Abstract
Socioecological theory predicts that larger groups are able to gain better access to resources because of their numerical advantage in intergroup contests. Nevertheless, the numerical superiority hypothesis has received mixed support, perhaps due to the collective action problem and sex differences in strategies and payoffs. We tested the numerical superiority and the collective action problem hypotheses using 141 intergroup encounters in a 7-year dataset on 5 groups of Verreaux’s sifaka (Propithecus verreauxi) at Ankoatsifaka Research Station in Kirindy Mitea National Park in western Madagascar. Contrary to the numerical superiority hypothesis, larger groups were not more likely to supplant smaller groups, nor was success determined by participation of a larger number of one sex. Consistent with a collective action problem, group size negatively affected participation. Notably, the sexes differed in which factors predicted individual participation. Male participation, which may serve to defend mating opportunities with resident females and signal competitive ability to neighboring groups, was greater than female participation, though we did not detect any strong predictor of male participation. Female participation was more likely during the lactation season, when food resources were scarce, than during the mating season. Contrary to previous studies, which argued that mothers with infants avoid intergroup conflicts because of the risk of infanticide, our study suggests that maternal energetic stress due to lactation and food scarcity increases the benefits of defending resources and instead drives mothers to participate in intergroup encounters. Thus, individual reproductive payoffs provide the private incentives needed to induce collective action.
Similar content being viewed by others
References
Abondano, L. A., Lewis, R. J., & Di Fiore, A. (2014). Does female dominance facilitate female mate choice? An examination of mate choice in Verreaux’s sifaka (Propithecus verreauxi). American Journal of Physical Anthropology, Suppl153, 201.
Arseneau, T. J. M., Taucher, A. L., van Schaik, C. P., & Willems, E. P. (2015). Male monkeys fight in between-group conflicts as protective parents and reluctant recruits. Animal Behaviour, 110, 39–50.
Arseneau-Robar, T. J. M., Taucher, A. L., Schnider, A. B., van Schaik, C. P., & Willems, E. P. (2017). Intra-and interindividual differences in the costs and benefits of intergroup aggression in female vervet monkeys. Animal Behaviour, 123, 129–137.
Bartoń, K. (2016). MuMIn: Multi-Model Inference. R Package Version, 1(15), 6.
Bates, D., Maechler, M., Bolker, B., & Walker, S. (2015). Fitting linear mixed-effects Models Using lme4. Journal of Statistical Software, 67(1), 1–48.
Beehner, J., & Kitchen, D. (2007). Factors affecting individual participation in group-level aggression among non-human primates. Behaviour, 144(12), 1551–1581.
Benadi, G., Fichtel, C., & Kappeler, P. (2008). Intergroup relations and home range use in Verreaux's sifaka (Propithecus verreauxi). American Journal of Primatology, 70(10), 956–965.
Bonanni, R., Valsecchi, P., & Natoli, E. (2010). Pattern of individual participation and cheating in conflicts between groups of free ranging dogs. Animal Behaviour, 97, 957–968.
Burnham, K. P., Anderson, D. R., & Huyvaert, K. P. (2011). AIC model selection and multimodel inference in behavioral ecology: Some background, observations, and comparisons. Behavioral Ecology and Sociobiology, 65(1), 23–35.
Cant, M. A., Otali, E., & Mwanguhya, F. (2002). Fighting and mating between groups in a cooperatively breeding mammal, the banded mongoose. Ethology, 108(6), 541–555.
Cheney, D. L., & Seyfarth, R. M. (1987). The influence of intergroup competition on the survival and reproduction of female vervet monkeys. Behavioral Ecology and Sociobiology, 21(6), 375–386.
Cords, M. (2007). Variable participation in the defense of communal feeding territories by blue monkeys in the Kakamega Forest, Kenya. Behaviour, 144(12), 1537–1550.
Core Team, R. (2016). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Crofoot, M. C., & Gilby, I. C. (2012). Cheating monkeys undermine group strength in enemy territory. Proceedings of the National Academy of Sciences of the USA, 109, 501–505.
Crofoot, M. C., Gilby, I. C., Wikelski, M. C., & Kays, R. W. (2008). Interaction location outweighs the competitive advantage of numerical superiority in Cebus capucinus intergroup contests. Proceedings of the National Academy of Sciences of the USA, 105(2), 577–581.
Crofoot, M. C., Rubenstein, D. I., Maiya, A. S., & Berger-Wolf, T. Y. (2011). Aggression, grooming and group-level cooperation in white-faced capuchins (Cebus capucinus): Insights from social networks. American Journal of Primatology, 73(8), 821–833.
Dormann, C. F., Elith, J., Bacher, S., Buchmann, C., Carl, G., et al (2013). Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography, 36, 27–46.
Fashing, P. J. (2001). Male and female strategies during intergroup encounters in guerezas (Colobus guereza): Evidence for resource defense mediated through males and a comparison with other primates. Behavioral Ecology and Sociobiology, 50(3), 219–230.
Graham, M. H. (2003). Confronting multicollinearity in ecological multiple regression. Ecology, 84(11), 2809–2815.
Grueter, C. C., Robbins, A. M., Abavandimwe, D., Vecellio, V., Ndagijimana, F., et al (2018). Quadratic relationships between group size and foraging efficiency in a herbivorous primate. Scientific Reports, 8(1), 16718.
Hrdy, S. B. (1974). Male-male competition and infanticide among the langurs (Presbytis entellus) of Abu, Rajasthan. Folia Primatologica, 22(1), 19–58.
Janson, C. H., & van Schaik, C. P. (1988). Recognizing the many faces of primate food competition: Methods. Behaviour, 105(1/2), 165–186.
Kappeler, P. M., & Schäffler, L. (2008). The lemur syndrome unresolved: Extreme male reproductive skew in sifakas (Propithecus verreauxi), a sexually monomorphic primate with female dominance. Behavioral Ecology and Sociobiology, 62(6), 1007–1015.
Kitchen, D., Seyfarth, R., & Cheney, D. (2004). Factors mediating inter-group encounters in savannah baboons (Papio cynocephalus ursinus). Behaviour, 141(2), 197–218.
Kitchen, D. M. (2004). Alpha male black howler monkey responses to loud calls: Effect of numeric odds, male companion behaviour and reproductive investment. Animal Behaviour, 67(1), 125–139.
Kitchen, D. M. (2006). Experimental test of female black howler monkey (Alouatta pigra) responses to loud calls from potentially infanticidal males: Effects of numeric odds, vulnerable offspring, and companion behavior. American Journal of Physical Anthropology, 131, 73–83.
Koch, F., Signer, J., Kappeler, P. M., & Fichtel, C. (2016a). Intergroup encounters in Verreaux’s sifakas (Propithecus verreauxi): Who fights and why? Behavioral Ecology and Sociobiology, 70(5), 797–808.
Koch, F., Signer, J., Kappeler, P. M., & Fichtel, C. (2016b). The role of the residence-effect on the outcome of intergroup encounters in Verreaux’s sifakas. Scientific Reports, 6, 28457.
Lawler, R. R. (2007). Fitness and extra-group reproduction in male Verreaux's sifaka: An analysis of reproductive success from 1989–1999. American Journal of Physical Anthropology, 132(2), 267–277.
Leimberger, K. G., & Lewis, R. J. (2017). Patterns of male dispersal in Verreaux's sifaka (Propithecus verreauxi) at Kirindy Mitea National Park. American Journal of Primatology, 79(7), e22455.
Lewis, R. J. (2004). Sources of variation in male–female relationships: Power, conflict, and cooperation. PhD dissertation, Duke University, Durham, NC.
Lewis, R. J. (2005). Sex differences in scent-marking in sifaka: Mating conflict or male services? American Journal of Physical Anthropology, 128(2), 389–398.
Lewis, R. J. (2006). Scent marking in sifaka: No one function explains it all. American Journal of Primatology, 68(6), 622–636.
Lewis, R. J. (2008). Social influences on group membership in Propithecus verreauxi verreauxi. International Journal of Primatology, 29, 1249–1270.
Lewis, R. J., & Axel, A. C. (2019). Using vegetation phenology and long-term demographic data to assess the impact of Cyclone Fanele on a lemur population in Madagascar. In A. Behie, J. Teichroeb, & N. Malone (Eds.), Primate research and conservation in the Anthropocene (pp. 216–236). Cambridge: Cambridge University Press.
Lewis, R. J., & Kappeler, P. M. (2005). Seasonality, body condition, and timing of reproduction in Propithecus verreauxi verreauxi in the Kirindy Forest. American Journal of Primatology, 67, 347–364.
Lewis, R. J., & Lawler, R. R. (2011). Verreaux’s sifaka. In N. Rowe & M. Myers (Eds.), All the world’s primates. Charlestown, RI: www.alltheworldsprimates.org. Primate Conservation Inc.
Lewis, R. J., Razafindrasamba, S. M., Tolojanahary, J. P. (2003). Observed infanticide in a seasonal breeding prosimian (Propithecus verreauxi verreauxi) in Kirindy Forest, Madagascar. Folia Primatologica 74(2):101–103. https://doi.org/10.1159/000070006.
Lewis, R. J., & van Schaik, C. P. (2007). Bimorphism in male Verreaux’s sifaka in the Kirindy Forest of Madagascar. International Journal of Primatology, 28, 159–182.
Littlefield, B. L. (2010). Infanticide following male takeover event in Verreaux’s sifaka (Propithecus verreauxi verreauxi). Primates, 51(1), 83–86.
Majolo, B., Ventura, R., & Koyama, N. F. (2005). Sex, rank and age differences in the Japanese macaque (Macaca fuscata yakui) participation in inter-group encounters. Ethology, 111(5), 455–468.
Majolo, B., deBortoli Vizioli, A., Martinez Inigo, L., & Lehmann, J. (2020). The effect of group size and individual characteristics on intergroup encounters in primates. International Journal of Primatology, 41(2). https://doi.org/10.1007/s10764-019-00119-5.
Markham, A. C., Alberts, S. C., & Altmann, J. (2012). Intergroup conflict: Ecological predictors of winning and consequences of defeat in a wild primate population. Animal Behaviour, 82(2), 399–403.
McComb, K., Packer, C., & Pusey, A. (1994). Roaring and numerical assessment in contests between groups of female lions, Panthera leo. Animal Behaviour, 47(2), 379–387.
Nakamichi, M., & Koyama, N. (1997). Social relationships among ring-tailed lemurs (Lemur catta) in two free-ranging troops at Berenty reserve, Madagascar. International Journal of Primatology, 18(1), 73–93.
Nunn, C. L. (2000). Collective benefits, free-riders, and male extra-group conflict. In P. M. Kappeler (Ed.), Primate males: Causes and consequences of variation in group composition (pp. 192–204). Cambridge: Cambridge University Press.
Nunn, C. L., & Deaner, R. O. (2004). Patterns of participation and free riding in territorial conflicts among ringtailed lemurs (Lemur catta). Behavioral Ecology and Sociobiology, 57(1), 50–61.
Nunn, C. L., & Lewis, R. J. (2001). Cooperation and collective benefits: Applying economic models of collective action to animal behavior. In R. Noë, J. A. R. A. M. van Hooff, & P. Hammerstein (Eds.), Economics in nature: Social dilemmas, mate choice and biological markets (pp. 42–66). Cambridge: Cambridge University Press.
Rasambainarivo, F. T., Junge, R. E., & Lewis, R. J. (2014). Biomedical evaluation of Verreaux’s sifaka (Propithecus verreauxi) from Kirindy Mitea National Park in Madagascar. Journal of Zoo and Wildlife Medicine, 45(2), 247–255.
Richard, A. F. (1978). Behavioral variation: Case study of a Malagasy lemur. Lewisburg, PA: Bucknell University Press.
Richard, A. F., & Nicoll, M. E. (1987). Female social dominance and basal metabolism in a Malagasy primate, Propithecus verreauxi. American Journal of Primatology, 12, 309–314.
Richard, A. F., Rakotomanga, P., & Schwartz, M. (1991). Demography of Propithecus verreauxi at Beza Mahafali, Madagascar: Sex ratio, survival, and fertility. American Journal of Physical Anthropology, 84, 307–322.
Richard, A. F., Rakotomanga, P., & Schwartz, M. (1993). Dispersal by Propithecus verreauxi at Beza Mahafaly, Madagascar: 1984–1991. American Journal of Primatology, 30, 1–20.
Scarry, C. J. (2013). Between-group contest competition among tufted capuchin monkeys, Sapajus nigritus, and the role of male resource defence. Animal Behavior, 85(5), 931–939.
Sussman, R. W., Richard, A. F., Ratsirarson, J., Sauther, M. L., Brockman, D. K., et al (2012). Beza Mahafaly Special Reserve: Long-term research on lemurs in Southwestern Madagascar. In P. M. Kappeler & D. P. Watts (Eds.), Long-term field studies of primates (pp. 45–66). Berlin and Heidelberg: Springer.
Symonds, M. R., & Moussalli, A. (2011). A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behavioral Ecology and Sociobiology, 65(1), 13–21.
Teichroeb, J. A., & Sicotte, P. (2018). Cascading competition: The seasonal strength of scramble influences between-group contest in a folivorous primate. Behavioral Ecology and Sociobiology, 72(1), 6.
Trivers, R. L. (1972). Parental Investment and sexual selection. In B. Campbell (Ed.), Sexual selection and the descent of man 1871–1971 (pp. 136–179). Chicago: Aldine.
Van Belle, S. (2015). Female participation in collective group defense in black howler monkeys (Alouatta pigra). American Journal of Primatology, 77(6), 595–604.
Van Belle, S., & Scarry, C. J. (2015). Individual participation in intergroup contests is mediated by numerical assessment strategies in black howler and tufted capuchin monkeys. Philosophical Transactions of the Royal Society, B: Biological Sciences, 370(1683), 20150007.
Van Belle, S., Garber, P. A., Estrada, A., & Di Fiore, A. (2014). Social and genetic factors mediating male participation in collective group defence in black howler monkeys. Animal Behaviour, 98, 7–17.
van Schaik, C. P. (1989). The ecology of social relationships amongst female primates. In V. Standen & R. A. Foley (Eds.), Comparative socioecology: The behavioral ecology of humans and other mammals (pp. 195–218). Oxford: Blackwell.
van Schaik, C. P. (1996). Social evolution in primates: The role of ecological factors and male behaviour. Proceedings of the British Academy, 88, 9–31.
Voyt, R. A., Sandel, A. A., Ortiz, K. M., & Lewis, R. J. (2019). Female power in Verreaux's sifaka (Propithecus verreauxi) is based on maturity, not size. International Journal of Primatology, 40, 417–434.
Willems, E. P., Hellriegel, B., & van Schaik, C. P. (2013). The collective action problem in primate territory economics. Proceedings of the Royal Society of London B: Biological Sciences, 280, 20130081.
Willems, E. P., Arseneau, T. J. M., Schleuning, X., & van Schaik, C. P. (2015). Communal range defence in primates as a public goods dilemma. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 370, 20150003.
Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 262–300.
Zhao, Q., & Tan, C. L. (2011). Inter-unit contests within a provisioned troop of Sichuan snub nosed monkeys (Rhinopithecus roxellana) in the Qinling Mountains, China. American Journal of Primatology, 73(3), 262–269.
Acknowledgements
We would like to thank Sarie Van Belle, Takeshi Furiuchi, and Cyril Grueter for inviting us to participate in their symposium. The manuscript benefited greatly from suggestions by Takeshi Furiuchi, Jo Setchell, and two anonymous reviewers. This research would not have been possible without the Sifaka Research Project assistants at the Ankoatsifaka Research Station, whose work provided the majority of the data analyzed here. We thank the Madagascar government and Madagascar National Parks for permission to conduct this research and the University of Antananarivo and MICET for facilitating the field component of our research. Our research was financed by the University of Texas at Austin, the Leakey Foundation, Primate Conservation, Inc., and multiple private donors.
Author information
Authors and Affiliations
Contributions
RJL conceived, designed, and funded the project, as well as conducted fieldwork and wrote the manuscript; AAS analyzed the data and wrote the manuscript; SH and SEB entered and analyzed data and contributed to writing the manuscript.
Corresponding author
Additional information
Handling Editor: Takeshi Furuichi
Electronic Supplementary Material
ESM 1
(XLSX 161 kb)
Rights and permissions
About this article
Cite this article
Lewis, R.J., Sandel, A.A., Hilty, S. et al. The Collective Action Problem but Not Numerical Superiority Explains Success in Intergroup Encounters in Verreaux’s Sifaka (Propithecus verreauxi): Implications for Individual Participation and Free-Riding. Int J Primatol 41, 305–324 (2020). https://doi.org/10.1007/s10764-020-00155-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10764-020-00155-6