The Temporal Scale of Behavioural and Demographic Flexibility: Implications for Comparative Analyses and Conservation

  • Karen B. StrierEmail author
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


Many primate species exhibit high levels of behavioural variation that correlate with demographic variance across populations and within populations over time. Analyses of these relationships have typically treated behavioural variance as the product of individual responses to local ecological and demographic conditions and therefore indicative of behavioural flexibility. However, in contrast to the extrinsic nature of the variance in ecological conditions such as climate, food availability, or predation pressure, demographic variance can reflect both extrinsic processes and intrinsic properties of individual life histories, such as the timing and rate of fertility and dispersal decisions. If we follow the rationale for interpreting behavioural flexibility, then demographic flexibility would correspondingly reflect the responses of components of individual life histories that are free to vary to external stimuli. The dynamics between behavioural and demographic flexibility can shift over the course of individual lifespans and are expected to affect the size and composition of groups and populations and therefore levels of intrasexual competition and many other features of sociality. These dynamics also affect group and population growth rates, with implications for the recovery and management of small populations and the resilience of large populations subject to rapidly or unpredictably changing conditions. Longitudinal and cross-sectional data from the critically endangered northern muriqui (Brachyteles hypoxanthus) and other primate species provide comparative insights into patterns of behavioural and demographic flexibility that can advance our understanding of primate adaptive potentials and constraints over ecological and evolutionary time.


Behavioural variation Demographic variation Dispersal Interbirth interval Fertility 



I thank Jeremy Hogan and other members of the planning committee for inviting me to participate in the Festschrift honouring Linda Fedigan in December 2016, where an earlier version of this paper was presented. I am also grateful to the editors of this volume and especially my editor, Kathy Jack, and to Louise Barrett and Phyllis Lee for their helpful comments as external reviewers. The muriqui data presented in this chapter were collected with permission from the Brazilian government (CNPq) and the Sociedade Preserve Muriqui, in collaboration with Dr. Sérgio Lucena Mendes, and with support from Conservation International and CI-Brasil. Many funding sources have financed parts of the fieldwork, and many people have contributed to the long-term demographic data; please see these acknowledgements at my website,


  1. Alberts SC, Altmann J, Brockman DK et al (2013) Reproductive aging patterns in primates reveal that humans are distinct. Proc Natl Acad Sci U S A 110(33):13440–13445CrossRefGoogle Scholar
  2. Aureli F, Schaffner CM, Boesch C et al (2008) Fission-fusion dynamics: new research frameworks. Curr Anthropol 49:627–654Google Scholar
  3. Barrett L, Halliday J, Henzi SP (2006a) The ecology of motherhood: the structuring of lactation costs by chacma baboons. J Anim Ecol 75:875–886CrossRefGoogle Scholar
  4. Barrett L, Henzi SP, Lycett JE (2006b) Whose life is it anyway? Maternal investment, developmental trajectories, and life history strategies in baboons. In: Swedell L, Leigh SR (eds) Reproduction and fitness in baboons: behavioral, ecological, and life history perspectives. Springer, New York, pp 199–224CrossRefGoogle Scholar
  5. Boubli JP, Couto-Santos F, Strier KB (2011) Structure and floristic composition of one of the last forest fragments containing the critically endangered northern muriqui (Brachyteles hypoxanthus, primates). Ecotropica 17(2):53–69Google Scholar
  6. Brasington LF, Wikberg EC, Kawamura S et al (2017) Infant mortality in white-faced capuchins: the impact of alpha male replacements. Am J Primatol.
  7. Brockman DK, Van Schaik CP (2005) Seasonality and reproductive function. 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 269–309CrossRefGoogle Scholar
  8. Bronikowski AM, Cords M, Alberts SC et al (2016) Female and male life tables for seven wild primate species. Sci Data 3:160006CrossRefGoogle Scholar
  9. Campos FA (2018, this volume) A synthesis of long-term environmental change in Santa Rosa, Costa Rica. In: Kalbitzer U, Jack KM (eds) Primate life histories, sex roles, and adaptability - essays in honour of Linda M. Fedigan. Developments in primatology: progress and prospects. Springer, New York, pp 331–354Google Scholar
  10. Campos FA, Jack KM, Fedigan LM (2015) Climate oscillations and conservation measures regulate white-faced population growth and demography in a regenerating tropical dry forest in Costa Rica. Biol Conserv 186:204–221CrossRefGoogle Scholar
  11. Campos FA, Morris WF, Alberts SC et al (2017) Does climate variability influence the demography of wild primates? Evidence from long-term life-history data in seven species. Glob Change Biol.
  12. Chapman CA, Chapman LJ (2000) Constraints on group size in redtail monkeys and red colobus: testing the generality of the ecological constraints model. Int J Primatol 21:565–585CrossRefGoogle Scholar
  13. Chapman CA, Rothman JM (2009) Within-species differences in primate social structure: evolution of plasticity and phylogenetic constraints. Primates 50(1):12–22CrossRefGoogle Scholar
  14. Chaves PB, Alvarenga CS, Possamai CB et al (2011) Genetic diversity and population history of a critically endangered primate, the northern muriqui (Brachyteles hypoxanthus). PLoS ONE 6(6):e20722CrossRefGoogle Scholar
  15. Di Fiore A, Rendall D (1994) Evolution of social organization: a reappraisal for primates by using phylogenetic methods. Proc Natl Acad Sci U S A 91:9941–9945CrossRefGoogle Scholar
  16. Dias LG, Strier KB (2003) Effects of group size on ranging patterns in Brachyteles arachnoides hypoxanthus. Int J Primatol 24:209–221CrossRefGoogle Scholar
  17. Dingemanse NJ, Wolf M (2013) Between-individual differences in behavioural plasticity within populations: causes and consequences. Anim Behav 85(5):1031–1039CrossRefGoogle Scholar
  18. Dobson AP, Lyles AM (1989) The population dynamics and conservation of primate populations. Conserv Biol 3:362–380CrossRefGoogle Scholar
  19. Emery Thompson M, Muller MN, Wrangham RW et al (2009) Urinary C-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees. Horm Behav 55(2):299–305CrossRefGoogle Scholar
  20. Emery Thompson M, Muller MN, Wrangham RW (2012) The energetics of lactation and the return to fecundity in wild chimpanzees. Behav Ecol 23(6):1234–1241CrossRefGoogle Scholar
  21. Erhart EM, Overdorff DJ (2008) Population demography and social structure changes in Eulemur fulvus rufus from 1988 to 2003. Am J Phys Anthropol 136:183–193CrossRefGoogle Scholar
  22. Fedigan LM, Jack KM (2012) Tracking neotropical monkeys in Santa Rosa: lessons from a regenerating Costa Rican dry forest. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer-Verlag, Berlin, pp 165–184CrossRefGoogle Scholar
  23. Fedigan LM, Rose LM (1995) Interbirth interval variation in three sympatric species of neotropical monkey. Am J Primatol 37:9–24CrossRefGoogle Scholar
  24. Fedigan LM, Rose LM, Avila RM (1996) See how they grow: tracking capuchin monkey (Cebus capucinus) populations in a regenerating Costa Rican dry forest. In: Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiations of neotropical primates. Plenum Press, New York, pp 289–307CrossRefGoogle Scholar
  25. Fedigan LM, Carnegie SD, Jack K (2008) Predictors of reproductive success in female white-faced capuchins (Cebus capucinus). Am J Phys Anthropol 137:82–90CrossRefGoogle Scholar
  26. Forsman A (2015) Rethinking phenotypic plasticity and its consequences for individuals, populations and species. Heredity 115(4):276–284CrossRefGoogle Scholar
  27. Franklin IR (1980) Evolutionary change in small populations. In: Soule ME, Wilcox BA (eds) Conservation biology, an evolutionary-ecological perspective. Sinauer Associates, Sunderland, pp 135–149Google Scholar
  28. Gillespie TR, Chapman CA (2001) Determinants of group size in the red colobus monkey (Procolobus badius): an evaluation of the generality of the ecological-constraints model. Behav Ecol Sociobiol 50:329–338CrossRefGoogle Scholar
  29. Gilpin ME, Soule ME (1986) Minimum viable populations: processes of species extinction. In: Soule ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer Associates, Sunderland, pp 19–34Google Scholar
  30. Gogarten JF, Brown LM, Chapman CA et al (2012) Seasonal mortality patterns in non-human primates: implications for variation in selection pressures across environments. Evolution 66(10):3252–3266CrossRefGoogle Scholar
  31. Gogarten JF, Bonnell TR, Brown LM et al (2014) Increasing group size alters behavior of a folivorous primate. Int J Primatol 35(2):590–608CrossRefGoogle Scholar
  32. Gogarten JF, Jacob AJ, Ghai RR et al (2015) Group size dynamics over 15+ years in an African forest primate community. Biotropica 47:101–112CrossRefGoogle Scholar
  33. Guedes D, Young RJ, Strier KB (2008) Energetic costs of reproduction in female northern muriquis, Brachyteles hypoxanthus (Primates: Platyrrhini: Atelidae). Rev Brasil Zool 25:587–593CrossRefGoogle Scholar
  34. Isbell LA (1991) Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behav Ecol 2:143–155CrossRefGoogle Scholar
  35. Jack KM, Fedigan LM (2018, this volume) Alpha male capuchins (Cebus capucinus imitator) as keystone individuals in: Kalbitzer U, Jack KM (eds) Primate life histories, sex roles, and adaptability - essays in honour of Linda M. Fedigan. Developments in primatology: progress and prospects. Springer, New York, pp 91–109Google Scholar
  36. Kalbitzer U, Bergstrom ML, Carnegie SD et al (2017) Female sociality and sexual conflict shape offspring survival in a neotropical primate. Proc Natl Acad Sci U S A 114(8):1892–1897CrossRefGoogle Scholar
  37. Kamilar JM, Baden AL (2014) What drives flexibility in primate social organization? Behav Ecol Sociobiol 68:1677–1692CrossRefGoogle Scholar
  38. Kappeler PM, Kraus C (2010) Levels and mechanisms of behavioural variability. In: Kappeler PM (ed) Animal behaviour: evolution and mechanisms. Springer, New York, pp 655–684CrossRefGoogle Scholar
  39. Knott CD (1998) Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability. Int J Primatol 19(6):1061–1079CrossRefGoogle Scholar
  40. Lee PC (1996) The meanings of weaning: growth, lactation and life history. Evol Anthropol 5:87–96CrossRefGoogle Scholar
  41. Lee PC (1999) Comparative ecology of postnatal growth and weaning among haplorhine primates. In: Lee PC (ed) Comparative primate socioecology. Cambridge University Press, Cambridge, pp 111–136CrossRefGoogle Scholar
  42. Lee PC, Kappeler P (2003) Socio-ecological correlates of phenotypic plasticity in primate life history. In: Kappeler PM, Pereira M (eds) Primate life histories. University of Chicago Press, Chicago, pp 41–65Google Scholar
  43. Lee PC, Strier KB (2015) Complexities of understanding female dispersal in primates. In: Furuichi T, Aureli F, Yamagiwa J (eds) Dispersing primate females. Springer, Tokyo, pp 215–230CrossRefGoogle Scholar
  44. Maldonado-Chaparro AA, Read DW, Blumstein DT (2017) Can individual variation in phenotypic plasticity enhance population viability? Ecol Model 352:19–30CrossRefGoogle Scholar
  45. Mendes SL, Melo FR, Boubli JP et al (2005) Directives for the conservation of the northern muriqui, Brachyteles hypoxanthus (Primates, Atelidae). Neotrop Primates 13(Supplement):7–18Google Scholar
  46. Moore J (1999) Population density, social pathology, and behavioral ecology. Primates 40:5–26CrossRefGoogle Scholar
  47. Morris WF, Altmann J, Brockman DK et al (2011) Low demographic variability in wild primate populations: fitness impacts of variation, covariation, and serial correlation in vital rates. Am Nat 177(1):E14–E28CrossRefGoogle Scholar
  48. Myers N, Mittermeier RA, Mittermeier CG et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858CrossRefGoogle Scholar
  49. Printes RC, Strier KB (1999) Behavioral correlates of dispersal in female muriquis (Brachyteles arachnoides). Int J Primatol 20:941–960CrossRefGoogle Scholar
  50. Rudran R, Fernandez-Duque E (2003) Demographic changes over thirty years in a red howler population in Venezuela. Int J Primatol 24:925–947CrossRefGoogle Scholar
  51. Saccheri I, Hanski I (2006) Natural selection and population dynamics. Trends Ecol Evol 21:341–347CrossRefGoogle Scholar
  52. Saether BE, Coulson T, Grotan V et al (2013) How life history influences population dynamics in fluctuating environments. Am Nat 182(6):743–759CrossRefGoogle Scholar
  53. Shaffer ML (1981) Minimum population sizes for species conservation. Bioscience 31:131–134CrossRefGoogle Scholar
  54. Snell-Rood EC (2013) An overview of the evolutionary causes and consequences of behavioural plasticity. Anim Behav 85(5):1004–1011CrossRefGoogle Scholar
  55. Strier KB (1999a) Faces in the forest: the endangered muriqui monkeys of Brazil. Harvard University Press, Cambridge, MAGoogle Scholar
  56. Strier KB (1999b) Predicting primate responses to “stochastic” demographic events. Primates 40:131–142CrossRefGoogle Scholar
  57. Strier KB (2000) Population viabilities and conservation implications for muriquis (Brachyteles arachnoides) in Brazil's Atlantic forest. Biotropica 32:903–913Google Scholar
  58. Strier KB (2003) Demography and the temporal scale of sexual selection. In: Jones CB (ed) Sexual selection and reproductive competition in primates: new perspectives and directions. American Society of Primatologists, Norman, pp 45–63Google Scholar
  59. Strier KB (2004) Reproductive strategies of New World primates: interbirth intervals and reproductive rates. In: Mendes SL, Chiarello AG (eds) A primatologia no Brasil-8. IPEMA/Sociedade Brasileiro de Primatologia, Vitoria/Espirito Santo, pp 53–63Google Scholar
  60. Strier KB (2008) The effects of kin on primate life histories. Annu Rev Anthropol 37:21–36CrossRefGoogle Scholar
  61. Strier KB (2009) Seeing the forest through the seeds: mechanisms of primate behavioral diversity from individuals to populations and beyond. Curr Anthropol 50:213–228CrossRefGoogle Scholar
  62. Strier KB (2011) Social plasticity and demographic variation in primates. In: Sussman RW, Cloninger CR (eds) The origins and nature of cooperation and altruism in non-human and human primates. Springer, New York, pp 179–192Google Scholar
  63. Strier KB (2017) What does variation in primate behavior mean? Am J Phys Anthropol 162(S63):4–14CrossRefGoogle Scholar
  64. Strier KB, Boubli JP (2006) A history of long-term research and conservation of northern muriquis (Brachyteles hypoxanthus) at the Estação Biológica de Caratinga/RPPN-FMA. Primate Conserv 20:53–63CrossRefGoogle Scholar
  65. Strier KB, Ives AR (2012) Unexpected demography in the recovery of an endangered primate population. PLoS One 7(9):e44407CrossRefGoogle Scholar
  66. Strier KB, Mendes SL (2012) The northern muriqui (Brachyteles hypoxanthus): lessons on behavioral plasticity and population dynamics from a critically endangered primate. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer-Verlag, Berlin, pp 125–140CrossRefGoogle Scholar
  67. Strier KB, Ziegler TE (1997) Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys, Brachyteles arachnoides. Am J Primatol 42(4):299–310CrossRefGoogle Scholar
  68. Strier KB, Ziegler TE (2000) Lack of pubertal influences on female dispersal in muriqui monkeys (Brachyteles arachnoides). Anim Behav 59:849–860CrossRefGoogle Scholar
  69. Strier KB, Mendes FDC, Rímoli J et al (1993) Demography and social structure in one group of muriquis (Brachyteles arachnoides). Int J Primatol 14:513–526CrossRefGoogle Scholar
  70. Strier KB, Ziegler TE, Wittwer DJ (1999) Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoides). Horm Behav 35(2):125–134CrossRefGoogle Scholar
  71. Strier KB, Carvalho DS, Bejar NO (2001a) Prescription for peacefulness. In: Aureli F, de Waal FBM (eds) Natural conflict resolution. Harvard University Press, Cambridge, MA, pp 315–317Google Scholar
  72. Strier KB, Mendes SL, Santos RR (2001b) Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus). Am J Primatol 55(2):87–100CrossRefGoogle Scholar
  73. Strier KB, Boubli JP, Possamai CB et al (2006) Population demography of northern muriquis (Brachyteles hypoxanthus) at the Estação Biológica de Caratinga/Reserva particular do Patrimônio natural-Feliciano Miguel Abdala, Minas Gerais, Brazil. Am J Phys Anthropol 130:227–237CrossRefGoogle Scholar
  74. Strier KB, Altmann J, Brockman DK et al (2010) The primate life history database: a unique shared ecological data resource. Methods Ecol Evol 1:199–210CrossRefGoogle Scholar
  75. Strier KB, Chaves PB, Mendes SL et al (2011) Low paternity skew and the influence of maternal kin in an egalitarian, patrilocal primate. Proc Natl Acad Sci U S A 108(47):18915–18919CrossRefGoogle Scholar
  76. Strier KB, Lee PC, Ives AR (2014) Behavioral flexibility and the evolution of primate social states. PLoS One 9(12):e114099CrossRefGoogle Scholar
  77. Strier KB, Possamai CB, Mendes SL (2015) Dispersal patterns of female northern muriquis: implications for social dynamics, life history, and conservation. In: Furuichi T, Aureli F, Yamagiwa J (eds) Dispersing primate females. Springer, Tokyo, pp 3–22CrossRefGoogle Scholar
  78. Struhsaker TT (2008) Demographic variability in monkeys: implications for theory and conservation. Int J Primatol 29:19–34CrossRefGoogle Scholar
  79. Tabacow FP, Mendes SL, Strier KB (2009) Spread of a terrestrial tradition in an arboreal primate. Am Anthropol 111:238–249CrossRefGoogle Scholar
  80. Tokuda M, Boubli JP, Mourthé I et al (2014) Males follow females during fissioning of a group of northern muriquis. Am J Primatol 76:529–538CrossRefGoogle Scholar
  81. van Noordwijk MA, van Schaik CP (2005) Development of ecological competence in Sumatran orangutans. Am J Phys Anthropol 127:79–94CrossRefGoogle Scholar
  82. Wong BBM, Candolin U (2015) Behavioral responses to changing environments. Behav Ecol 26(3):665–673CrossRefGoogle Scholar
  83. Xiang Z, Yang W, Qi X et al (2017) An examination of factors potentially influencing birth distributions in golden snub-nosed monkeys (Rhinopithecus roxellana). PeerJ 5:e2892CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of Wisconsin-MadisonMadisonUSA

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