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Primates

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Using multiplex networks to capture the multidimensional nature of social structure

  • Sandra E. Smith-Aguilar
  • Filippo Aureli
  • Laura Busia
  • Colleen Schaffner
  • Gabriel Ramos-Fernández
Special Feature: Original Article Social networks analysis in primates, a multilevel perspective

Abstract

Network analysis has increasingly expanded our understanding of social structure in primates and other animal species. However, most studies use networks representing only one interaction type, when social relationships (and the emerging social structure) are the result of many types of interactions and their interplay through time. The recent development of tools facilitating the integrated analysis of multiple interaction types using multiplex networks has opened the possibility of extending the insight provided by social network analysis. We use a multiplex representation of interactions among the members of a group of wild Geoffroy’s spider monkeys (Ateles geoffroyi), to study their social structure. We constructed a six-layered multiplex network based on three indices of overt social interactions (aggression, embraces, grooming) and three distance-based indices (contact, proximity, and association). With tools provided by the MuxViz software, we assessed the relevance of including all six indices in our analysis, the role of individuals in the network (through node versatility), and the presence of modules and non-random triadic structures or motifs. The multiplex provided information which was not equivalent to any individual layer or to the simple aggregation of layers. Network patterns based on associations did not correspond with those observed for overt-interactions or for the multiplex structure. Males were the most versatile individuals, while multiplex modularity and motifs highlighted the relevance of different interaction types for the overall connectivity of the network. We conclude that the multiplex approach improves on previous methods by retaining valuable information from each interaction type and how it is patterned among individuals.

Keywords

Social network analysis Multilayer networks Social interactions Robert Hinde Ateles geoffroyi Node versatility 

Notes

Acknowledgements

We thank Ivan Puga, Sebastian Sosa, and Cédric Sueur for their invitation to participate in this special issue. We also thank Anthony R. Denice for his outstanding contribution in data collection, Augusto Canul, Eulogio Canul, Juan Canul, and Macedonio Canul for their valuable assistance during fieldwork, and Dr. Kelly Finn together with an anonymous reviewer for their valuable and useful comments and suggestions. SSA would also like to thank Sherie Simms for support and inspiration throughout the writing of this paper. We are also indebted to the Chester Zoo, The National Geographic Society, the Instituto Politécnico Nacional and the Consejo Nacional por la Ciencia y la Tecnologia (CONACyT) for financial support. We conducted this research with permission from CONANP and SEMARNAT (SGPA/DGVS/00910/13 and SGPA/DGVS/02716/14).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

10329_2018_686_MOESM1_ESM.docx (173 kb)
Supplementary material 1 (DOCX 172 kb)

References

  1. Aguilar-Melo AR, Calmé S, Smith-Aguilar S, Ramos-Fernández G (2018) Fission–fusion dynamics as a temporally and spatially flexible behavioral strategy in spider monkeys. Behav Ecol Sociobiol 72:150.  https://doi.org/10.1007/s00265-018-2562-y CrossRefGoogle Scholar
  2. Asensio N, Korstjens A, Schaffner CM, Aureli F (2008) Intragroup aggression, fission–fusion dynamics and feeding competition in spider monkeys. Behaviour 145:983–1001.  https://doi.org/10.1163/156853908784089234 CrossRefGoogle Scholar
  3. Aureli F, Schaffner CM (2007) Aggression and conflict management at fusion in spider monkeys. Biol Lett 3:147–149.  https://doi.org/10.1098/rsbl.2007.0041 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Aureli F, Schaffner CM (2008) Social interactions, social relationships and the social system of spider monkeys. In: Campbell CJ (ed) Spider monkeys. Behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge, pp 236–257CrossRefGoogle Scholar
  5. Aureli F, Schaffner CM, Verpooten J et al (2006) Raiding parties of male spider monkeys: insights into human warfare? Am J Phys Anthropol 131:486–497.  https://doi.org/10.1002/ajpa.20451 CrossRefPubMedGoogle Scholar
  6. Aureli F, Schaffner CM, Boesch C et al (2008) Fission–fusion dynamics. Curr Anthropol 49:627–654.  https://doi.org/10.1086/586708 CrossRefGoogle Scholar
  7. Aureli F, Schaffner CM, Asensio N et al (2012) What is a subgroup? How socioecological factors influence interindividual distance. Behav Ecol 23(6):1308–1315.  https://doi.org/10.1093/beheco/ars122 CrossRefGoogle Scholar
  8. Baggio JA, Burnsilver SB, Magdanz JS et al (2016) Multiplex social ecological network analysis reveals how social changes affect community robustness more than resource depletion. Proc Natl Acad Sci 113:13708–13713.  https://doi.org/10.1073/pnas.1604401113 CrossRefPubMedGoogle Scholar
  9. Barrett L, Henzi SP, Lusseau D (2012) Taking sociality seriously: the structure of multi-dimensional social networks as a source of information for individuals. Philos Trans R Soc B Biol Sci 367:2108–2118.  https://doi.org/10.1098/rstb.2012.0113 CrossRefGoogle Scholar
  10. Battiston F, Nicosia V, Latora V (2014) Structural measures for multiplex networks. Phys Rev E 89:1–16.  https://doi.org/10.1103/PhysRevE.89.032804 CrossRefGoogle Scholar
  11. Beisner BA, Jin J, Fushing H, McCowan B (2015) Detection of social group instability among captive rhesus macaques using joint network modeling. Curr Zool 61:70–84.  https://doi.org/10.1093/czoolo/61.1.70 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Boccaletti S, Bianconi G, Criado R et al (2014) The structure and dynamics of multilayer networks. Phys Rep 544:1–122.  https://doi.org/10.1016/j.physrep.2014.07.001 CrossRefGoogle Scholar
  13. Brent LJN, Lehmann J, Ramos-Fernández G (2011) Social network analysis in the study of nonhuman primates: a historical perspective. Am J Primatol 73:720–730.  https://doi.org/10.1002/ajp.20949 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Busia L, Schaffner CM, Aureli F (2015) Watch out or relax: conspecifics affect vigilance in wild spider monkeys (Ateles geoffroyi). Behaviour 153:107–124.  https://doi.org/10.1163/1568539X-00003329 CrossRefGoogle Scholar
  15. Busia L, Schaffner CM, Aureli F (2017) Relationship quality affects fission decisions in wild spider monkeys (Ateles geoffroyi). Ethology 123:405–411.  https://doi.org/10.1111/eth.12609 CrossRefGoogle Scholar
  16. Busia L, Denice AR, Aureli F, Schaffner CM (2018) Homosexual behavior between male spider monkeys (Ateles geoffroyi). Arch Sex Behav.  https://doi.org/10.1007/s10508-018-1177-8 CrossRefPubMedGoogle Scholar
  17. Campbell CJ (2006) Copulation in free-ranging black-handed spider monkeys. Am J Primatol 68:1–5Google Scholar
  18. Campbell CJ, Gibson KN (2008) Spider monkey reproduction and sexual behavior. In: Campbell C (ed) Spider monkeys. Behaviour, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge, pp 266–287CrossRefGoogle Scholar
  19. Cantini L, Medico E, Fortunato S, Caselle M (2015) Detection of gene communities in multi-networks reveals cancer drivers. Sci Rep 5:1–10.  https://doi.org/10.1038/srep17386 CrossRefGoogle Scholar
  20. Cantor M, Whitehead H (2013) The interplay between social networks and culture: theoretically and among whales and dolphins. Philos Trans R Soc B Biol Sci 368:20120340.  https://doi.org/10.1098/rstb.2012.0340 CrossRefGoogle Scholar
  21. Cantor M, Shoemaker LG, Cabral RB et al (2015) Multilevel animal societies can emerge from cultural transmission. Nat Commun 6:8091.  https://doi.org/10.1038/ncomms9091 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Chan S, Fushing H, Beisner BA, McCowan B (2013) Joint modeling of multiple social networks to elucidate primate social dynamics: I. Maximum entropy principle and network-based interactions. PLoS ONE 8(2):e51903.  https://doi.org/10.1371/journal.pone.0051903 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Chapman CA, Wrangham RW, Chapman LJ (1995) Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behav Ecol Sociobiol 36(1):59–70CrossRefGoogle Scholar
  24. Daura-Jorge FG, Cantor M, Ingram SN et al (2012) The structure of a bottlenose dolphin society is coupled to a unique foraging cooperation with artisanal fishermen. Biol Lett 8:702–705.  https://doi.org/10.1098/rsbl.2012.0174 CrossRefPubMedPubMedCentralGoogle Scholar
  25. De Domenico MD, Solé-Ribalta A (2013) Centrality in interconnected multilayer networks. arXiv, pp 1–12.  https://doi.org/10.1038/ncomms7868
  26. De Domenico M, Nicosia V, Arenas A, Latora V (2014a) Layer aggregation and reducibility of multilayer interconnected networks, pp 1–7.  https://doi.org/10.1038/ncomms7864
  27. De Domenico M, Solé-Ribalta A, Cozzo E et al (2014b) Mathematical formulation of multilayer networks. Phys Rev X 3:1–15.  https://doi.org/10.1103/PhysRevX.3.041022 CrossRefGoogle Scholar
  28. De Domenico M, Lancichinetti A, Arenas A, Rosvall M (2015a) Identifying modular flows on multilayer networks reveals highly overlapping organization in interconnected systems. Phys Rev X 5:1–11.  https://doi.org/10.1103/PhysRevX.5.011027 CrossRefGoogle Scholar
  29. De Domenico M, Nicosia V, Arenas A, Latora V (2015b) Structural reducibility of multilayer networks. Nat Commun 6:1–9.  https://doi.org/10.1038/ncomms7864 CrossRefGoogle Scholar
  30. De Domenico M, Porter MA, Arenas A (2015c) MuxViz: a tool for multilayer analysis and visualization of networks. J Complex Netw 3:159–176.  https://doi.org/10.1093/comnet/cnu038 CrossRefGoogle Scholar
  31. De Domenico M, Solé-Ribalta A, Omodei E et al (2015d) Ranking in interconnected multilayer networks reveals versatile nodes. Nat Commun 6:1–6.  https://doi.org/10.1038/ncomms7868 CrossRefGoogle Scholar
  32. De Domenico M, Granell C, Porter MA, Arenas A (2016) The physics of spreading processes in multilayer networks. Nat Phys 12:901–906.  https://doi.org/10.1038/nphys3865 CrossRefGoogle Scholar
  33. Farine DR, Whitehead H (2015) Constructing, conducting and interpreting animal social network analysis. J Anim Ecol 84:1144–1163.  https://doi.org/10.1111/1365-2656.12418 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Fedigan LM, Baxter MJ (1984) Sex differences and social organization in free-ranging spider monkeys (Ateles geoffroyi). Primates 25:279–294CrossRefGoogle Scholar
  35. Finn KR, Silk MJ, Porter MA, Pinter-Wollman N (2017) Novel insights into animal sociality from multilayer networks. arXiv preprint arXiv:1712.01790, pp 1–44
  36. Flack JC (2012) Multiple time-scales and the developmental dynamics of social systems. Philos Trans R Soc Lond B Biol Sci 367:1802–1810.  https://doi.org/10.1098/rstb.2011.0214 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Flack JC (2017) Life’s information hierarchy. In: Walker S, Davies P, Ellis G (eds) From matter to life. Information and causality. Cambridge University Press, Cambridge, pp 283–302.  https://doi.org/10.1017/9781316584200.012 CrossRefGoogle Scholar
  38. Flack JC, de Waal FBM, Krakauer DC (2005) Social structure, robustness, and policing cost in a cognitively sophisticated species. Am Nat 165:E126–E139.  https://doi.org/10.1086/429277 CrossRefPubMedGoogle Scholar
  39. Fortuna MA, Popa-Lisseanu AG, Ibáñez C, Bascompte J (2009) The roosting spatial network of a bird-predator bat. Ecology 90:934–944.  https://doi.org/10.1890/08-0174.1 CrossRefPubMedGoogle Scholar
  40. Fraser ON, Bugnyar T (2010) The quality of social relationships in ravens. Anim Behav 79:927–933.  https://doi.org/10.1016/j.anbehav.2010.01.008 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Fraser ON, Schino G, Aureli F (2008) Components of relationship quality in chimpanzees. Ethology 114:834–843.  https://doi.org/10.1111/j.1439-0310.2008.01527.x CrossRefGoogle Scholar
  42. Gao J, Buldyrev SV, Stanley HE, Havlin S (2012) Networks formed from interdependent networks. Nat Phys 8:40–48.  https://doi.org/10.1038/nphys2180 CrossRefGoogle Scholar
  43. García-Frapolli E, Ayala-Orozco B, Bonilla-Moheno M, Espadas-Manrique C, Ramos-Fernández 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. Lands Urban Plan 83 (2–3):137–153.  https://doi.org/10.1016/j.landurbplan.2007.03.007 CrossRefGoogle Scholar
  44. Ge H, Walhout AJM, Vidal M (2003) Integrating “omic” information: a bridge between genomics and systems biology. Trends Genet 19:551–560.  https://doi.org/10.1016/j.tig.2003.08.009 CrossRefPubMedGoogle Scholar
  45. Girvan M, Newman MEJ (2002) Community structure in social and biological networks. Proc Natl Acad Sci 99:7821–7826.  https://doi.org/10.1073/pnas.122653799 CrossRefPubMedGoogle Scholar
  46. Granell C, Gómez S, Arenas A (2013) Dynamical interplay between awareness and epidemic spreading in multiplex networks. Phys Rev Lett 111:1–10.  https://doi.org/10.1103/PhysRevLett.111.128701 CrossRefGoogle Scholar
  47. Guimerà R, Amaral LAN (2005) Functional cartography of complex metabolic networks. Nature 433:895–900.  https://doi.org/10.1038/nature03288 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Hartwell KS, Notman H, Bonenfant C, Pavelka MSM (2014) Assessing the occurrence of sexual segregation in spider monkeys (Ateles geoffroyi yucatanensis), its mechanisms and function. Int J Primatol 35:425–444.  https://doi.org/10.1007/s10764-013-9746-0 CrossRefGoogle Scholar
  49. Hasenjager MJ, Dugatkin LA (2015) Social network analysis in behavioral ecology. Adv Study Behav 47:39–114.  https://doi.org/10.1016/bs.asb.2015.02.003 CrossRefGoogle Scholar
  50. Henzi SP, Lusseau D, Weingrill T et al (2009) Cyclicity in the structure of female baboon social networks. Behav Ecol Sociobiol 63:1015–1021.  https://doi.org/10.1007/s00265-009-0720-y CrossRefGoogle Scholar
  51. Hinde RA (1976) Interactions, relationships and social structure. Man 11:1–17.  https://doi.org/10.2307/2800384 CrossRefGoogle Scholar
  52. Ilany A, Booms AS, Holekamp KE (2015) Topological effects of network structure on long-term social network dynamics in a wild mammal. Ecol Lett 18:687–695.  https://doi.org/10.1111/ele.12447 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Kasper C, Voelkl B (2009) A social network analysis of primate groups. Primates 50:343–356.  https://doi.org/10.1007/s10329-009-0153-2 CrossRefPubMedGoogle Scholar
  54. King AJ, Sueur C (2011) Where next? Group coordination and collective decision making by primates. Int J Primatol 32:1245–1267.  https://doi.org/10.1007/s10764-011-9526-7 CrossRefGoogle Scholar
  55. Kivelä M, Arenas A, Barthelemy M et al (2014) Multilayer networks. J Complex Netw 2:203–271.  https://doi.org/10.1093/comnet/cnu016 CrossRefGoogle Scholar
  56. Krause J, Croft DP, James R (2007) Social network theory in the behavioural sciences: potential applications. Behav Ecol Sociobiol 62:15–27.  https://doi.org/10.1007/s00265-007-0445-8 CrossRefGoogle Scholar
  57. Lee KM, Min B, Goh KI (2015) Towards real-world complexity: an introduction to multiplex networks. Eur Phys J B 88:48.  https://doi.org/10.1140/epjb/e2015-50742-1 CrossRefGoogle Scholar
  58. Lusseau D, Conradt L (2009) The emergence of unshared consensus decisions in bottlenose dolphins. Behav Ecol Sociobiol 63:1067–1077CrossRefGoogle Scholar
  59. Lusseau D, Newman MEJ (2004) Identifying the role that animals play in their social networks. Proc Biol Sci 271(Suppl):S477–S481.  https://doi.org/10.1098/rsbl.2004.0225 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Milo R, Shen-Orr S, Itzkovitz S et al (2002) Network motifs: simple building blocks of complex networks. Science 298:824–827.  https://doi.org/10.1126/science.298.5594.824 CrossRefGoogle Scholar
  61. Mucha PJ, Richardson T, Macon K et al (2010) Community structure in time-dependent, multiscale, and multiplex networks. Science 328:876–878.  https://doi.org/10.1126/science.1184819 CrossRefPubMedGoogle Scholar
  62. Newman MEJ (2001) The structure of scientific collaboration networks. Proc Natl Acad Sci 98(2):404–409.  https://doi.org/10.1073/pnas.021544898 CrossRefPubMedGoogle Scholar
  63. Newman MEJ (2003) The structure and function of complex networks. SIAM Rev 45(2):167–256.  https://doi.org/10.1137/S003614450342480 CrossRefGoogle Scholar
  64. Newman MEJ (2004) Analysis of weighted networks. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 70(5):056131.  https://doi.org/10.1103/PhysRevE.70.056131 CrossRefGoogle Scholar
  65. Newman MEJ (2006) Modularity and community structure in networks. Proc Natl Acad Sci USA 103:8577–8582.  https://doi.org/10.1073/pnas.0601602103 CrossRefGoogle Scholar
  66. Palacios T, Castellanos F, Ramos-Fernandez G (2018) Uncovering the decision rules behind collective foraging in spider monkeys. Anim Behav (in revision) Google Scholar
  67. Pinter-Wollman N, Hobson EA, Smith JE et al (2013) The dynamics of animal social networks: analytical, conceptual, and theoretical advances. Behav Ecol 25:242–255.  https://doi.org/10.1093/beheco/art047 CrossRefGoogle Scholar
  68. Pujari M, Kanawati R (2015) Link prediction in multiplex networks. Netw Heterog Media 10:17–35.  https://doi.org/10.3934/nhm.2015.10.17 CrossRefGoogle Scholar
  69. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  70. Ramos-Fernández G (2005) Vocal communication in a fission-fusion society: do spider monkeys stay in touch with close associates? Int J Primatol 26:1077–1092.  https://doi.org/10.1007/s10764-005-6459-z CrossRefGoogle Scholar
  71. Ramos-Fernández G, Morales JM (2014) Unraveling fission–fusion dynamics: how subgroup properties and dyadic interactions influence individual decisions. Behav Ecol Sociobiol 68:1225–1235.  https://doi.org/10.1007/s00265-014-1733-8 CrossRefGoogle Scholar
  72. Ramos-Fernández G, Boyer D, Gómez VP (2006) A complex social structure with fission–fusion properties can emerge from a simple foraging model. Behav Ecol Sociobiol 60:536–549.  https://doi.org/10.1007/s00265-006-0197-x CrossRefGoogle Scholar
  73. Ramos-Fernández G, Boyer D, Aureli F, Vick LG (2009) Association networks in spider monkeys (Ateles geoffroyi). Behav Ecol Sociobiol 63:999–1013.  https://doi.org/10.1007/s00265-009-0719-4 CrossRefGoogle Scholar
  74. Ramos-Fernandez G, Smith Aguilar SE, Schaffner CM, Vick LG, Aureli F (2013) Site Fidelity in Space Use by Spider Monkeys (Ateles geoffroyi) in the Yucatan Peninsula, Mexico. PLoS ONE 8 (5):e62813.  https://doi.org/10.1371/journal.pone.0062813 CrossRefPubMedGoogle Scholar
  75. Ramos-Fernández G, Aureli F, Schaffner CM, Vick LG (2018) Ecología, comportamiento y conservación de los monos araña (Ateles geoffroyi): 20 años de estudio. In: Urbani B, Kowalewski M, Teixeira da Cunha RG, de la Torre S, Cortés-Ortiz L (eds) La primatología en Latinoamérica 2/A primatologia na America Latina 2. Instituto Venezolano de Investigaciones Científicas, Caracas, pp 531–544Google Scholar
  76. Rebecchini L, Schaffner CM, Aureli F (2011) Risk is a component of social relationships in spider monkeys. Ethology 117:691–699.  https://doi.org/10.1111/j.1439-0310.2011.01923.x CrossRefGoogle Scholar
  77. Rebollar EA, Sandoval-Castellanos E, Roessler K et al (2017) Seasonal changes in a maize-based polyculture of central Mexico reshape the co-occurrence networks of soil bacterial communities. Front Microbiol 8:1–13.  https://doi.org/10.3389/fmicb.2017.02478 CrossRefGoogle Scholar
  78. Rimbach R, Bisanzio D, Galvis N et al (2015) Brown spider monkeys (Ateles hybridus): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics. Philos Trans R Soc B Biol Sci 370:20140110.  https://doi.org/10.1098/rstb.2014.0110 CrossRefGoogle Scholar
  79. Riveros J, Schaffner CM, Aureli F (2017) You are not welcome: social exchanges between female spider monkeys (Ateles geoffroyi). Int J Primatol 38:856–871.  https://doi.org/10.1007/s10764-017-9982-9 CrossRefGoogle Scholar
  80. Schaffner CM, Aureli F (2005) Embraces and grooming in captive spider monkeys. Int J Primatol 26:1093–1106.  https://doi.org/10.1007/s10764-005-6460-6 CrossRefGoogle Scholar
  81. Schaffner CM, Rebecchini L, Ramos-Fernández G et al (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.  https://doi.org/10.1007/s10764-012-9621-4 CrossRefGoogle Scholar
  82. Shimooka Y (2003) Seasonal variation in association patterns of wild spider monkeys (Ateles belzebuth belzebuth) at La Macarena, Colombia. Primates 44(2):83–90.  https://doi.org/10.1007/s10329-002-0028-2 CrossRefPubMedGoogle Scholar
  83. Shimooka Y (2005) Sexual differences in ranging of Ateles belzebuth belzebuth at La Macarena, Colombia. Int J Primatol 26:385–406.  https://doi.org/10.1007/s10764-005-2930-0 CrossRefGoogle Scholar
  84. Sih A, Hanser SF, McHugh KA (2009) Social network theory: new insights and issues for behavioral ecologists. Behav Ecol Sociobiol 63:975–988.  https://doi.org/10.1007/s00265-009-0725-6 CrossRefGoogle Scholar
  85. Silk J, Cheney D, Seyfarth R (2013) A practical guide to the study of social relationships. Evol Anthropol 22:213–225.  https://doi.org/10.1002/evan.21367 CrossRefPubMedGoogle Scholar
  86. Silk MJ, Finn KR, Porter MA, Pinter-Wollman N (2018) Can multilayer networks advance animal behavior research? Trends Ecol Evol 33:376–378.  https://doi.org/10.1016/j.tree.2018.03.008 CrossRefPubMedGoogle Scholar
  87. Sistema Meteorológico Nacional (2015) Normales climatológicas en la estación 00023012 (Cobá, Quintana Roo), periodo 1980–2010. Servicio Meteorológico Nacional, Comisión Nacional del Agua, MéxicoGoogle Scholar
  88. Slater K (2007) Sex differences in the social relationships of wild spider monkeys (Ateles geoffroyi yucatanesis). Dissertation, University of LiverpoolGoogle Scholar
  89. Slater KY, Schaffner CMM, Aureli F (2007) Embraces for infant handling in spider monkeys: evidence for a biological market? Anim Behav 74:455–461.  https://doi.org/10.1016/j.anbehav.2006.11.026 CrossRefGoogle Scholar
  90. Slater K, Schaffner CM, Aureli F (2009) Sex differences in the social behavior of wild spider monkeys (Ateles geoffroyi yucatanensis). Am J Primatol 29:1657–1669.  https://doi.org/10.1002/ajp.20618 CrossRefGoogle Scholar
  91. Smith-Aguilar SE, Ramos-Fernández G, Getz WM (2016) Seasonal changes in socio-spatial structure in a group of free-living spider monkeys (Ateles geoffroyi). PLoS ONE 11:e0157228.  https://doi.org/10.1371/journal.pone.0157228 CrossRefPubMedPubMedCentralGoogle Scholar
  92. Sueur C, Petit O (2008) Organization of group members at departure is driven by social structure in Macaca. Int J Primatol 29:1085–1098.  https://doi.org/10.1007/s10764-008-9262-9 CrossRefGoogle Scholar
  93. Sueur C, Jacobs A, Amblard F et al (2011a) How can social network analysis improve the study of primate behavior? Am J Primatol 73:703–719.  https://doi.org/10.1002/ajp.20915 CrossRefPubMedGoogle Scholar
  94. Sueur C, King AJ, Conradt L et al (2011b) Collective decision-making and fission–fusion dynamics: a conceptual framework. Oikos 120:1608–1617.  https://doi.org/10.1111/j.1600-0706.2011.19685.x CrossRefGoogle Scholar
  95. Sueur C, King A, Pelé M, Petit O (2013) Fast and accurate decisions as a result of scale-free network properties in two primate species. In: Gilbert T, Kirkilionis M, Nicolis G (eds) Proceedings of the European conference on complex systems 2012. Springer International Publishing, pp 579–584Google Scholar
  96. Sundaresan SR, Fischhoff IR, Dushoff J, Rubenstein DI (2007) Network metrics reveal differences in social organization between two fission-fusion species, Grevy’s zebra and Onager. Oecologia 151:140–149.  https://doi.org/10.1007/s00442-006-0553-6 CrossRefPubMedGoogle Scholar
  97. Symington MM (1988) Demography, ranging patterns, and activity budgets of black spider monkeys (Ateles paniscus charnek) in the Manu National Park, Peru. Am J Primatol 15:45–67CrossRefGoogle Scholar
  98. Symington MM (1990) Fission-fusion social organization in Ateles and Pan. Int J Primatol 11:47–61CrossRefGoogle Scholar
  99. Vespignani A (2010) Complex networks: the fragility of interdependency. Nature 464:984–985.  https://doi.org/10.1038/464984a CrossRefPubMedGoogle Scholar
  100. Vick LG (2008) Immaturity in spider monkeys: a risky business. In: Campbell CJ (ed) Spider monkeys. Behavior, ecology and evolution of the genus Ateles. Cambridge University Press, Cambridge, pp 288–328CrossRefGoogle Scholar
  101. Voelkl B, Kasper C (2009) Social structure of primate interaction networks facilitates the emergence of cooperation. Biol Lett 5:462–464.  https://doi.org/10.1098/rsbl.2009.0204 CrossRefPubMedPubMedCentralGoogle Scholar
  102. Voelkl B, Noe R (2008) The influence of social structure on the propagation of social information in artificial primate groups: a graph-based simulation approach. J Theor Biol 252:77–86.  https://doi.org/10.1016/j.jtbi.2008.02.002 CrossRefPubMedGoogle Scholar
  103. Wey T, Blumstein DT, Shen W, Jordán F (2008) Social network analysis of animal behaviour: a promising tool for the study of sociality. Anim Behav 75:333–344.  https://doi.org/10.1016/j.anbehav.2007.06.020 CrossRefGoogle Scholar
  104. Whitehead H (2008) Analyzing animal societies: quantitative methods for vertebrate social analysis. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  105. Whitehead H, Dufault S (1999) Techniques for analyzing vertebrate social structure using identified individuals: review and recommendations. Adv Study Behav 28:33–74CrossRefGoogle Scholar
  106. Wolf JBW, Mawdsley D, Trillmich F, James R (2007) Social structure in a colonial mammal: unravelling hidden structural layers and their foundations by network analysis. Anim Behav 74:1293–1302.  https://doi.org/10.1016/j.anbehav.2007.02.024 CrossRefGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer Japan KK, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional, Unidad OaxacaInstituto Politécnico NacionalSanta Cruz XoxocotlánMexico
  2. 2.Conservación Biológica y Desarrollo Social ACMexico CityMexico
  3. 3.Instituto de NeuroetologíaUniversidad VeracruzanaXalapaMexico
  4. 4.Research Centre in Evolutionary Anthropology and PalaeoecologyLiverpool John Moores UniversityLiverpoolUK
  5. 5.School of Sociology and AnthropologySun Yat-sen UniversityGuangzhouChina
  6. 6.Psychology DepartmentAdams State UniversityAlamosaUSA
  7. 7.Instituto de Investigación en Matemáticas Aplicadas y Sistemas, Universidad Nacional Autónoma de MéxicoMexico CityMexico
  8. 8.Centro de Ciencias de la Complejidad, Universidad Nacional Autónoma de MéxicoMexico CityMexico
  9. 9.Unidad Profesional Interdisciplinaria en Ingeniería y Tecnologías Avanzadas, Instituto Politécnico NacionalMexico CityMexico

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