Skip to main content
SpringerLink
Log in

What drives flexibility in primate social organization?

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

Abstract

The importance of behavioral flexibility for understanding primate ecology and evolutionary diversity is becoming increasingly apparent, and yet despite the abundance of long-term studies across diverse sampling localities, we still do not understand the myriad factors responsible for among-site variation in species’ social organization. The goals of our study were to address this question via three main objectives: to quantify social organization flexibility (i.e., across-site intraspecific variation) of well-studied primate species, test the idea that closely related species exhibit similar levels of flexibility, and test hypotheses explaining variation in social organization flexibility among primate species. We obtained data for a total of 175 study sites from 32 primate species representing all major primate clades. We employed phylogenetic principal components analysis to quantify social organization flexibility for each species. We quantified the phylogenetic signal in social organization flexibility and then evaluated the best predictors of flexibility. We found that mean group size was positively related to social organization flexibility. Large social groups may be more flexible because the foraging costs and predation risk associated with adding or subtracting individuals are lower compared to small social groups. There was some support that absolute brain size and the presence of fission–fusion dynamics were also related to high levels of social organization flexibility, suggesting that cognitive ability and/or within-site behavioral flexibility may also lead to increased variation across sites. Our results serve as an early step in understanding the patterns and processes related to social organization flexibility in primates and other social mammals.

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

Similar content being viewed by others

References

  • Aiello LC, Dunbar RIM (1993) Neocortex size, group size, and the evolution of language. Curr Anthropol 34:184–193

    Google Scholar 

  • Alexander RD (1974) The evolution of social behavior. Ann Rev Ecol Syst 5:325–383

    Google Scholar 

  • Altmann J (2000) Models of outcome and process: predicting the number of males in primate groups. In: Kappeler PM (ed) Primate males: causes and consequences of variation in group composition. Cambridge University Press, Cambridge, pp 236–237

    Google Scholar 

  • Altmann J, Alberts SC (2003) Variability in reproductive success viewed from a life-history perspective in baboons. Am J Hum Biol 15:401–409

    PubMed  Google Scholar 

  • Arnold C, Matthews LJ, Nunn CL (2010) The 10kTrees website: a new online resource for primate phylogeny. Evol Anthopol 19:114–118

    Google Scholar 

  • Aureli F, Schaffner CM, Boesch C, Bearder SK, Call J et al (2008) Fission-fusion dynamics: new research frameworks. Curr Anthropol 49:627–646

    Google Scholar 

  • Barton RA (2000) Primate brain evolution: cognitive demands of foraging or of social life? In: Boinski S, Garber PA (eds) On the move: how and why animals travel in groups. University of Chicago Press, Chicago, pp 204–237

    Google Scholar 

  • Batschelet E (1981) Circular statistics in biology. Academic Press, London

    Google Scholar 

  • Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745

    PubMed  Google Scholar 

  • Borries C (1997) Infanticide in seasonally breeding multimale groups of Hanuman langurs (Presbytis entellus) in Ramnagar (South Nepal). Behav Ecol Sociobiol 41:139–150

    Google Scholar 

  • Borries C (2000) Male dispersal and mating season influxes in Hanuman langurs living in multi-male groups. In: Kappeler PM (ed) Primate males: causes and consequences of variation in group composition. Cambridge University Press, Cambridge, pp 146–158

    Google Scholar 

  • Borries C, Larney E, Lu A, Ossi K, Koenig A (2008) Costs of group size: lower developmental and reproductive rates in larger groups of leaf monkeys. Behav Ecol 19:1186–1191

    Google Scholar 

  • Brockman DK, van Schaik CP (eds) (2005) Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge Univ Press, New York

    Google Scholar 

  • Burnham KP, Anderson D (2002) Model selection and multi-model inference. Springer, New York

    Google Scholar 

  • Catlett KK, Schwartz GT, Godfrey LR, Jungers WL (2010) “Life history space”: a multivariate analysis of life history variation in extant and extinct Malagasy lemurs. Am J Phys Anthropol 142:391–404

  • Chapman CA, Pavelka M (2005) Group size in folivorous primates: ecological constraints and the possible influence of social factors. Primates 46:1–9

    PubMed  Google Scholar 

  • Chapman CA, Rothman JM (2009) Within-species differences in primate social structure: evolution of plasticity and phylogenetic constraints. Primates 50:12–22

    PubMed  Google Scholar 

  • Chapman CA, Wrangham RW, Chapman LJ (1995) Ecological constraints on group-size—an analysis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 36:59–70

    Google Scholar 

  • Chapman CA, Wrangham RW, Chapman LJ, Kennard DK, Zanne AE (1999) Fruit and flower phenology at two sites in Kibale National Park, Uganda. J Trop Ecol 15:189–211

    Google Scholar 

  • Chapman CA, Chapman L, Cords M, Gathua J, Gautier-Hion A et al (2002) Variation in the diets of Cercopithecus species: differences within forests, among forests, and across species. In: Glenn M, Cords M (eds) The guenons: diversity and adaptation in African monkeys. Kluwer Acad/Plenum Publ, New York, pp 325–350

    Google Scholar 

  • Clutton-Brock TH, Harvey PH (1977) Primate ecology and social organization. J Zool 183:1–39

    Google Scholar 

  • Clutton-Brock TH, Harvey PH (1980) Primates, brains and ecology. J Zool 190:309–323

    Google Scholar 

  • Cords M (2000) The number of males in guenon groups. In: Kappeler PM (ed) Primate males: causes and consequences of variation in group composition. Cambridge University Press, Cambridge, pp 84–96

    Google Scholar 

  • Crockett CM, Janson CH (2000) Infanticide in red howlers: female group size, male membership, and a possible link to folivory. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge Univ Press, Cambridge, pp 75–98

    Google Scholar 

  • Crook JH (1970) Social organization and environment: aspects of contemporary social ethology. Anim Behav 18:197–209

    Google Scholar 

  • Davies AG, Oates JF (1994) Colobine monkeys: their ecology, behaviour and evolution. Cambridge University Press, New York

    Google Scholar 

  • Deacon TW (1990) Fallacies of progression in theories of brain-size evolution. Int J Primatol 11:193–236

    Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://cran.r-project.org/

  • DiFiore A, Rendall D (1994) Evolution of social organization: a reappraisal for primates by using phylogenetic methods. Proc Natl Acad Sci U S A 91:9941–9945

    CAS  Google Scholar 

  • Dunbar RIM (1992) Neocortex size as a constraint on group size in primates. J Hum Evol 20:469–493

    Google Scholar 

  • Dunbar RIM (1996) Determinants of group size in primates: a general model. In: Runciman WG, Smith JM, Dunbar RIM (eds) Evolution of social behaviour patterns in primates and man. P Brit Acad, Vol. 88. Oxford University Press, New York, pp 33–57

    Google Scholar 

  • Dunbar RIM (1998) The social brain hypothesis. Evol Anthropol 6:178–190

    Google Scholar 

  • Eisenberg JF, Muckenhirn NA, Rudran R (1972) The relation between ecology and social structure in primates. Science 176:863–874

    PubMed  CAS  Google Scholar 

  • Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197:215–223

    PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Google Scholar 

  • Fleagle JG (1999) Primate adaptation and evolution, 2nd edn. Academic Press, San Diego

    Google Scholar 

  • Fleagle JG, Gilbert CC, Baden AL (2010) Primate cranial diversity. Am J Phys Anthropol 142:565–578

    PubMed  Google Scholar 

  • Foster SA, Endler JA (1999) Geographic variation in behavior: perspectives on evolutionary mechanisms. Oxford University Press, Oxford

    Google Scholar 

  • Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat 160:712–726

    PubMed  CAS  Google Scholar 

  • Ganzhorn JU, Klaus S, Ortmann S, Schmid J (2003) Adaptations to seasonality: some primate and nonprimate examples. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. Univ Chicago Press, Chicago, pp 132–144

    Google Scholar 

  • Garamszegi LZ (2011) Information-theoretic approaches to statistical analysis in behavioural ecology: an introduction. Behav Ecol Sociobiol 65:1–11

    Google Scholar 

  • Graham CH, Parra JL, Tinoco BA, Stiles G, McGuire JA (2012) Untangling the influence of ecological and evolutionary factors on trait variation across hummingbird assemblages. Ecology 93:S99–S111

    Google Scholar 

  • Harrison MJS (1983) Age and sex differences in the diet and feeding strategies of the green monkey, Cercopithecus sabaeus. Anim Behav 31:969–977

    Google Scholar 

  • Hemingway C, Bynum N (2005) The influence of seasonality on primate diet and ranging. In: Brockman DK, van Schaik CP (eds) Seasonality in primates: studies of living and extinct human and non-human primates. Cambridge University Press, Cambridge, pp 57–104

    Google Scholar 

  • Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978

    Google Scholar 

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

    Google Scholar 

  • Isler K, van Schaik CP (2009) The expensive brain: a framework for explaining evolutionary changes in brain size. J Hum Evol 57:392–400

    PubMed  Google Scholar 

  • Isler K, Kirk EC, Miller JMA, Albrecht GA, Gelvin BR, Martin RD (2008) Endocranial volumes of primate species: scaling analyses using a comprehensive and reliable dataset. J Hum Evol 55:967–978

    PubMed  Google Scholar 

  • Janson CH (1988) Food competition in brown capuchin monkeys (Cebus apella): quantitative effects of group size and tree productivity. Behaviour 105:53–76

    Google Scholar 

  • Janson CH (1992) Evolutionary ecology of primate social structure. In: Smith EA, Winterhalder B (eds) Evolutionary ecology and human behavior. Aldine de Gruyter, New York, pp 95–130

    Google Scholar 

  • Janson CH (2003) Puzzles, predation, and primates: using life history to understand selection pressures. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. University of Chicago Press, Chicago, pp 103–131

    Google Scholar 

  • Janson CH, Goldsmith ML (1995) Predicting group size in primates: foraging costs and predation risks. Behav Ecol 6:326–336

    Google Scholar 

  • Jolly CJ (1993) Species, subspecies, and baboon systematics. In: Kimbel WH, Martin LB (eds) Species, species concepts, and primate evolution. Plenum, New York, pp 67–107

    Google Scholar 

  • Kamilar JM (2006a) Geographic variation in primate behavior and ecology: from populations to communities. Dissertation, Stony Brook University

  • Kamilar JM (2006b) Geographic variation in savanna baboon (Papio) ecology and its taxonomic and evolutionary implications. In: Lehman SM, Fleagle JG (eds) Primate biogeography. Springer, New York, pp 169–200

    Google Scholar 

  • Kamilar JM, Atkinson QD (2014) Cultural assemblages show nested structure in humans and chimpanzees but not orangutans. Proc Natl Acad Sci U S A 111:111–115

    PubMed  CAS  PubMed Central  Google Scholar 

  • Kamilar JM, Beaudrot L (2013) Understanding primate communities: recent developments and future directions. Evol Anthropol 22:174–185

    PubMed  Google Scholar 

  • Kamilar JM, Cooper N (2013) Phylogenetic signal in primate behaviour, ecology, and life history. Phil Trans R Soc B 368:20120341

    PubMed  PubMed Central  Google Scholar 

  • Kamilar JM, Pokempner AA (2008) Does body mass dimorphism increase male–female dietary niche separation? A comparative study of primates. Behaviour 145:1211–1234

    Google Scholar 

  • Kamilar JM, Bribiescas RG, Bradley BJ (2010) Is group size related to longevity in mammals? Biol Lett 6:736–739

    PubMed  PubMed Central  Google Scholar 

  • Kamilar JM, Muldoon KM, Lehman SM, Herrera JP (2012) Testing Bergmann’s rule and the resource seasonality hypothesis in Malagasy primates using GIS-based climate data. Am J Phys Anthropol 147:401–408

    PubMed  Google Scholar 

  • Kamilar JM, Heesy CP, Bradley BJ (2013) Did trichromatic color vision and red hair color co-evolve in primates? Am J Primatol 75:740–751

    PubMed  Google Scholar 

  • Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23:707–740

    Google Scholar 

  • Kappeler PM, Watts DP (eds) (2012) Long-term field studies of primates. Springer, New York

    Google Scholar 

  • Kappeler PM, Barrett L, Blumstein DT, Clutton-Brock TH (2013) Constraints and flexibility in mammalian social behaviour: introduction and synthesis. Phil Trans R Soc B 368:20120337

    PubMed  PubMed Central  Google Scholar 

  • Koenig A (2002) Competition for resources and its behavioral consequences among female primates. Int J Primatol 23:759–783

    Google Scholar 

  • Lee PC (1999) Comparative primate socioecology. Cambridge University Press, New York

    Google Scholar 

  • Lee PC, Kappeler PM (2003) Socioecological correlates of phenotypic plasticity of primate life histories. In: Kappeler PM, Pereira ME (eds) Primate life histories and socioecology. The University of Chicago Press, Chicago, pp 41–65

    Google Scholar 

  • Lehmann J, Boesch C (2005) Bisexually bonded ranging in chimpanzees (Pan troglodytes verus). Behav Ecol Sociobiol 57:525–535

    Google Scholar 

  • Leyhausen P (1965) Communal organization of solitary mammals. Sym Zool S 14:249–263

    Google Scholar 

  • Lorenz K (1950) The comparative method in studying innate behavior patterns. Sym Soc Exp Biol 4:221–268

    Google Scholar 

  • Lorenz K (1970) Studies in animal and human behavior. Methuen, London

    Google Scholar 

  • Lukas D, Clutton-Brock TH (2013) The evolution of social monogamy in mammals. Science 341:526–530

    PubMed  CAS  Google Scholar 

  • Mayr E (1976) Evolution and the diversity of life. Harvard University Press, Cambridge

    Google Scholar 

  • Milton K (1988) Foraging behaviour and the evolution of primate intelligence. In: Byrne R, Whiten A (eds) Machiavellian intelligence. Clarendon Press, Oxford, pp 285–305

    Google Scholar 

  • Mittermeier RA, Louis EE, Richardson M, Schwitzer C, Langrand O et al (2010) Lemurs of Madagascar, 3rd edn. Conservation International, Washington D.C

    Google Scholar 

  • Moran N (1992) The evolutionary maintenance of alternative phenotypes. Am Nat 139:971–989

    Google Scholar 

  • Murphy PG, Lugo AE (1986) Ecology of tropical dry forest. Annu Rev Ecol Syst 17:67–88

    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

    Google Scholar 

  • Nunn CL (2011) The comparative method in evolutionary anthropology and biology. University of Chicago Press, Chicago

    Google Scholar 

  • Nunn CL, Altizer SM, Sechrest W, Cunningham AA (2005) Latitudinal gradients of parasite species richness in primates. Divers Distrib 11:249–256

    Google Scholar 

  • Oates JF (2013) Primate conservation: unmet challenges and the role of the international primatological society. Int J Primatol 34:235–245

    Google Scholar 

  • Oates JF, Whitesides GH, Davies AG, Waterman PG, Green SM, Dasilva GL, Mole S (1990) Determinants of variation in tropical forest primate biomass: new evidence from west Africa. Ecology 71:328–343

    Google Scholar 

  • Opie C, Atkinson QD, Dunbar RIM, Shultz S (2013) Male infanticide leads to social monogamy in primates. Proc Natl Acad Sci U S A 110:13328–13332

    PubMed  CAS  PubMed Central  Google Scholar 

  • Oring LW (1982) Avian mating systems. In: Farner DS, King JR, Parkes KC (eds) Avian biology. Academic Press, New York, pp 1–92

    Google Scholar 

  • Orme CDL, Freckleton RP, Thomas GH, Petzoldt T, Fritz SA, Isaac NJB (2012) caper: comparative analyses of phylogenetics and evolution in R, http://cran.r-project.org/web/packages/caper/index.html

  • Ossi KM, Kamilar JM (2006) Environmental and phylogenetic correlates of Eulemur behavior and ecology (Primates: Lemuridae). Behav Ecol Sociobiol 61:53–64

    Google Scholar 

  • Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–884

    PubMed  CAS  Google Scholar 

  • Papworth S, Milner-Gulland EJ, Slocombe K (2013) Hunted woolly monkeys (Lagothrix poeppigii) show threat-sensitive responses to human presence. PLoS One 8:e62000

    PubMed  CAS  PubMed Central  Google Scholar 

  • Reed KE, Bidner LR (2004) Primate communities: past, present, and possible future. Am J Phys Anthropol 47:2–39

    Google Scholar 

  • Revell LJ (2009) Size-correction and principal components for interspecific comparative studies. Evolution 63:3258–3268

    PubMed  Google Scholar 

  • Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 3:217–223

    Google Scholar 

  • Rose LM (1994) Sex differences in diet and foraging behavior in white-faced capuchins (Cebus capucinus). Int J Primatol 15:95–114

    Google Scholar 

  • Ross C, MacLarnon A (2000) The evolution of non-maternal care in anthropoid primates: a test of hypotheses. Folia Primatol 71:93–112

    PubMed  CAS  Google Scholar 

  • Rylands A, Mittermeier RA (2009) The diversity of the New World primates (Platyrrhini): an annotated taxonomy. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (eds) South American primates: comparative perspectives in the study of behavior, ecology, and conservation. Springer, New York, pp 23–54

    Google Scholar 

  • Schaffner CM, Rebecchini L, Ramos-Fernandez G, Vick LG, Aureli F (2012) Spider monkeys (Ateles geoffroyi yucatenensis) cope with the negative consequences of hurricanes through changes in diet, activity budget, and fission–fusion dynamics. Int J Primatol 33:922–936

    Google Scholar 

  • Shultz S, Opie C, Atkinson QD (2011) Stepwise evolution of stable sociality in primates. Nature 479:219–222

    PubMed  CAS  Google Scholar 

  • Snaith TV, Chapman CA (2007) Primate group size and interpreting socioecological models: do folivores really play by different rules? Evol Anthropol 16:94–106

    Google Scholar 

  • Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton

    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

    Google Scholar 

  • Strier KB (2009) Seeing the forest through the seeds: mechanisms of primate behavioral diversity from individuals to populations and beyond. Curr Anthropol 50:213–228

    PubMed  Google Scholar 

  • Struhsaker TT (1967) Social structure among vervet monkeys (Cercopithecus aethiops). Behaviour 29:83–121

    Google Scholar 

  • Struhsaker T (2000) Variation in adult sex ratios of red colobus monkey social groups: implications for interspecific comparisons. In: Kappeler PM (ed) Primate males: causes and consequences of variation in group composition. Cambridge University Press, Cambridge, pp 108–119

    Google Scholar 

  • Tecot SR, Baden AL, Romine N, Kamilar JM (2012) Infant parking and nesting, not allomaternal care, influence Malagasy primate life histories. Behav Ecol Sociobiol 66:1375–1386

    Google Scholar 

  • Teichroeb JA, Sicotte P (2009) Test of the ecological constraints model on ursine colobus monkeys (Colobus vellerosus) in Ghana. Am J Primatol 71:49–59

    PubMed  Google Scholar 

  • Terborgh J (1983) Five New World Primates: a study in comparative ecology. Princeton University Press, Princeton

    Google Scholar 

  • Terborgh J, Janson CH (1986) The sociobiology of primate groups. Annu Rev Ecol Syst 17:111–135

    Google Scholar 

  • Thierry B (2013) Identifying constraints in the evolution of primate societies. Philos T Roy Soc B 368:20120342

    Google Scholar 

  • Thierry B, Iwaniuk A, Pellis S (2000) The influence of phylogeny on the social behaviour of macaques (Primates: Cercopithecidae, genus Macaca). Ethology 106:713–728

    Google Scholar 

  • Tinbergen N (1963) On aims and methods in ethology. Z Tierpsychol 20:410–433

    Google Scholar 

  • van Schaik CP (1989) The ecology of social relationships amongst female primates. In: Standen V, Foley RA (eds) Comparative socioecology. Blackwell, Oxford, pp 195–218

    Google Scholar 

  • van Schaik CP, van Noordwijk MA, de Boer RJ, den Tonkelaar I (1983) The effect of group size on time budgets and social behaviour in wild long-tailed macaques (Macaca fascicularis). Behav Ecol Sociobiol 13:173–181

    Google Scholar 

  • Vasey N (2003) Varecia, ruffed lemurs. In: Goodman SM, Benstead JP (eds) The natural history of Madagascar. Univ Chicago Press, Chicago, pp 1332–1336

    Google Scholar 

  • Wills MA, Briggs DEG, Fortey RA (1994) Disparity as an evolutionary index: a comparison of Cambrian and recent arthropods. Paleobiology 20:93–130

    Google Scholar 

Download references

Acknowledgments

An earlier version of this paper benefited from discussions and/or comments from Charlie Janson, John Fleagle, Pat Wright, Charlie Nunn, Diane Doran, Andreas Koenig, Carola Borries, Chris Gilbert, Elise Huchard, and three anonymous reviewers. Jim Rohlf provided assistance with the statistical aspects of this research, especially exploring methods for calculating within-species variation. Thanks to E. Florendo and J. Ledogar for data entry assistance. This research was supported by an NSF DDIG grant (BCS-0452814) provided to JMK.

Author information

Authors and Affiliations

  1. Department of Anatomy, Arizona College of Osteopathic Medicine, Midwestern University, Glendale, AZ, 85308, USA

    Jason M. Kamilar

  2. School of Human Evolution and Social Change, Arizona State University, Tempe, AZ, 85287, USA

    Jason M. Kamilar

  3. Department of Anthropology, Hunter College of City University of New York, New York, NY, 10065, USA

    Andrea L. Baden

Authors
  1. Jason M. Kamilar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea L. Baden
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jason M. Kamilar.

Additional information

Communicated by E. Huchard

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(XLSX 51 kb)

ESM 2

(PDF 524 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kamilar, J.M., Baden, A.L. What drives flexibility in primate social organization?. Behav Ecol Sociobiol 68, 1677–1692 (2014). https://doi.org/10.1007/s00265-014-1776-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-014-1776-x

Keywords

Search

Navigation