Abstract
We use two novel techniques to analyze association patterns in a group of wild spider monkeys (Ateles geoffroyi) studied continuously for 8 years. Permutation tests identified association rates higher or lower than chance expectation, indicating active processes of companionship and avoidance as opposed to passive aggregation. Network graphs represented individual adults as nodes and their association rates as weighted edges. Strength and eigenvector centrality (a measure of how strongly linked an individual is to other strongly linked individuals) were used to quantify the particular role of individuals in determining the network's structure. Female–female dyads showed higher association rates than any other type of dyad, but permutation tests revealed that these associations cannot be distinguished from random aggregation. Females formed tightly linked clusters that were stable over time, with the exception of immigrant females who showed little association with any adult in the group. Eigenvector centrality was higher for females than for males. Adult males were associated mostly among them, and although their strength of association with others was lower than that of females, their association rates revealed a process of active companionship. Female–male bonds were weaker than those between same-sex pairs, with the exception of those involving young male adults, who by virtue of their strong connections both with female and male adults, appear as temporary brokers between the female and male clusters of the network. This analytical framework can serve to develop a more complete explanation of social structure in species with high levels of fission–fusion dynamics.
Similar content being viewed by others
References
Asensio N, Korstjens AH, Schaffner CM, Aureli F (2008) Intragroup aggression, fission-fusion dynamics and feeding competition in spider monkeys. Behaviour 145:983–1001
Aureli F, Schaffner CM (2008) Social interactions, social relationships and the social system of spider monkeys. Chapter 9. In: Campbell CJ (ed) Spider monkeys: behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge
Aureli F, Schaffner C, Boesch C, Bearder SK, Call J, Chapman CA, Connor R, DiFiore A, Dunbar RIM, Henzi PS, Holekamp K, Korstjens AH, Layton R, Lee P, Lehmann J, Manson JH, Ramos-Fernandez G, Strier KB, van Schaik CP (2008) Fission–fusion dynamics: new research frameworks. Curr Anthropol 49:627–654
Bedjer L, Fletcher D, Brager S (1998) A method for testing association patterns of social animals. Anim Behav 56:719–725
Bernstein IS (1981) Dominance: the baby and the bathwater. Behav Brain Sci 4:419–457
Borgatti SP (2002) NetDraw: Graph Visualization Software Harvard: Analytic Technologies
Cairns SJ, Schwager SJ (1987) A comparison of association indices. Anim Behav 35:1454–1469
Chapman CA (1990) Association patterns of spider monkeys: the influence of ecology and sex on social organization. Behav Ecol Sociobiol 26:409–414
Croft DP, Krause J, James R (2004) Social networks in the guppy (Poecilia reticulata). Proc R Soc Lond B (Suppl) 271:S516–S519
De Waal FBM (1987) Dynamics of social relationships. Chapter 34. In: Smuts B, Cheney D, Seyfarth R, Wrangham R, Struhsaker T (eds) Primate societies. University of Chicago Press, Chicago
Fedigan LM, Baxter MJ (1984) Sex differences and social organization in free-ranging spider monkeys (Ateles geoffroyi). Primates 25:279–294
García-Frapolli E, Ayala-Orozco B, Bonilla-Moheno M, Espadas-Manrique C, Ramos-Fernandez G (2007) Biodiversity conservation, traditional agriculture and ecotourism: Land cover/land use change projections for a natural protected area in the northeastern Yucatan Peninsula, Mexico. Land Urb Plan 83:137–153
Gowans S, Whitehead H, Hooker SK (2001) Social organization in northern bottlenose whales, Hyperoodon ampullatus: not driven by deep-water foraging? Anim Behav 62:369–377
Granovetter MS (1973) The strength of weak ties. Am J Sociol 78:1360–1380
Henzi P, Lusseau D, Weingrill T, van Schaik C, Barrett L (2009) Cyclicity in the structure of female baboon social networks. Behav Ecol Sociobiol. doi:10.1007/s00265-009-0720-y
Hinde RA (1976) Interactions, relationships and social structure. Man (New Series) 11:1–17
James R, Croft DP, Krause J (2009) Potential banana skins in animal social network analysis. Behav Ecol Sociobiol. doi:10.1007/s00265-009-0742-5
Kappeler PM, van Schaik CP (2002) Evolution of primate social systems. Int J Primatol 23:707–740
Klein LL (1972) The ecology and social organization of spider monkeys Ateles belzebuth. PhD Thesis, University of California, Berkeley
Krause J, Lusseau D, James R (2009) Animal social networks: an introduction. Behav Ecol Sociobiol. doi:10.1007/s00265-009-0747-0
Lusseau D, Newman MEJ (2004) Identifying the role that animals play in their social networks. Proc R Soc Lond B (Suppl) 271:S477–S481
Mann J, Connor RC, Tyack PL, Whitehead H (2000) Cetacean societies: field studies of dolphins and whales. University of Chicago Press, Chicago
Newman MEJ (2003) The structure and function of complex networks. SIAM Review 45:167–256
Newman MEJ (2004) Analysis of weighted networks. Phys Rev E 70:056131
Owen ECG, Wells RS, Hofmann S (2002) Ranging and association patterns of paired and unpaired adult male Atlantic bottlenose dolphins, Tursiops truncatus, in Sarasota, Florida, provide no evidence for alternative male strategies. Can J Zool 80:2072–2089
Ramos-Fernandez G (2001) Patterns of association, feeding competition and vocal communication in spider monkeys, Ateles geoffroyi. PhD dissertation, University of Pennsylvania
Ramos-Fernandez G (2005) Vocal communication in a fission-fusion society: do spider monkeys stay in touch with close associates? Int J Primatol 26:1077–1092
Ramos-Fernandez G, Ayala-Orozco B (2003) Population size and habitat use of spider monkeys in Punta Laguna, Mexico. In: Marsh LK (ed) Primates in fragments: ecology and conservation. Kluwer, New York
Ramos-Fernandez G, Vick LG, Aureli F, Schaffner C, Taub DM (2003) Behavioral ecology and conservation status of spider monkeys in the Otoch ma'ax yetel kooh protected area. Neotrop Primates 11:157–160
Ramos-Fernandez G, Boyer D, Gómez VP (2006) A complex social structure with fission-fusion properties can emerge from a simple foraging model. Behav Ecol and Sociobiol 60:536–549
Shimooka Y, Campbell C, DiFiore A, Felton A, Izawa K, Nishimura A, Ramos-Fernandez G, Wallace R (2008) Demography and group composition of Ateles. In: Campbell CJ (ed) Spider monkeys: behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge
Slater KY, Schaffner CM, Aureli F (2007) Embraces for infant handling in spider monkeys: evidence for a biological market? Anim Behav 74:455–461
Smuts B, Cheney D, Seyfarth R, Wrangham R, Struhsaker T (eds) (1987) Primate societies. The University of Chicago Press, Chicago
Sugardjito J, te Boekhorst IJA, van Hooff JARAM (1987) Ecological constraints on the grouping of wild orang-utans (Pongo pygmaeus) in the Gunung Leuser National Park, Sumatra, Indonesia. Int J Primatol 8:17–41
Symington MM (1987) Ecological correlates of party size in the black spider monkey, Ateles paniscus chamek. PhD thesis, Princeton University
Valero A, Schaffner CM, Vick LG, Aureli F, Ramos-Fernández G (2006) Intragroup lethal aggression in wild spider monkeys. Amer J Primatol 68:732–737
Vick LG (2008) Immaturity in spider monkeys: a risky business Chapter 11. In: Campbell CJ (ed) Spider Monkeys Behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge
Vonhof MJ, Whitehead H, Fenton MB (2004) Analysis of Spix's disc-winged bat association patterns and roosting home ranges reveal a novel social structure among bats. Anim Behav 68:507–521
Whitehead H (1995) Investigating structure and temporal scale in social organizations using identified individuals. Behav Ecol 6:199–208
Whitehead H (1997) Analyzing animal social structure. Anim Behav 53:1053–1067
Whitehead H (1999) Testing association patterns of social animals. Anim Behav 57:26–27
Whitehead H (2008) Analyzing animal societies: quantitative methods for vertebrate social analysis. University of Chicago Press, Chicago
Whitehead H (2009) SOCPROG programs: analyzing animal social structures. Behav Ecol Sociobiol 63:765–778. doi:10.1007/s00265-008-0697-y
Whitehead H, Dufault S (1999) Techniques for analyzing vertebrate social structure using identified individuals: review and recommendations. Adv Stud Behav 28:33–74
Whitehead H, Bejder L, Ottensmeyer AC (2005) Testing association patterns: issues arising and extensions. Anim Behav 69:e1–e6
Wittemyer G, Douglas-Hamilton I, Getz WM (2005) The socioecology of elephants: analysis of the processes creating multitiered social structures. Anim Behav 69:1357–1371
Acknowledgments
We would like to thank David Lusseau for assistance in several aspects of data analysis, as well as to the rest of the participants in the Halifax IEC symposium on animal social networks for interesting ideas and discussion. Louise Barrett and one anonymous reviewer provided useful comments. We are grateful to the logistic support from the Punta Laguna community and Pronatura Peninsula de Yucatan. We would like to thank Eulogio Canul, Macedonio Canul, Augusto Canul, and Juan Canul for valuable assistance in the field and Colleen Schaffner and David Taub for sharing the management of the long-term project. Funding for fieldwork and data analysis was provided by the Wildlife Conservation Society, the Wenner-Gren Foundation for Anthropological Research, the North of England Zoological Society, Peace College, CONABIO, SEMARNAT-CONACYT (Project 0536-2002), SEP-CONACYT (Project J51278), and Instituto Politécnico Nacional. The experiments comply with the current laws of Mexico.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Guest Editor D. Lusseau
This contribution is part of the special issue “Social Networks: new perspectives” (Guest Editors: J. Krause, D. Lusseau and R. James)
Rights and permissions
About this article
Cite this article
Ramos-Fernández, G., Boyer, D., Aureli, F. et al. Association networks in spider monkeys (Ateles geoffroyi). Behav Ecol Sociobiol 63, 999–1013 (2009). https://doi.org/10.1007/s00265-009-0719-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00265-009-0719-4