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Fission–Fusion Dynamics in Southern Muriquis (Brachyteles arachnoides) in Continuous Brazilian Atlantic Forest

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Abstract

Fission–fusion social dynamics, the spatiotemporal variance in subunit size, composition, and cohesion, are the subject of considerable interest owing to their complex nature and widespread appearance in the primate order. We here aim to describe the nature of fission–fusion dynamics in a population of egalitarian southern muriquis inhabiting a relatively undisturbed extension of mildly seasonal Brazilian Atlantic forest to provide insights into the functions of fission–fusion dynamics and to examine the constraints on and opportunities for associations among individuals. We collected instantaneous scan samples and ad libitum data over a total of 13 mo in 2 yr (1599 observation hours) on subunit size at 2 spatiotemporal scales (party and nomadic party), party composition, spatial cohesion, and the behavioral context of fission–fusion events. These southern muriquis exhibited high levels of fission–fusion with significant variation in party size, cohesion, and composition. The group was weakly cohesive with a small mean party size (3.74 adults, 5.32 all individuals) and nomadic party size (13.73 adults, 19.38 all individuals). Mixed parties were the most frequently observed party type, although the high frequency of all-male parties suggests strong relationships based on philopatry and a mating strategy under scramble competition. We compare fission–fusion dynamics across populations of Brachyteles and highlight the striking continuum of these dynamics in the genus. We make interspecific comparisons with Ateles and Pan, with well documented high levels of fission–fusion, and demonstrate interspecific variation and convergence in grouping patterns.

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References

  • Altmann, J. (1974). Observational study of behaviour: sampling methods. Behaviour, 49, 227–267.

    Article  PubMed  CAS  Google Scholar 

  • Altmann, S. A., & Altmann, J. (1979). Demographic constraints on behaviour and social organization. In I. S. Bernstein & E. O. Smith (Eds.), Primate ecology and human origins: Ecological influences on social organisation (pp. 47–63). New York: Garland STPM Press.

    Google Scholar 

  • Asensio, N., Korstjens, A. H., & Aureli, F. (2009). Fissioning minimizes ranging costs in spider monkeys: a multiple-level approach. Behavioral Ecology and Sociobiology, 63(5), 649–659.

    Article  Google Scholar 

  • Aureli, F., & Schaffner, C. M. (2007). Aggression and conflict management at fusion in spider monkeys. Biology Letters, 3, 147–149.

    Article  PubMed  Google Scholar 

  • Aureli, F., & Schaffner, C. M. (2008). Social interactions, social relationships and the social system of spider monkeys. In C. J. Campbell (Ed.), Spider monkeys: Behavior, ecology and evolution of the genus Ateles (pp. 236–265). New York: Cambridge University Press.

    Google Scholar 

  • Aureli, F., Schaffner, C. M., Boesch, C., Bearder, S. K., Call, J., Chapman, C. A., Connor, R., et al. (2008). Fission-fusion dynamics: new research frameworks. Current Anthropology, 49(4), 627–654.

    Article  Google Scholar 

  • Badrian, A., & Badrian, N. (1984). Social organization of Pan paniscus in the Lomako forest, Zaïre. In R. L. Susman (Ed.), The Pygmy chimpanzee: Evolutionary biology and behaviour (pp. 325–346). New York: Plenum Press.

    Google Scholar 

  • Basabose, A. K. (2004). Fruit availability and chimpanzee party size at Kahuzi Montane Forest, Democratic Republic of Congo. Primates, 45(4), 211–219.

    Article  PubMed  Google Scholar 

  • Bezanson, M., Garber, P. A., Murphy, J. T., & Premo, L. S. (2008). Patterns of subgrouping and spatial affiliation in a community of mantled howling monkeys (Alouatta palliata). American Journal of Primatology, 70(3), 282–293.

    Article  PubMed  Google Scholar 

  • Bleisch, W. V., Cheng, A. S., Ren, W. D., & Xie, J. H. (1993). Preliminary results from a field study of wild Guizhou snub-nosed monkeys (Rhinopithecus brelichi). Folia Primatologica, 60(1–2), 72–82.

    Article  CAS  Google Scholar 

  • Boesch, C. (1996). Social grouping in Taï chimpanzees. In W. C. McGrew, L. Marchant, & T. Nishida (Eds.), Great ape societies (pp. 101–113). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Boesch, C., & Boesch, H. (1989). Hunting behaviour of wild chimpanzees in the Taï National Park. American Journal of Anthropology, 78, 547–573.

    Article  CAS  Google Scholar 

  • Bonabeau, E., Dagorn, L., & Fréon, P. (1999). Scaling in animal group-size distributions. Proceedings of the National Academy of Sciences of the USA, 96, 4472–4477.

    Article  PubMed  CAS  Google Scholar 

  • Boubli, J. P., Couto-Santos, F. R., & Mourthé, I. M. C. (2010). A quantitative assessment of habitat differences between northern and southern muriquis (Primates, Atelidae) in the Brazilian Atlantic Forest. Ecotropica, 16, 63–69.

    Google Scholar 

  • Bowler, M., & Bodmer, R. (2009). Social behavior in fission-fusion groups of red uakari monkeys (Cacajao calvus ucayalii). American Journal of Primatology, 71, 1–12.

    Article  Google Scholar 

  • Bradbury, J. W., & Vehrencamp, S. L. (1976). Social organization and foraging in emballonurid bats. II: A model for the determination of group size. Behavioral Ecology and Sociobiology, 1, 383–404.

    Article  Google Scholar 

  • Chapman, C. A. (1988). Patch use and patch depletion by the spider and howling monkeys of Santa Rosa National Park, Costa Rica. Behaviour, 105, 99–116.

    Article  Google Scholar 

  • Chapman, C. A. (1990). Association patterns of spider monkeys: the influence of ecology and sex on social organisation. Behavioral Ecology and Sociobiology, 26, 409–414.

    Article  Google Scholar 

  • Chapman, C. A., & Chapman, L. J. (2000). Determinants of group size in primates: The importance of travel costs. In S. Boinski & P. A. Garber (Eds.), On the move: How and why animals travel in groups (pp. 24–42). Chicago: University of Chicago Press.

    Google Scholar 

  • Chapman, C. A., & Rothman, J. M. (2009). Within-species differences in primate social structure: evolution of plasticity and phylogenetic constraints. Primates, 50(1), 12–22.

    Article  PubMed  Google Scholar 

  • Chapman, C. A., White, F. J., & Wrangham, R. W. (1993). Defining subgroup size in fission-fusion societies. Folia Primatologica, 61(1), 31–34.

    Article  CAS  Google Scholar 

  • Chapman, C. A., Wrangham, R. W., & Chapman, L. J. (1995). Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology, 36, 59–70.

    Article  Google Scholar 

  • Coles, R. C. (2009). Fission-fusion sociality in southern muriquis (Brachyteles arachnoides) in continuous Brazilian Atlantic forest. Ph.D. thesis, University of Cambridge.

  • Coles, R. C., Talebi, M. G., & Lee, P. C. (2008). Fission-fusion sociality in southern muriquis (Brachyteles arachnoides) in the continuous Atlantic Forest of Brazil. Primate Eye, 96, 652.

    Google Scholar 

  • Couto-Santos, F. R. (2007). Fenologia de espécies arbóreas do dossle e sub-dossel em um fragmento de Mata Atlântica semi-decídua em Caratinga, Minas Gerais. M.Sc. thesis, Federal University of Minas Gerais.

  • Couzin, I. D., & Krause, J. (2003). Self-organization and collective behavior of vertebrates. Advances in the Study of Behavior, 32, 1–75.

    Article  Google Scholar 

  • Custódio-Filho, A., Negreiros, O. C., Dias, A. C., & Franco, G. A. D. C. (1992). Composiçao florística do estrato arbóreo do Parque Estadual de Carlos Botelho, SP. Segundo Congresso Nacional de Essências Nativas, 1, 184–191.

    Google Scholar 

  • De Carvalho, O., Jr., Ferrari, S. F., & Strier, K. B. (2004). Diet of a muriqui group (Brachyteles arachnoides) in continuous primary forest. Primates, 45(3), 201–204.

    PubMed  Google Scholar 

  • de Moraes, P. L. R., De Carvalho, O., Jr., & Strier, K. B. (1998). Population variation in patch and party size in muriquis (Brachyteles arachnoides). International Journal of Primatology, 19(2), 325–337.

    Article  Google Scholar 

  • Di Fiore, A., & Campbell, C. J. (2007). The Atelines: Variations in ecology, behavior, and social organization. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 155–185). New York: Oxford University Press.

    Google Scholar 

  • Dias, L. G., & Strier, K. B. (2003). Effects of group size on ranging patterns in Brachyteles arachnoides hypoxanthus. International Journal of Primatology, 24, 209–221.

    Article  Google Scholar 

  • Doran, D. (1997). Influence of seasonality on activity patterns, feeding behaviour, ranging, and grouping patterns in Tai chimpanzees. International Journal of Primatology, 18, 183–206.

    Article  Google Scholar 

  • Dunbar, R. I. M. (1988). Primate social systems. London: Croom Helm.

    Google Scholar 

  • Dunbar, R. I. M. (1992). Neocortex size as a constraint on group size in primates. Journal of Human Evolution, 22(6), 469–493.

    Article  Google Scholar 

  • Eberle, M., & Kappeler, P. M. (2002). Mouse lemurs in space and time: a test of the socioecological model. Behavioral Ecology and Sociobiology, 51, 131–139.

    Article  Google Scholar 

  • Fukuda, F. (1989). Habitual fission-fusion and social organisation of the Hakone troop T of Japanese macaques in Kanagawa Prefecture, Japan. International Journal of Primatology, 10, 419–439.

    Article  Google Scholar 

  • Furuichi, T. (2009). Factors underlying party size differences between chimpanzees and bonobos: a review and hypotheses for future study. Primates, 50(3), 197–209.

    Article  PubMed  Google Scholar 

  • Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behaviour. Cambridge: Harvard University Press.

    Google Scholar 

  • Hartwig, W. (2007). Primate evolution. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 11–22). New York: Oxford University Press.

    Google Scholar 

  • Itoh, N., & Nishida, T. (2007). Chimpanzee grouping patterns and food availability in Mahale Mountains National Park, Tanzania. Primates, 48, 87–96.

    Article  PubMed  Google Scholar 

  • Kano, T. (1982). The social group of pygmy chimpanzees (Pan paniscus) of Wamba. Primates, 23(2), 171–188.

    Article  Google Scholar 

  • Kappeler, P. M., & van Schaik, C. P. (2002). Evolution of primate social systems. International Journal of Primatology, 23(4), 707–740.

    Article  Google Scholar 

  • Kinzey, W. G., & Cunningham, E. P. (1994). Variability in platyrrhine social organization. American Journal of Primatology, 34, 185–198.

    Article  Google Scholar 

  • Korstjens, A. H., Verhoeckx, I., & Dunbar, R. I. M. (2006). Time as a constraint on group size in spider monkeys. Behavioral Ecology and Sociobiology, 60, 683–694.

    Article  Google Scholar 

  • Krause, J., & Ruxton, G. D. (2002). Living in groups. Oxford: Oxford University Press.

    Google Scholar 

  • Kummer, H. (1971). Primate societies: Group techniques of ecological adaptation. Chicago: Aldine.

    Google Scholar 

  • Kuroda, S. (1979). Grouping patterns of the pygmy chimpanzees. Primates, 20, 161–83.

    Article  Google Scholar 

  • Lehmann, J., & Boesch, C. (2004). To fission or to fusion: effects of community size on wild chimpanzees (Pan troglodytes verus) social organisation. Behavioral Ecology and Sociobiology, 56, 207–216.

    Article  Google Scholar 

  • Lehmann, J., Korstjens, A. H., & Dunbar, R. I. M. (2007). Fission-fusion social systems as a strategy for coping with ecological constraints: a primate case. Evolutionary Ecology, 21(5), 613–634.

    Article  Google Scholar 

  • Lemos de Sá, R. M., & Glander, K. (1993). Capture techniques and morphometrics for the woolly spider monkey or muriqui (Brachyteles arachnoides E. Geoffroy 1806). American Journal of Primatology, 29, 145–153.

    Article  Google Scholar 

  • Lynch-Alfaro, J. W. (2007). Subgrouping patterns in a group of wild Cebus apella nigritus. International Journal of Primatology, 28, 271–289.

    Article  Google Scholar 

  • Maia, R. T., Fávaro, L. B., Moreira, L. S., & Dias, L. G. (2007). Area de vida de uma grupo de muriquis (Brachyteles hypoxanthus) em um fragmento florestal do Parque Estadual da Serra de Brigadeiro, MG. In F. R. Melo, A. Hirsch, C. G. Costa, L. G. Dias, I. M. C. Mourthé, F. P. Tabacow, & L. M. Scoss (Eds.), CD-ROM de Resumos XII Congresso Brasileiro de Primatologica (p. 63).

  • Martins, M. M. (2005). The southern muriqui, Brachyteles arachnoides: ecology of a population in a semi-deciduous fragment. Neotropical Primates, 13, 61–65.

    Google Scholar 

  • Martins, M. M. (2006). Comparative seed dispersal effectiveness of sympatric Alouatta guariba and Brachyteles arachnoides in southeastern Brazil. Biotropica, 38(1), 57–63.

    Google Scholar 

  • Matsumoto-Oda, A., Hosaka, K., Huffman, M. A., & Kawanaka, K. (1998). Factors affecting party size in chimpanzees of the Mahale mountains. International Journal of Primatology, 19(6), 999–1011.

    Article  Google Scholar 

  • Ménard, N. (2002). Ecological plasticity of barbary macaques (Macaca sylvanus). Evolutionary Anthropology, 1, 95–100.

    Google Scholar 

  • Mendes, F. D. C., & Ades, C. (2004). Vocal sequential exchanges and intragroup spacing in the northern muriqui Brachyteles arachnoides hypoxanthus. Anais da Academis Brasileira de Ciencias, 76(2), 399–404.

    Article  Google Scholar 

  • Mendes, S. L., Melo, F., Boubli, J. P., Dias, L. G., Strier, K. B., Pinto, L. P. S., et al. (2005). Directives for the conservation of the northern muriqui, Brachyteles hypoxanthus. Neotropical Primates, 13, 7–18.

    Google Scholar 

  • Mendes, C. L. S., Dias, L. G., & Melo, F. R. (2007). Area de uso e preferencia de habitat do muriqui-do-norte (Brachyteles hypoxanthus) na Mata do Sossego, Simonesia, MG. In F. R. Melo, A. Hirsch, C. G. Costa, L. G. Dias, I. M. C. Mourthé, F. P. Tabacow, & L. M. Scoss (Eds), CD-ROM de Resumos XII Congresso Brasileiro de Primatologia (p. 71).

  • Milton, K. (1984). Habitat, diet, and activity patterns of free ranging woolly spider monkeys (Brachyteles arachnoides, E Geoffroy 1806). International Journal of Primatology, 5, 491–514.

    Article  Google Scholar 

  • Mitani, J. C., & Amsler, S. J. (2003). Social and spatial aspects of male subgrouping in a community of wild chimpanzees. Behaviour, 140(7), 869–884.

    Article  Google Scholar 

  • Mitani, J. C., Watts, D. P., & Lwanga, J. S. (2002). Ecological and social correlates of chimpanzee party size and composition. In C. Boesch, G. Hohmann, & L. F. Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos (pp. 102–111). Cambridge: Cambridge University Press.

    Chapter  Google Scholar 

  • Morgan, D. (2007). Socio-ecology of chimpanzees in the Goualougo Triangle, Republic of Congo. Ph.D. thesis, University of Cambridge.

  • Morland, H. S. (1991). Preliminary report on the social organization of ruffed lemurs (Varecia variegata) in a northeast Madagascar rain forest. Folia Primatologica, 56, 157–161.

    Article  Google Scholar 

  • Mourthé, I. M. C. (2006). A ecologia do forrageamento do muriqui do norte (Brachyteles hypoxanthus, Kuhl, 1820). M.Sc. thesis, Federal University of Minas Gerais.

  • Mulavwa, M., Furuichi, T., Yangozene, K., Yamba-Yamba, M., Motema-Salo, B., Idani, G., et al. (2008). Seasonal changes in fruit production and party size of bonobos at Wamba. In T. Furuichi & J. Thompson (Eds.), The bonobos: Behavior, ecology and conservation (pp. 121–134). New York: Springer.

    Google Scholar 

  • Nakai, E. S. (2007). Fissão-fusão em Cebus nigritus: Flexibilidade social como estratégia de ocupação de ambientes limitantes. M.Sc. thesis, University of São Paulo.

  • Neuhaus, P., Ruckstuhl, K. E., & Conradt, L. (2005). Conclusions and future directions. In K. E. Ruckstuhl & P. Neuhaus (Eds.), Sexual segregation in vertebrates: Ecology of the two sexes (pp. 395–402). Cambridge: Cambridge University Press.

    Google Scholar 

  • Newton-Fisher, N. E., Reynolds, V., & Plumptre, A. J. (2000). Food supply and chimpanzee (Pan troglodytes schweinfurthii) party size in the Budongo Forest Reserve, Uganda. International Journal of Primatology, 21(4), 613–628.

    Article  Google Scholar 

  • Nishida, T. (1968). The social group of wild chimpanzees in the Mahali mountains. Primates, 9, 167–224.

    Article  Google Scholar 

  • Nunes, A. (1996). Foraging and ranging patterns in white-bellied spider monkeys. Folia Primatologica, 65, 85–99.

    Google Scholar 

  • Pacagnella, S. (1991). Censo de população de monos-carvoeiro (Brachyteles arachnoides) no Parque Estadual de Carlos Botelho, estado de São Paulo. In A. B. Rylands & A. T. Bernardes (Eds.), A primatologia no Brasil 3 (pp. 225–234). Belo Horizonte: Sociedade Brasileira de Primatologia (SBPr) and Fundação Biodiversitas.

    Google Scholar 

  • Pepper, J. W. (2001). GROUPS. A program for analyzing association preferences in group composition data. Program given on request.

  • Pepper, J. W., Mitani, J. C., & Watts, D. P. (1999). General gregariousness and specific social preferences among wild chimpanzees. International Journal of Primatology, 20(5), 613–632.

    Article  Google Scholar 

  • Petroni, L. (2000). Caracterização da área de uso e dieta do mono-carvoeiro (Brachyteles arachnoides, Cebidae-Primates) na Mata Atlantica, Serra de Paranapiacaba, SP. Ph.D. thesis, University of São Paulo.

  • Pusey, A. E. (1990). Behavioural changes at adolescence in chimpanzees. Behaviour, 115(3–4), 203–246.

    Article  Google Scholar 

  • Ramos-Fernández, G., & Ayala-Orozco, B. (2003). Population size and habitat use of spider monkeys at Punta Laguna, Mexico. In L. K. Marsh (Ed.), Primates in fragments: Ecology and conservation (pp. 191–209). New York: Kluwer Academic/Plenum.

    Google Scholar 

  • Reynolds, V. (2005). The chimpanzees of the Budongo Forest: Ecology, behaviour and conservation. New York: Oxford University Press.

    Google Scholar 

  • Rodseth, L., Wrangham, R. W., Harrigan, A. M., & Smuts, B. B. (1991). The human community as a primate society. Current Anthropology, 32, 221–254.

    Article  Google Scholar 

  • Rohlf, J. F., & Sokal, R. R. (1994). Biometry: Principles and practice of statistics in biological research. San Francisco: W. H. Freeman.

    Google Scholar 

  • Rosenberger, A. L., & Strier, K. B. (1989). Adaptive radiation of the Ateline Primates. Journal of Human Evolution, 18(7), 717–750.

    Article  Google Scholar 

  • Sakura, O. (1994). Factors affecting party size and composition of chimpanzees (Pan troglodytes verus) at Bossou, Guinea. International Journal of Primatology, 15, 167–183.

    Article  Google Scholar 

  • Shimooka, Y. (2003). Seasonal variation in association patterns of wild spider monkeys (Ateles belzebuth belzebuth) at La Macarena, Colombia. Primates, 44, 83–90.

    PubMed  Google Scholar 

  • Sibly, R. M. (1983). Optimal group size is unstable. Animal Behaviour, 31, 947–948.

    Article  Google Scholar 

  • Silva, S. S. B., & Ferrari, S. F. (2009). Behavior patterns of southern bearded sakis (Chiropotes satanas) in the fragmented landscape of eastern Brazilian Amazonia. American Journal of Primatology, 71(1), 1–7.

    Article  PubMed  Google Scholar 

  • Slater, K. Y., Schaffner, C. M., & Aureli, F. (2009). Sex differences in the social behavior of wild spider monkeys (Ateles geoffroyi yucatanensis). American Journal of Primatology, 71(1), 21–29.

    Article  PubMed  Google Scholar 

  • Smolker, R. A., Richards, A. F., Connor, R. C., & Pepper, J. W. (1992). Sex-differences in patterns of association among Indian-Ocean bottle-nosed dolphins. Behaviour, 123, 38–69.

    Article  Google Scholar 

  • Strier, K. B. (1986). The behavior and ecology of the woolly spider monkey, or muriqui: (Brachyteles arachnoides, E. Geoffroy 1806). Ph.D. thesis, Harvard University.

  • Strier, K. B. (1989). Effects of patch size on feeding associations in muriquis (Brachyteles arachnoides). Folia Primatologica, 52, 70–77.

    Article  CAS  Google Scholar 

  • Strier, K. B. (1990). New World Primates, new frontiers: insights from the woolly spider monkey or muriqui (Brachyteles arachnoides). International Journal of Primatology, 11, 7–19.

    Article  Google Scholar 

  • Strier, K. B. (1992a). Faces in the forest: The endangered muriqui monkeys of Brazil. New York: Oxford University Press.

    Google Scholar 

  • Strier, K. B. (1992b). Causes and consequences of nonaggression in woolly spider monkey, or muriqui (Brachyteles arachnoides). In J. Silverberg & P. J. Gray (Eds.), Aggression and peacefulness in humans and other primates (pp. 100–115). New York: Oxford University Press.

    Google Scholar 

  • Strier, K. B. (2000). Lack of pubertal influences on female dispersal in female muriqui monkeys (Brachyteles arachnoides). Animal Behaviour, 59, 849–860.

    Article  PubMed  Google Scholar 

  • Strier, K. B., & da Fonseca, G. A. B. (1996/1997). The endangered muriqui in Brazil’s Atlantic forest. Primate Conservation, 17, 131–137.

    Google Scholar 

  • Strier, K. B., Mendes, F. D. C., Rimoli, J., & Rimoli, A. O. (1993). Demography and social structure of one group of muriquis (Brachyteles arachnoides). International Journal of Primatology, 14(4), 513–526.

    Article  Google Scholar 

  • Strier, K. B., Dib, L. T., & Figueira, J. E. C. (2002). Social dynamics of male muriquis (Brachyteles arachnoides hypoxanthus). Behaviour, 139, 315–342.

    Article  Google Scholar 

  • Strier, K. B., Boubli, J. P., Possamai, C. B., & Mendes, S. L. (2006). Population demography of northern muriquis (Brachyteles hypoxanthus) at the Estacao Biologica de Caratinga/Reserva Particular do Patrimonio Natural-Feliciano Miguel Abdala, Minas Gerais, Brazil. American Journal of Physical Anthropology, 130(20), 227–237.

    Article  PubMed  Google Scholar 

  • Stumpf, R. (2007). Chimpanzees and bonobos: Diversity within and between species. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 321–344). New York: Oxford University Press.

    Google Scholar 

  • Suarez, S. A. (2003). Spatio-temporal foraging skills of white-bellied spider monkeys (Ateles belzebuth belzebuth) in the Yasuni National Park, Ecuador. Ph.D. thesis, State University of New York at Stony Brook.

  • Symington, M. M. (1988). Food competition and foraging party size in the black spider monkey (Ateles paniscus chamek). Behaviour, 105, 117–135.

    Article  Google Scholar 

  • Talebi, M. G. (2005). Factors affecting food choices and digestive efficiency of the critically endangered muriquis (Brachyteles arachnoides, Primates - E. Geoffroy, 1806) of the Brazilian Atlantic Forest. Ph.D. thesis, University of Cambridge.

  • Talebi, M. G., & Lee, P. C. (2010). Activity patterns of Brachyteles arachnoides in the largest remaining fragment of Brazilian Atlantic Forest. International Journal of Primatology, 31, 571–583.

    Article  Google Scholar 

  • Talebi, M. G., Bastos, A., & Lee, P. C. (2005). Diet of southern muriquis in continuous Brazilian Atlantic Forest. International Journal of Primatology, 26(5), 1175–1187.

    Article  Google Scholar 

  • Talebi, M. G., Beltrão-Mendes, R., & Lee, P. C. (2009). Intra-community coalitionary lethal attack of an adult male southern muriqui (Brachyteles arachnoides). American Journal of Primatology, 71, 1–8.

    Article  Google Scholar 

  • Toborowsky, C. (2008). Preliminary evidence of fission-fusion sub-grouping behavior in white-fronted brown lemurs (Eulemur fulvus albifrons) in Betampona Natural Reserve, Madagascar. American Journal of Physical Anthropology, 46, 208.

    Google Scholar 

  • Tutin, C. E., McGrew, W. C., & Baldwin, P. J. (1983). Social organisation of savanna-dwelling chimpanzees, Pan troglodytes verus at Mt. Assirik, Senegal. Primates, 24, 154–173.

    Article  Google Scholar 

  • Underwood, R. (1981). Companion preference in an eland herd. African Journal of Ecology, 19, 341–354.

    Article  Google Scholar 

  • UNESCO. (1999). Convention concerning the protection of the world cultural and natural heritage. Morocco: United Nations Educational, Scientific and Cultural Organizations.

    Google Scholar 

  • van Elsacker, L., Vervaecke, H., & Verheyen, R. F. (1995). A review of the terminology on aggregation patterns in bonobos (Pan paniscus). International Journal of Primatology, 16, 37–52.

    Article  Google Scholar 

  • van Schaik, C. P. (1989). The ecology of social relationships amongst female primates. In V. Standen & R. A. Foley (Eds.), Comparative socioecology: The behavioural ecology of humans and mammals (pp. 195–218). Oxford: Blackwell.

    Google Scholar 

  • van Schaik, C. P., & van Hooff, J. (1983). On the ultimate causes of primate social systems. Behaviour, 85, 91–117.

    Article  Google Scholar 

  • Veiga, L. M., Pinto, L. P., & Ferrari, S. F. (2006). Fission-fusion sociality in bearded sakis (Chiropotes albinasus and Chiropotes satanas) in Brazilian Amazonia. International Journal of Primatology, 27, 224.

    Google Scholar 

  • Wallace, R. B. (1998). The behavioral ecology of black spider monkeys in north-eastern Bolivia. Ph.D. thesis, University of Liverpool.

  • Wallace, R. B. (2008). The influence of feeding patch size and relative fruit density on the foraging behavior of the black spider monkey Ateles chamek. Biotropica, 40(4), 501–506.

    Article  Google Scholar 

  • White, F. J. (1988). Party composition and dynamics in Pan paniscus. International Journal of Primatology, 9(3), 179–193.

    Article  Google Scholar 

  • Williams, J. M., Hsien-Yang, L., & Pusey, A. E. (2002). Costs and benefits of grouping for female chimpanzees at Gombe. In C. Boesch, G. Hohmann, & L. F. Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos (pp. 90–101). Cambridge: Cambridge University Press.

    Google Scholar 

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Acknowledgments

We thank Pró-Muriqui Association for logistical support and concession of field assistance by Pedro Soares and Rafael de Silveira Bueno Silva; Director J. L. C. Maia of Parque Estadual Carlos Botelho, CNPq and the Forestry Foundation of São Paulo State for granting research permits (SMA 41513/1999–2009); Dr. Roland Barriot (Laboratoire de Microbiologie et Génétique Moléculaires, Université Paul Sabatier, Toulouse) for data format conversions in PERL; 2 anonymous reviewers for valuable comments on an earlier version of the manuscript. R. C. Coles was the recipient of a University of Cambridge Domestic Research Scholarship. M. Talebi was the recipient of a WWF-Brazil Postgraduate Support Grant (2002) and grants from the Margot Marsh Biodiversity Foundation through the Primate Action Fund of Conservation International, USA; Conservation International Brazil; Idea Wild; Manfred Hermsen Stiftung Foundation, Bremen, Germany; British Airways Assisting Conservation Bureau; and Downing College and University of Cambridge, UK. The authors declare no conflict of interest.

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Coles, R.C., Lee, P.C. & Talebi, M. Fission–Fusion Dynamics in Southern Muriquis (Brachyteles arachnoides) in Continuous Brazilian Atlantic Forest. Int J Primatol 33, 93–114 (2012). https://doi.org/10.1007/s10764-011-9555-2

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