Skip to main content
SpringerLink
Log in

Rank-related partner choice in the fission–fusion society of the spotted hyena (Crocuta crocuta)

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

Abstract

When social partners vary in their relative value, individuals should theoretically initiate partnerships with conspecifics of the highest value. Here, we tested this prediction in a wild population of spotted hyenas (Crocuta crocuta). Crocuta live in complex, fission–fusion societies structured by dominance hierarchies in which individuals vary greatly in their value as social companions. Because patterns of association among Crocuta reflect social preferences, we calculated association indices (AIs) to examine how social rank influences intrasexual partner choice among unrelated adults of both sexes. The highest-ranking individuals were generally most gregarious in both sexes. Females associated most often with dominant and adjacent-ranking females. Females joined subgroups based on the presence of particular conspecifics such that subordinates joined focal females at higher rates than did dominants. Dominants benefit from associations with subordinates by enjoying priority of access to resources obtained and defended by multiple group members, but the benefits of these associations to subordinates are unknown. To investigate this, we tested three hypotheses suggesting how subordinates might benefit from rank-related partner choice among unrelated females. We found that subordinates who initiated group formation benefited by gaining social and feeding tolerance from dominants. However, rates at which dominants provided coalitionary support to subordinates did not vary with AIs. Overall, our data resemble those documenting patterns of association among cercopithecine primates. We consider our results in light of optimal reproductive skew theory, Seyfarth’s rank attractiveness model, and biological market theory. Our data are more consistent with the predictions of Seyfarth’s model and of biological market theory than with those of skew theory.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

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

    PubMed  CAS  Google Scholar 

  • Appleby MC (1983) Competition in a red deer stag social group: rank, age and relatedness of opponents. Anim Behav 31:913–918

    Article  Google Scholar 

  • Barrett L, Henzi SP (2001) The utility of grooming in baboon troops. In: Noë R, van Hooff J, Hammerstein P (eds) Economics in nature: social dilemmas, mate choice, biological markets. Cambridge University Press, Cambridge, pp 119–145

    Google Scholar 

  • Barrett L, Henzi SP, Weingrill T, Lycett JE, Hill RA (1999) Market forces predict grooming reciprocity in female baboons. Proceedings of the Royal Society of London Series B-Biological Sciences 266:665–670

    Article  Google Scholar 

  • Boydston EE, Morelli TL, Holekamp KE (2001) Sex differences in territorial behavior exhibited by the spotted hyena (Hyaenidae, Crocuta crocuta). Ethology 107:369–385

    Article  Google Scholar 

  • Boydston EE, Kapheim KM, Szykman M, Holekamp KE (2003) Individual variation in space use by female spotted hyenas. J Mammal 84:1006–1018

    Article  Google Scholar 

  • Cairns SJ, Schwager SJ (1987) A comparison of association indices. Anim Behav 35:1454–1469

    Article  Google Scholar 

  • Cheney DL, Seyfarth RM, Smuts B (1986) Social relationships and social cognition in non-human primates. Science 234:1361–1366

    Article  PubMed  CAS  Google Scholar 

  • Clutton-Brock TH (1998) Reproductive skew, concessions and limited control. Trends Ecol Evol 13:288–292

    Article  Google Scholar 

  • Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavioral ecology of two sexes. University of Chicago, Chicago

    Google Scholar 

  • Conradt L, Roper TJ (2000) Activity synchrony and social cohesion: a fission–fusion model. Proceedings of the Royal Society of London Series B-Biological Sciences 267:2213–2218

    Article  CAS  Google Scholar 

  • Cooper SM (1991) Optimal hunting group size: the need for lions to defend their kills against loss to spotted hyaenas. Afr J Ecol 29:130–136

    Google Scholar 

  • Couzin ID (2006) Behavioral ecology: social organization in fission–fusion societies. Curr Biol 16:R169–R171

    Article  PubMed  CAS  Google Scholar 

  • Cross PC, Lloyd-Smith JO, Getz WM (2005) Disentangling association patterns in fission–fusion societies using African buffalo as an example. Anim Behav 69:499–506

    Article  Google Scholar 

  • de Villiers PA, Kok OB (1997) Home range, association and related aspects of elephants in eastern Transvaal Lowveld. Afr J Ecol 35:224–236

    Article  Google Scholar 

  • Dloniak SM, French JA, Holekamp KE (2006) Faecal androgen concentrations in adult male spotted hyaenas, Crocuta crocuta, reflect interactions with socially dominant females. Anim Behav 71:27–37

    Article  Google Scholar 

  • Drea CM, Frank LG (2003) The social complexity of spotted hyenas. In: de Waal FBM, Tyack PL (eds) Animal social complexity: intelligence, culture, and individualized societies. Harvard University Press, Cambridge, Massachusetts, pp 121–148

    Google Scholar 

  • Dugatkin LA, Sih A (1995) Behavioral ecology and the study of partner choice. Ethology 99:265–277

    Article  Google Scholar 

  • Dugatkin LA, Sih A (1998) Evolutionary ecology of partner choice. In: Dukas R (ed) Cognitive ecology. University of Chicago Press, Chicago, pp 379–403

    Google Scholar 

  • East ML, Hofer H (2001) Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females. Behav Ecol 12:558–568

    Article  Google Scholar 

  • East ML, Hofer H, Wickler W (1993) The erect ‘penis’ as a flag of submission in a female-dominated society: greetings in Serengeti spotted hyenas. Behav Ecol Sociobiol 33:355–370

    Article  Google Scholar 

  • Engh AL, Esch K, Smale L, Holekamp KE (2000) Mechanisms of maternal rank ‘inheritance’ in the spotted hyaena, Crocuta crocuta. Anim Behav 60:323–332

    Article  PubMed  Google Scholar 

  • Engh AL, Siebert ER, Greenberg DA, Holekamp KE (2005) Patterns of alliance formation and postconflict aggression indicate spotted hyaenas recognize third-party relationships. Anim Behav 69:209–217

    Article  Google Scholar 

  • Frank LG (1986) Social organization of the spotted hyaena (Crocuta crocuta). II. Dominance and reproduction. Anim Behav 34:1510–1527

    Article  Google Scholar 

  • Frank LG, Glickman SE, Powch I (1990) Sexual dimorphism in the spotted hyaena (Crocuta crocuta). J Zool (Lond) 221:308–313

    Google Scholar 

  • Frank LG, Holekamp KE, Smale L (1995) Dominance, demography, and reproductive success of female spotted hyenas. In: Sinclair ARE, Arcese P (eds) Serengeti II: Dynamics, management, and conservation of an ecosystem. University of Chicago Press, Chicago, Illinois, pp 364–384

    Google Scholar 

  • Glickman SE, Frank LG, Pavgi S, Licht P (1992) Hormonal correlates of ‘masculinization’ in female spotted hyaenas (Crocuta crocuta). 1. Infancy to sexual maturity. J Reprod Fertil 95:451–462

    Article  PubMed  CAS  Google Scholar 

  • Gouzoules S, Gouzoules H (1987) Kinship. In: Smuts BB, Cheney DL, Seyfarth RM (eds) Primate Societies. University of Chicago Press, Chicago and London, pp 299–305

    Google Scholar 

  • Hamilton IM (2000) Recruiters and joiners: using optimal skew theory to predict group size and the division of resources within groups of social foragers. Am Nat 155:684–695

    Article  PubMed  Google Scholar 

  • Hammerstein P (2001) Games and markets: economic behaviour in humans and other animals. In: Noë R, van Hooff JARAM, Hammerstein P (eds) Economics in nature: social dilemmas, mate choice, and biological markets. Cambridge University Press, Cambridge, pp 1–22

    Google Scholar 

  • Henzi SP, Barrett L (2002) Infants as a commodity in a baboon market. Anim Behav 63:915–921

    Article  Google Scholar 

  • Henzi SP, Barrett L, Gaynor D, Greeff J, Weingrill T, Hill RA (2003) Effect of resource competition on the long-term allocation of grooming by female baboons: evaluating Seyfarth’s model. Anim Behav 66:931–938

    Article  Google Scholar 

  • Holekamp KE, Smale L (1993) Ontogeny of dominance in free-living spotted hyaenas: juvenile rank relations with other immature individuals. Anim Behav 46:451–466

    Article  Google Scholar 

  • Holekamp KE, Smale L, Szykman M (1996) Rank and reproduction in the female spotted hyaena. J Reprod Fertil 108:229–237

    Article  PubMed  CAS  Google Scholar 

  • Holekamp KE, Cooper SM, Katona CI, Berry NA, Frank LG, Smale L (1997a) Patterns of association among female spotted hyenas (Crocuta crocuta). J Mammal 78:55–74

    Article  Google Scholar 

  • Holekamp KE, Smale L, Berg R, Cooper SM (1997b) Hunting rates and hunting success in the spotted hyena (Crocuta crocuta). J Zool (Lond) 242:1–15

    Article  Google Scholar 

  • Holekamp KE, Boydston EE, Smale L (2000) Group travel in social carnivores. In: Boinski S, Garber PA (eds) On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 587–627

    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 

  • Kruuk H (1972) The spotted hyena: a study of predation and social behavior. University of Chicago Press, Chicago, Illinois

    Google Scholar 

  • Manson JH, Navarrete CD, Silk JB, Perry S (2004) Time-matched grooming in female primates? New analyses from two species. Anim Behav 67:493–500

    Article  Google Scholar 

  • Mills MGL (1990) Kalahari hyaenas: comparative behavioral ecology of two species. Unwin Hyman, London

    Google Scholar 

  • Mundry R, Fischer J (1998) Use of statistical programs for nonparametric tests of small samples often leads to incorrect P values: examples from animal behaviour. Anim Behav 56:256–259

    Article  PubMed  Google Scholar 

  • Noë R (2001) Biological markets: partner choice as the driving force behind the evolution of mutualisms. In: Noë R, van Hooff JARAM, Hammerstein P (eds) Economics in nature: social dilemmas, mate choice, biological markets. Cambridge University Press, Cambridge, pp 93–118

    Google Scholar 

  • Noë R (2006) Cooperation experiments: coordination through communication versus acting apart together. Anim Behav 71:1–18

    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

    Google Scholar 

  • Noë R, Hammerstein P (1995) Biological markets. Trends Ecol Evol 10:336–339

    Article  Google Scholar 

  • Pawlowski B, Dunbar RIM (1999) Impact of market value on human mate choice decisions. Proceedings of the Royal Society of London Series B-Biological Sciences 266:281–285

    Article  CAS  Google Scholar 

  • Reeve HK (1998) Game theory, reproductive skew, and nepotism. In: Dugatkin LA, Reeve HK (eds) Game theory and animal behavior. Oxford University Press, Oxford, pp 118–145

    Google Scholar 

  • Reeve HK (2000) A transactional theory of within-group conflict. Am Nat 155:365–382

    Article  PubMed  Google Scholar 

  • Reeve HK, Emlen ST, Keller L (1998) Reproductive sharing in animal societies: reproductive incentives or incomplete control by dominant breeders? Behav Ecol 9:267–278

    Article  Google Scholar 

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

    Article  PubMed  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 

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

    Article  PubMed  CAS  Google Scholar 

  • Smale L, Frank LG, Holekamp KE (1993) Ontogeny of dominance in free-living spotted hyaenas: juvenile rank relations with adult females and immigrant males. Anim Behav 46:467–477

    Article  Google Scholar 

  • Smale L, Holekamp KE, Weldele M, Frank LG, Glickman SE (1995) Competition and cooperation between litter-mates in the spotted hyaena, Crocuta crocuta. Anim Behav 50:671–682

    Article  Google Scholar 

  • Smale L, Nunes S, Holekamp KE (1997) Sexually dimorphic dispersal in mammals: patterns, causes, and consequences. Adv Study Behav 26:181–250

    Article  Google Scholar 

  • Springer MS, Murphy WJ, Eizirik E, O’Brien SJ (2003) Placental mammal diversification and the Cretaceous–Tertiary boundary. Proceedings of the National Academy of Sciences of the United States of America 100:1056–1061

    Article  PubMed  CAS  Google Scholar 

  • Springer MS, Murphy WJ, Eizirik E, O’Brien SJ (2005) Molecular evidence for major placental clades. In: Rose KD, Archibald JD (eds) The Rise of Placental Mammals. The John Hopkins University Press, Baltimore, pp 37–49

    Google Scholar 

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

    Article  Google Scholar 

  • Szykman M, Engh AL, Van Horn RC, Funk SM, Scribner KT, Holekamp KE (2001) Association patterns among male and female spotted hyenas (Crocuta crocuta) reflect male mate choice. Behav Ecol Sociobiol 50:231–238

    Article  Google Scholar 

  • Van Horn RC, McElhinny TL, Holekamp KE (2003) Age estimation and dispersal in the spotted hyena (Crocuta crocuta). J Mammal 84:1019–1030

    Article  Google Scholar 

  • Van Horn RC, Engh AL, Scribner KT, Funk SM, Holekamp KE (2004) Behavioral structuring of relatedness in the spotted hyena (Crocuta crocuta) suggests direct fitness benefits of clan-level cooperation. Mol Ecol 13:449–458

    Article  PubMed  Google Scholar 

  • Vehrencamp SL (1983) A model for the evolution of despotic versus egalitarian societies. Anim Behav 31:667–682

    Article  Google Scholar 

  • Wahaj SA, Guse KR, Holekamp KE (2001) Reconciliation in the spotted hyena (Crocuta crocuta). Ethology 107:1057–1074

    Article  Google Scholar 

  • Wahaj SA, Van Horn RC, Van Horn TL, Dreyer R, Hilgris R, Schwarz J, Holekamp KE (2004) Kin discrimination in the spotted hyena (Crocuta crocuta): nepotism among siblings. Behav Ecol Sociobiol 56:237–247

    Article  Google Scholar 

  • Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300

    Google Scholar 

Download references

Acknowledgements

We thank the Office of the President of Kenya and the Kenyan Ministry of Education, Science, and Technology for permission to conduct this research. We also thank the Kenya Wildlife Service, the Narok County Council, and the Senior Warden of the Masai Mara National Reserve for their cooperation. Our research, described in Animal Research Protocol AUF 02/03-033-00, was approved most recently on 4 February 2005 by the All University Committee on Animal Use and Care at Michigan State University (MSU) and complies with the current laws of Kenya. We thank L. Smale for her role in data collection and the following individuals for their assistance in the field: N.E. Berry, E.E. Boydston, S.M. Cooper, S.M. Dloniak, M. Durham, A.L. Engh, J. Friedman, P. Garrett, I. Graham, T.H. Harty, C.I. Katona, K. Nelson, G. Ording, M. Szykman, K. Weibel, S.A. Wahaj, and B. White. Thoughtful suggestions from T. Getty, A.G. McAdam, R.M. Seyfarth, L. Smale, and two anonymous reviewers greatly improved the overall quality of this manuscript. Finally, we thank P.S. Bills, M.L. Fisher, and C.C. Strelioff for assistance extracting data from archived field notes. Our work was supported by NSF grants IBN9630667, IBN9906445, IBN0113170, IBN0343381, and IOB0618022 to K.E.H. and fellowships from MSU to J.E.S.

Author information

Authors and Affiliations

  1. Department of Zoology, Michigan State University, East Lansing, MI, 48824-1115, USA

    Jennifer E. Smith, Sandra K. Memenis & Kay E. Holekamp

Authors
  1. Jennifer E. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sandra K. Memenis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kay E. Holekamp
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jennifer E. Smith.

Additional information

Communicated by M. Festa-Bianchet

Rights and permissions

Reprints and permissions

About this article

Cite this article

Smith, J.E., Memenis, S.K. & Holekamp, K.E. Rank-related partner choice in the fission–fusion society of the spotted hyena (Crocuta crocuta). Behav Ecol Sociobiol 61, 753–765 (2007). https://doi.org/10.1007/s00265-006-0305-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-006-0305-y

Keywords

Search

Navigation