sexual arousal. J Endocrinol 186:411–427

    Article  CAS  PubMed  Google Scholar 

  • 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

  • Berard JD, Nurnberg P, Epplen JT, Schmidtke J (1994) Alternative reproductive tactics and reproductive success in male rhesus macaques. Behaviour 129:177–201

    Article  Google Scholar 

  • Berenstain L, Wade TD (1983) Intrasexual selection and male mating strategies in baboons and macaques. Int J Powder Metall 4:201–235

    Google Scholar 

  • 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 62:1453–1466

    Article  Google Scholar 

  • 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 52:375–383

    Article  PubMed  Google Scholar 

  • Bretman A, Gage MJ, Chapman T (2011) Quick-change artists: male plastic behavioural responses to rivals. Trends Ecol Evol 26:467–473

    Article  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • 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 29–62

    Google Scholar 

  • Carroll SP (1988) Contrasts in reproductive ecology between temperate and tropical populations of Jadera haematoloma, a mate-guarding hemipteran (Rhopalidae). Ann Entomol Soc Am 81:54–63

    Article  Google Scholar 

  • Cheney DL, Seyfarth RM (2009) Stress and coping mechanisms in female primates. Adv Study Behav 39:1–44

    Article  Google Scholar 

  • 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 53:254–265

    Article  PubMed  Google Scholar 

  • de Vries H, Netto WJ, Hanegraaf PL (1993) Matman: a program for the analysis of sociometric matrices and behavioural transition matrices. Behaviour 125:157–175

    Article  Google Scholar 

  • Deag JM (1974) A study of the social behavior and ecology of the wild Barbary macaque (Macaca sylvanus). PhD Thesis, University of Bristol

  • Deag JM, Crook JH (1971) Social behaviour and ‘agonistic buffering’ in the wild Barbary macaque Macaca sylvana. L Folia Primatol 15:183–200

    Article  CAS  PubMed  Google Scholar 

  • Dewsbury DA (1972) Patterns of copulatory behavior in male mammals. Q Rev Biol 47:1–33

    Article  CAS  PubMed  Google Scholar 

  • Dewsbury DA (1973) Copulatory behavior of montane voles (Microtus montanus). Behaviour 44:186–202

    Article  Google Scholar 

  • Dixson AF (2012) Primate sexuality: comparative studies of the prosimians, monkeys, apes, and humans. Oxford University Press, Oxford

    Book  Google Scholar 

  • Dominey WJ (1984) Alternative mating tactics and evolutionarily stable strategies. Am Zool 24:385–396

    Article  Google Scholar 

  • Dunbar RIM (1991) Functional significance of social grooming in primates. Folia Primatol 57:121–131

    Article  Google Scholar 

  • 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, e23105

    Article  PubMed Central  PubMed  Google Scholar 

  • Gabriel W, Luttbeg B, Sih A, Tollrian R (2005) Environmental tolerance, heterogeneity, and the evolution of reversible plastic responses. Am Nat 166:339–353

    Article  PubMed  Google Scholar 

  • Goodall J (1986) The chimpanzees of Gombe: patterns of behavior. Harvard University Press, Cambridge, MA

    Google Scholar 

  • Gross MR (1996) Alternative reproductive strategies and tactics—diversity within sexes. Trends Ecol Evol 11:92–98

    Article  CAS  PubMed  Google Scholar 

  • Gumert MD (2007) Payment for sex in a macaque mating market. Anim Behav 74:1655–1667

    Article  Google Scholar 

  • 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 70:44–53

    Article  CAS  PubMed  Google Scholar 

  • Higham JP, Semple S, MacLarnon A, Heistermann M, Ross C (2009) Female reproductive signaling, and male mating behavior, in the olive baboon. Horm Behav 55:60–67

    Article  CAS  PubMed  Google Scholar 

  • Hughes SM, Kruger DJ (2011) Sex differences in post-coital behaviors in long- and short-term mating: an evolutionary perspective. J Sex Res 48:496–505

    Article  PubMed  Google Scholar 

  • Jackson R (1992) Conditional strategies and interpopulation variation in the behaviour of jumping spiders. New Zeal J Zool 19:99–111

    Article  Google Scholar 

  • Johnstone RA, Reynolds JD, Deutsch JC (1996) Mutual mate choice and sex differences in choosiness. Evolution 50:1382–1391

    Article  Google Scholar 

  • Kondo M, Kishi H, Kojima C et al (2003) Lactation-associated infertility in Japanese monkeys (Macaca fuscata) during the breeding season. Zoo Biol 22:65–76

    Article  Google Scholar 

  • Koyama NF, Caws C, Aureli F (2012) Supply and demand predict male grooming of swollen females in captive chimpanzees, Pan troglodytes. Anim Behav 84:1419–1425

    Article  Google Scholar 

  • Kuester J, Paul A (1984) Female reproductive characteristics in semifree-ranging Barbary macaques (Macaca sylvanus L. 1758). Folia Primatol 43:69–83

    Article  Google Scholar 

  • Kuester J, Paul A (1992) Influence of male competition and female mate choice on male mating success in Barbary macaques (Macaca sylvanus). Behaviour 120:192–217

    Article  Google Scholar 

  • Kuester J, Paul A (1996) Female-female competition and male mate choice in Barbary macaques (Macaca sylvanus). Behaviour 133:763–790

    Article  Google Scholar 

  • Lampiao F (2014) Coitus interruptus: are there spermatozoa in the pre-ejaculate? Int J Med Biomed Res 3:1–4

    Article  Google Scholar 

  • Lee HJ, Macbeth AH, Pagani JH, Young WS 3rd (2009) Oxytocin: the great facilitator of life. Prog Neurobiol 88:127–151

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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 62:1027–1035

    Article  Google Scholar 

  • Li BG, Zhao DP (2007) Copulation behavior within one-male groups of wild Rhinopithecus roxellana in the Qinling Mountains of China. Primates 48:190–196

    Article  PubMed  Google Scholar 

  • Li J, Yin H, Zhou L (2007) Non-reproductive copulation behavior among Tibetan macaques (Macaca thibetana) at Huangshan, China. Primates 48:64–72

    Article  PubMed  Google Scholar 

  • 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 92:371–375

    Article  CAS  PubMed  Google Scholar 

  • 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 33:73–92

    Google Scholar 

  • Massen JJ, Sterck EH (2013) Stability and durability of intra-and intersex social bonds of captive rhesus macaques (Macaca mulatta). Int J Powder Metall 34:770–791

    Google Scholar 

  • Massen JJ, Sterck EH, de Vos H (2010) Close social associations in animals and humans: functions and mechanisms of friendship. Behaviour 147:1379–1412

    Article  Google Scholar 

  • Matsumoto-Oda A (1999) Female choice in the opportunistic mating of wild chimpanzees (Pan troglodytes schweinfurthii) at Mahale. Behav Ecol Sociobiol 46:258–266

    Article  Google Scholar 

  • McGill TE (1962) Sexual behavior in three inbred strains of mice. Behaviour 19:341–350

    Article  Google Scholar 

  • McManus JJ (1967) Observations on sexual behavior of the opossum, Didelphis marsupialis. J Mammal 481:486–487

    Article  Google Scholar 

  • 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 324:601–610

    Article  Google Scholar 

  • 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 35:79–88

    Article  Google Scholar 

  • Nishida T (1997) Sexual behavior of adult male chimpanzees of the Mahale Mountains national park, Tanzania. Primates 38:379–398

    Article  Google Scholar 

  • 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 74:217–228

    Article  CAS  PubMed  Google Scholar 

  • Palombit RA, Cheney DL, Seyfarth RM (2001) Female–female competition for male ‘friends’ in wild chacma baboons (Papio cynocephalus ursinus). Anim Behav 61:1159–1171

    Article  Google Scholar 

  • Palombit RA, Seyfarth RM, Cheney DL (1997) The adaptive value of ‘friendships’ to female baboons: experimental and observational evidence. Anim Behav 54:599–614

    Article  PubMed  Google Scholar 

  • Parga JA (2010) Male post-ejaculatory mounting in the ring-tailed lemur (Lemur catta): a behavior solicited by females? Ethology 116:832–842

    Google Scholar 

  • Paul A, Kuester J, Arnemann J (1996) The sociobiology of male–infant interactions in Barbary macaques, Macaca sylvanus. Anim Behav 51:155–170

    Article  Google Scholar 

  • 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 89:2998–3006

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 275:571–578

    Article  Google Scholar 

  • Possamaia CB, Youngb RJ, de Oliveiraa RC, Mendesd SL, Striere KB (2005) Age-related variation in copulations of male northern muriquis. Folia Primatol 76:33–36

    Article  Google Scholar 

  • Prentice AM, Prentice A (1988) Energy costs of lactation. Annu Rev Nutr 8:63–79

    Article  CAS  PubMed  Google Scholar 

  • Rao GM (1995) Oxytocin induces intimate behaviors. Indian J Med Sci 49:261–266

    CAS  PubMed  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, www.r-project.org/

  • 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 36:135–143

    Article  Google Scholar 

  • Rowell TE (1963) Behaviour and female reproductive cycles of rhesus macaques. J Reprod Fertil 6:193–203

    Article  CAS  PubMed  Google Scholar 

  • Silk JB (2007a) The adaptive value of sociality in mammalian groups. Philos T Roy Soc B 362:539–559

    Article  Google Scholar 

  • Silk JB (2007b) Social components of fitness in primate groups. Science 317:1347–1351

    Article  CAS  PubMed  Google Scholar 

  • 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 121–143

    Google Scholar 

  • Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234

    Article  CAS  PubMed  Google Scholar 

  • 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 38:891–895

    Article  CAS  PubMed  Google Scholar 

  • Small MF (1990a) Alloparental behaviour in Barbary macaques, Macaca sylvanus. Anim Behav 39:297–306

    Article  Google Scholar 

  • Small MF (1990b) Promiscuity in Barbary macaques (Macaca sylvanus). Am J Primatol 20:267–282

    Article  Google Scholar 

  • Smuts BB (1985) Sex and friendship in baboons. Transaction Publishers, New York

    Google Scholar 

  • Soltis J (1999) Measuring male-female relationships during the mating season in wild Japanese macaques (Macaca fuscata yakui). Primates 40:453–467

    Article  Google Scholar 

  • 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 77:688–700

    Article  CAS  PubMed  Google Scholar 

  • Stopka P, Graciasová R (2001) Conditional allogrooming in the herb-field mouse. Behav Ecol 12:584–589

    Article  Google Scholar 

  • 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 287–344

    Google Scholar 

  • Taub DM (1982) Sexual behavior of wild Barbary macaque males (Macaca sylvanus). Am J Primatol 2:109–113

    Article  Google Scholar 

  • Townsend SW, Deschner T, Zuberbühler K (2008) Female chimpanzees use copulation calls flexibly to prevent social competition. PLoS One 3, e2431

    Article  PubMed Central  PubMed  Google Scholar 

  • Townsend SW, Zuberbuhler K (2009) Audience effects in chimpanzee copulation calls. Commun Integr Biol 2:282–284

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 179

    Google Scholar 

  • Tsukahara T (1990) Initiation and solicitation in male-female grooming in a wild Japanese macaque troop on Yakushima Island. Primates 31:147–156

    Article  Google Scholar 

  • 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 71:153–164

    Article  PubMed  Google Scholar 

  • Wallis J (1992) Chimpanzee genital swelling and its role in the pattern of sociosexual behavior. Am J Primatol 28:101–113

    Article  Google Scholar 

  • 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 52:69–75

    Article  PubMed  Google Scholar 

  • Wilson ME, Walker ML, Gordon TP (1983) Consequences of first pregnancy in rhesus monkeys. Am J Phys Anthropol 61:103–110

    Article  CAS  PubMed  Google Scholar 

  • 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 54:170–177

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 67:1665–1677

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Department of Cognitive Biology, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria

    Ruth S. Sonnweber, Jorg J. M. Massen & W. Tecumseh Fitch

Authors
  1. Ruth S. Sonnweber
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jorg J. M. Massen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. W. Tecumseh Fitch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ruth S. Sonnweber.

Additional information

Communicated by R. Noë

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 41 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sonnweber, R.S., Massen, J.J.M. & Fitch, W.T. Post-copulatory grooming: a conditional mating strategy?. Behav Ecol Sociobiol 69, 1749–1759 (2015). https://doi.org/10.1007/s00265-015-1987-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-015-1987-9

Keywords

Search

Navigation