Skip to main content
Log in

Does rank rule? Rank-related grooming patterns in Nicobar long-tailed macaques Macaca fascicularis umbrosus

  • Original Article
  • Published:
Primates Aims and scope Submit manuscript

Abstract

Primates maintain social bonds with specific individuals in the group by directing grooming toward them. Social grooming is often targeted toward individuals with whom the most benefits can be exchanged, which are usually the high-ranking individuals. We used the Seyfarth model to investigate whether dominance rank alters the distribution of grooming in a group of Macaca fascicularis umbrosus at Great Nicobar Island. We investigated whether dominance rank predicted grooming rate in both males and females. We used social network analysis to examine whether high-ranking animals maintain a central position in the grooming network. We also investigated whether adult individuals exchange grooming for social tolerance, as indicated by physical proximity. We found that more social grooming was directed toward high-ranking females, but not high-ranking males. Social network analysis suggested that high-ranking animals are not central individuals in the distribution of grooming; rather, middle-ranking animals were major contributors to the distribution of grooming. There was no relation between the grooming rate and proximity in both males and females. Overall, our findings suggest that females prefer to direct grooming toward high-ranking partners, although the dominance hierarchy is less steep than expected for Macaca fascicularis. Thus rank-related grooming patterns may be a relatively conserved trait in this isolated island population.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–266

    Article  CAS  PubMed  Google Scholar 

  • Aureli F, de Waal FBM (eds) (2000) Natural conflict resolution. University of California Press, California, 409 p

    Google Scholar 

  • Aureli F, Preston SD, de Waal FBM (1999) Heart rate responses to social interactions in free-moving rhesus macaques (Macaca mulatta): a pilot study. J Comp Psychol 113:59–65

    Article  CAS  PubMed  Google Scholar 

  • Balasubramaniam KN, Dittmar K, Berman CM, Butovskaya M, Cooper MA, Majolo B, Ogawa H, Schino G, Thierry B, de Waal FBM (2012) Hierarchical steepness, counter-aggression, and macaque social style scale. Am J Primatol 74:915–925

    Article  PubMed  Google Scholar 

  • Barrett L, Henzi SP, Lusseau D (2012) Taking sociality seriously: the structure of multi-dimensional social networks as a source of information for individuals. Philos T R Soc B 367:2108–2118

    Article  Google Scholar 

  • Barthélemy M, Barrat A, Pastor-Satorras R, Vespignani A (2005) Characterization and modeling of weighted networks. Phys A 346:34–43

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) lme4: Linear mixed-effects models using Eigen and S4. R package version 1:1–21

    Google Scholar 

  • Bejder L, Fletcher D, Bräger S (1998) A method for testing association patterns of social animals. Anim Behav 56:719–725

    Article  CAS  PubMed  Google Scholar 

  • Boccia ML (1987) The physiology of grooming: a test of the tension reduction hypothesis. Am J Primatol 12:330–332

    Article  Google Scholar 

  • Boccia ML (1989) Comparison of the physical characteristics of grooming in two species of macaques (Macaca nemestrina and M. radiata). J Comp Psychol 103:177–183

    Article  CAS  PubMed  Google Scholar 

  • Borgatti SP, Everett MG, Freeman LC (2002) Ucinet for Windows: Software for social network analysis. Analytic Technol, Harvard

    Google Scholar 

  • Brent LJ, Lehmann J, Ramos-Fernández G (2011) Social network analysis in the study of nonhuman primates: a historical perspective. Am J Primatol 73:720–730

    Article  PubMed  PubMed Central  Google Scholar 

  • Butovskaya ML, Kozintsev AG, Kozintsev BA (1994) The structure of affiliative relations in a primate community: allogrooming in stumptailed macaques (Macaca arctoides). J Hum Evol 9:11–23

    Article  Google Scholar 

  • Butovskaya M, Kozintsev A, Welker C (1995) Grooming and social rank by birth: the case of Macaca fascicularis. Folia Primatol 65:30–33

    Article  CAS  Google Scholar 

  • Carnes LM, Nunn CL, Lewis RJ (2011) Effects of the distribution of female primates on the number of males. PLoS ONE 6:e19853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapais B (1983) Reproductive activity in relation to male dominance and the likelihood of ovulation in rhesus monkeys. Behav Ecol Sociobiol 12:215–228

    Article  Google Scholar 

  • Chepko-Sade BD, Reitz KP, Sade DS (1989) Sociometrics of Macaca Mulatta IV: Network analysis of social structure of a pre-fission group. Soc Networks 11:293–314

    Article  Google Scholar 

  • Cohen B (2008) Explicit psychological statistics. John Wiley & Sons, New York

    Google Scholar 

  • Cooper MA, Bernstein IS (2000) Social grooming in Assamese macaques (Macaca assamensis). Am J Primatol 50:77–85

    Article  CAS  PubMed  Google Scholar 

  • Cooper MA, Bernstein IS (2008) Evaluating dominance styles in Assamese and rhesus macaques. Int J Primatol 29:225–243

    Article  Google Scholar 

  • Cords M (1995) Predator vigilance costs of allogrooming in wild blue monkeys. Behaviour 132:559–569

    Article  Google Scholar 

  • Croft DP, James R, Krause J (2008) Exploring animal social networks. Princeton University Press, Princeton

    Book  Google Scholar 

  • de Waal FBM (2008) Putting the altruism back into altruism: the evolution of empathy. Annu Rev Psychol 59:279–300

    Article  PubMed  Google Scholar 

  • de Waal FBM, Luttrell LM (1986) The similarity principle underlying social bonding among female rhesus monkeys. Folia Primatol 46:215–234

    Article  Google Scholar 

  • de Vries H, Stevens JM, Vervaecke H (2006) Measuring and testing the steepness of dominance hierarchies. Anim Behav 71:585–592

    Article  Google Scholar 

  • Dunbar RIM (2010) The social role of touch in humans and primates: behavioural function and neurobiological mechanisms. Neurosci Biobehav Rev 34:260–268

    Article  CAS  PubMed  Google Scholar 

  • Dunbar R (2018) Network structure and social complexity in primates. bioRxiv: 354068

  • Flack JC, Girvan M, de Waal FBM, Krakauer DC (2006) Policing stabilizes construction of social niches in primates. Nature 439:426–429

    Article  CAS  PubMed  Google Scholar 

  • Fooden J (1995) Systematics review of Southeast Asian longtail macaques, Macaca fascicularis (Raffles, 1821) Fieldiana. Zool 81:2–3

    Google Scholar 

  • Gammell MP, de Vries H, Jennings DJ, Carlin CM, Hayden TJ (2003) David’s score: a more appropriate dominance ranking method than Clutton-Brock et al’.s index. Anim Behav 66:601–605

    Article  Google Scholar 

  • Gumert MD (2010) Dominance and reciprocity in the grooming relationships of female long tailed macaques (Macaca fascicularis) in Indonesia. In: Gursky-Doyen, S, Supriatna, J. (eds) Indonesian Primates. Springer Science & Business Media, pp. 309–341

  • Hamilton WD (1964) The genetical evolution of social behaviour II. J Theoret Biol 7:17–52

    Article  CAS  Google Scholar 

  • Hannemann RA, Riddle M (2005) Introduction to social network methods. University of California, Riverside, CA

    Google Scholar 

  • Hemelrijk CK (1990) Models of, and tests for, reciprocity, unidirectionality and other social interaction patterns at a group level. Anim Behav 39:1013–1029

    Article  Google Scholar 

  • Hemelrijk CK, Ek A (1991) Reciprocity and interchange of grooming and ‘support’ in captive chimpanzees. Anim Behav 41:923–935

    Article  Google Scholar 

  • Henzi SP, Barrett L (1999) The value of grooming to female primates. Primates 40:47–59

    Article  Google Scholar 

  • Isbell LA (1991) Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behav Ecol 2:143–155

    Article  Google Scholar 

  • Isbell LA, Pruetz JD (1998) Differences between vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas) in agonistic interactions between adult females. Int J Primatol 19:837–855

    Article  Google Scholar 

  • Isbell LA, van Vuren D (1996) Differential costs of locational and social dispersal and their consequences for female group-living primates. Behaviour 133:1–36

    Article  Google Scholar 

  • Isbell LA, Young TP (2002) Ecological models of female social relationships in primates: similarities, disparities, and some directions for future clarity. Behaviour 139:177–202

    Article  Google Scholar 

  • Isbell LA, Pruetz JD, Young TP (1998) Movements of vervets (Cercopithecus aethiops) and patas monkeys (Erythrocebus patas) as estimators of food resource size, density, and distribution. Behav Ecol Sociobiol 42:123–133

    Article  Google Scholar 

  • Kanngiesser P, Sueur C, Riedl K, Grossmann J, Call J (2011) Grooming network cohesion and the role of individuals in a captive chimpanzee group. Am J Primatol 73:758–767

    Article  PubMed  Google Scholar 

  • Karunakaran C, Ray KK, Sen CR, Saha SS, Sarkar SK (1975) Geology of Great Nicobar Island. J Geol Soc India 16:135–142

    Google Scholar 

  • Keverne EB, Martensz ND, Tuite B (1989) Beta-endorphin concentrations in cerebrospinal fluid of monkeys are influenced by grooming relationships. Psychoneuroendocrinology 14:155–161

    Article  CAS  PubMed  Google Scholar 

  • Klass K, Cords M (2011) Effect of unknown relationships on linearity, steepness and rank ordering of dominance hierarchies: simulation studies based on data from wild monkeys. Behav Process 88:168–176

    Article  Google Scholar 

  • Koenig A, Borries C (2006) The predictive power of socioecological models: consideration of resource characteristics, agonism, and dominance hierarchies. In: Hohmann G, Robbins MM, Boesch C (eds) Feeding ecology in apes and other primates. Cambridge University Press, New York, pp 263–284

    Google Scholar 

  • Kumara HN, Singh M, Mukherjee S, Mishra PS, Vinoth S, Velankar AD, Pal A (2016) Social organization, behavior and phylogeography of Macaca fascicularis umbrosa on the Nicobar Islands, India. Sálim Ali Centre for Ornithology and Natural History, Coimbatore, India, Technical Report, Submitted to SERB-DST, Govt. of India

  • Lehmann J, Korstjens AH, Dunbar RIM (2007) Group size, grooming and social cohesion in primates. Anim Behav 74:1617–1629

    Article  Google Scholar 

  • Lindburg DG (1973) Grooming behavior as a regulator of social interaction in rhesus monkeys. In: Carpenter CR (ed) Behavioral regulators of behavior in primates. Bucknell University Press, Lewisberg, pp 124–148

    Google Scholar 

  • Macdonald S, Schülke O, Ostner J (2013) The absence of grooming for rank-related benefits in female Assamese macaques (Macaca assamensis). Int J Primatol 34:571–584

    Article  Google Scholar 

  • Maestripieri D (1993) Vigilance costs of allogrooming in macaque mothers. Amer Nat 141:744–753

    Article  CAS  Google Scholar 

  • Newman ME (2003) The structure and function of complex networks. SIAM Rev 45:167–256

    Article  Google Scholar 

  • Noë R, Hammerstein P (1994) Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism and mating. Behav Ecol Sociobiol 35:1–11

    Article  Google Scholar 

  • Nunn CL (1999) The number of males in primate social groups: a comparative test of the socioecological model. Behav Ecol Sociobiol 46:1–13

    Article  Google Scholar 

  • Ostner J, Schülke O (2014) The evolution of social bonds in primate males. Behaviour 151:871–906

    Article  Google Scholar 

  • Pal A (2018) A study on reproductive behavior of Nicobar long-tailed macaque (Macaca fascicularis umbrosus) in Nicobar Islands, India. PhD dissertation, Manipal Academy of Higher Education, Manipal

  • Pal A, Kumara HN, Velankar A, Mishra PS, Singh M (2018) Demography and birth seasonality in the Nicobar long-tailed macaque (Macaca fascicularis umbrosus). Curr Sci 114:1732–1737

    Article  Google Scholar 

  • Pasquaretta C, Levé M, Claidiere N, van De Waal E, Whiten A, MacIntosh AJ, Pelé M, Bergstrom ML, Borgeaud C, Brosnan SF, Crofoot MC (2014) Social networks in primates: smart and tolerant species have more efficient networks. Sci Rep 4:7600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paul A (1997) Breeding seasonality affects the association between dominance and reproductive success in non-human male primates. Folia Primatol 68:344–349

    Article  CAS  Google Scholar 

  • R Development Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.Rproject.org/

  • Roubová V, Konečná M, Šmilauer P, Wallner B (2015) Whom to groom and for what? Patterns of grooming in female Barbary macaques (Macaca sylvanus). PLoS ONE 10:e0117298

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schino G (2001) Grooming, competition and social rank among female primates: a meta-analysis. Anim Behav 62:265–271

    Article  Google Scholar 

  • Schino G, Aureli F (2008) Grooming reciprocation among female primates: a meta-analysis. Biol Lett 4:9–11

    Article  PubMed  Google Scholar 

  • Schino G, Scucchi S, Maestripieri D, Turillazzi PG (1988) Allogrooming as a tension-reduction mechanism: a behavioral approach. Am J Primatol 16:43–50

    Article  PubMed  Google Scholar 

  • Schmid VS, de Vries H (2013) Finding a dominance order most consistent with a linear hierarchy: an improved algorithm for the I & SI method. Anim Behav 86:1097–1105

    Article  Google Scholar 

  • Schülke O, Pesek D, Whitman BJ, Ostner J (2011) Ecology of Assamese macaques (Macaca assamensis) at Phu Khieo Wildlife Sanctuary, Thailand. J Wild Thailand 18:1–15

    Google Scholar 

  • Seyfarth RM (1977) A model of social grooming among adult female monkeys. J Theor Biol 65:671–698

    Article  CAS  PubMed  Google Scholar 

  • Silk JB (2002) Kin selection in primate groups. Int J Primatol 23:849–875

    Article  Google Scholar 

  • Sivakumar K (2010) Impact of the tsunami (December, 2004) on the long-tailed macaque of Nicobar Islands, India. Hystrix 21:35–42

    Google Scholar 

  • Sterck EH, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309

    Article  Google Scholar 

  • Sueur C, Jacobs A, Amblard F, Petit O, King AJ (2011) How can social network analysis improve the study of primate behavior? Am J Primatol 73:703–719

    Article  PubMed  Google Scholar 

  • Terry R (1970) Primate grooming as a tension reduction mechanism. J Psychol 76:129–136

    Article  CAS  PubMed  Google Scholar 

  • Thierry B (2007) Unity in diversity: lessons from macaque societies. Evol Anthropol 16:224–238

    Article  Google Scholar 

  • Thierry B, Gauthier C, Peignot P (1990) Social grooming in Tonkean macaques (Macaca tonkeana). Int J Primatol 11:357–375

    Article  Google Scholar 

  • Trivers RL (1971) The evolution of reciprocal altruism. Q Rev Biol 46:35–57

    Article  Google Scholar 

  • Umapathy G, Singh M, Mohnot SM (2003) Status and distribution of Macaca fascicularis umbrosa in the Nicobar Islands, India. Int J Primatol 24:281–293

    Article  Google Scholar 

  • van Hooff JARAM (2000) Relationships among non-human primate males: a deductive framework. In: Kappeler PM (ed) Primate males: causes and consequences of variation in group composition. Cambridge University Press, pp 183

  • van Schaik CP (1989) The ecology of social relationships amongst female primates. In: Standen V, Foley RA (eds) Comparative Socioecology: The Behavioural Ecology of Humans and other Mammals. Blackwell Scientific Publications, Oxford, pp 195–218

    Google Scholar 

  • van Schaik CP (1996) Social evolution in primates: the role of ecological factors and male behaviour. In: Proceedings-British Academy. Oxford University Press Inc

  • van Hooff JARAM, van Schaik CP (1992) Cooperation in competition: the ecology of primate bonds. — In: Harcourt AH, de Waal FBM (eds) Coalitions and alliances in humans and other animals. Oxford University Press, Oxford, pp. 357–389

  • van Hooff JARAM, van Schaik CP (1994) Male bonds: afilliative relationships among nonhuman primate males. Behaviour 130:309–337

    Article  Google Scholar 

  • Velankar AD, Kumara HN, Pal A, Mishra PS, Singh M (2016) Population recovery of Nicobar long-tailed macaque Macaca fascicularis umbrosus following a tsunami in the Nicobar Islands. India PLoS One 11:e0148205

    Article  PubMed  CAS  Google Scholar 

  • Wey T, Blumstein DT, Shen W, Jordan F (2008) Social network analysis of animal behaviour: a promising tool for the study of sociality. Anim Behav 75:333–344

    Article  Google Scholar 

  • Wheatley B (1999) The sacred monkeys of Bali. Waveland Press Inc, Prospect Heights, Illinois

    Google Scholar 

  • Whitehead H (2008) Analyzing animal societies. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–299

    Article  Google Scholar 

  • Xia D, Li J, Garber PA, Sun L, Zhu Y, Sun B (2012) Grooming reciprocity in female Tibetan macaques Macaca thibetana. Am J Primatol 74:569–579

    Article  PubMed  Google Scholar 

  • Xia D, Kyes RC, Wang X, Sun B, Sun L, Li Jl (2019) Grooming networks reveal intra- and intersexual social relationships in Macaca thibetana. Primates 60:223–232

    Article  PubMed  Google Scholar 

  • Zamma K (2002) Grooming site preferences determined by lice infection among Japanese macaques in Arashiyama. Primates 43:41–49

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank the Department of Science and Technology, Government of India, for the financial assistance to HNK (Grant No. SR/SO/AS-49/2011), and SERB J. C. Bose Fellowship to MS (Grant No. SB/S2/JCB-056/2015) for carrying out the project. We thank the Principal Chief Conservator of Forests, Port Blair, Andaman and Nicobar Islands, for granting permission to carry out the study (Permit No. CWLW/WL/134/566) and the Assistant Commissioner, Andaman and Nicobar Administration, for providing the necessary permits to access the tribal areas. We express our gratitude to the Andaman and Nicobar Forest Department, especially the Nicobar division, along with the Nicobar Administration for logistical support. We acknowledge the assistance and logistical support from people in Campbell Bay. We thank Dr. P. A. Azeez, former Director, and Dr. K. Sankar, Director, Sálim Ali Centre for Ornithology and Natural History, Coimbatore for their valuable support. PSM would like to thank Dr. Tha. Thayumanavan, Associate Professor in the Department of Biotechnology, KIT-Kalaignarkarunanidhi Institute of Technology, Coimbatore, for his assistance during the work. We thank Dr. D. Leiva, Dr. H. de Vries, Dr. V. Schmidt, and Dr. C. K. Hemelrijk for their valuable guidance in the data analysis. We thank Ms. S. Sneha, Ms. Dhee, Ms. Marishia Rodrigues, and Ms. Nikita Sarangdhar for their assistance in the fieldwork, and Ms. Annesa Mishra for her help with the sociograms.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Honnavalli N. Kumara.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mishra, P.S., Pal, A., Velankar, A.D. et al. Does rank rule? Rank-related grooming patterns in Nicobar long-tailed macaques Macaca fascicularis umbrosus. Primates 61, 443–453 (2020). https://doi.org/10.1007/s10329-020-00807-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10329-020-00807-4

Keywords

Navigation