Advertisement

The Northern Muriqui (Brachyteles hypoxanthus): Lessons on Behavioral Plasticity and Population Dynamics from a Critically Endangered Species

  • Karen B. Strier
  • Sérgio L. Mendes
Chapter

Abstract

Since its onset in the early 1980s, our ongoing field study of the northern muriqui in southeastern Brazil has yielded original data on the behavioral ecology, reproductive biology, and life histories of one of the most critically endangered primates in the world. At the same time, a sixfold expansion in the size of our study population has provided insights into the plasticity of behavior and life history patterns that have important implications for muriqui conservation as well as for comparative models of primate socioecology. In this review of the history, growth, and diversification of our long-term study, we describe the transformation of our field site into a federally protected private reserve, the progression of the research questions as our knowledge has increased, and our predictions about the effects of increased population density on key demographic and life history variables. We also reiterate the need for more comparative studies of other muriqui populations, and reflect on the essential role that long-term, international collaborations have played in advancing the scientific and conservation agendas we have pursued from the start.

Keywords

Forest Fragment Life History Data Main Study Group Intragroup Competition Male Philopatry 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

We thank CNPq for permission for us to conduct research in Brazil and for the support of part of this work, the Abdala family for permission to conduct this research at the RPPN Feliciano Miguel Abdala, and the Sociedade para a Preservação do Muriqui (Preserve Muriqui), Conservation International (CI) and CI-Brasil for their help with logistics and long-term collaboration. We thank the many people who have contributed to the long-term demographic data records (in alphabetical order): L. Arnedo, M.L. Assunção, N. Bejar, J.P. Boubli, A. Carvalho, D. Carvalho, C. Cäsar, A.Z. Coli, C.G. Costa, P. Coutinho, L. Dib, Leonardo G. Dias, Luiz G. Dias, D.S. Ferraz, J. Fidelis, J. Gomes, D. Guedes, V.O. Guimarães, R. Hack, M.F. Iurck, M. Kaizer, M. Maciel, W.P. Martins, F.D.C. Mendes, I.M. Mourthé, F. Neri, M. Nery, S. Neto, C.P. Nogueria, A. Odalia Rímoli, A. Oliva, L. Oliveira, F.P. Paim, C.B. Possamai, R.C. Printes, J. Rímoli, S.S. Rocha, R.C. Romanini, R.R. dos Santos, B.G.M. da Silva, J.C. da Silva, V. Souza, D.V. Slomp, F.P. Tabacow, W. Teixeira, M. Tokudo, K. Tolentino, and E.M. Veado. We especially thank Carla de Borba Possamai and Fernanda Pedreira Tabacow for their commitment to the long-term demographic data. The field study has been supported by a variety of sources, including the National Science Foundation (BNS 8305322, BCS 8619442, BCS 8958298, BCS 9414129, BCS 0621788, BCS 0921013), National Geographic Society, the Liz Claiborne and Art Ortenberg Foundation, Fulbright Foundation, Sigma Xi Grants-in-Aid, Grant #213 from the Joseph Henry Fund of the NAS, World Wildlife Fund, L.S.B. Leakey Foundation, Chicago Zoological Society, Lincoln Park Zoo Neotropic Fund, Center for Research on Endangered Species (CRES), Margot Marsh Biodiversity Foundation, Conservation International, the University of Wisconsin-Madison, and CNPq – Brazilian National Research Council. This research has complied with all U.S. and Brazilian regulations. We thank Peter Kappeler for inviting us to participate in the conference that led to this volume, and for including our contribution here despite our inability to attend. We appreciate the comments that he and David Watts provided on an earlier version of this chapter.

References

  1. Abdala Passos R (2003) A legacy of love for nature. In: da Fonseca MT (ed) 20 anos da Estação Biológica de Caratinga: reserva privada do patrimônio natural. Conservation International do Brasil, Belo Horizonte, pp 6–9Google Scholar
  2. Aguirre AC (1971) O mono Brachyteles arachnoides (E. Geoffroy): situação atual da espécie no Brasil. Academia Brasileira de Ciências, Rio de JaneiroGoogle Scholar
  3. Alberts SC, Altmann J (1995) Balancing costs and opportunities: dispersal in male baboons. Am Nat 145:279–306CrossRefGoogle Scholar
  4. Almeida-Silva B, Cunha AA, Boubli JP, Mendes SL, Strier KB (2005) Population density and vertical stratification of four primate species at the Estação Biológica de Caratinga/RPPN-FMA, Minas Gerais, Brazil. Neotrop Primates 13(suppl):25–29Google Scholar
  5. Altmann J, Alberts SC (2003) Variability in reproductive success viewed from a life-history perspective in baboons. Am J Hum Biol 15:401–409PubMedCrossRefGoogle Scholar
  6. Aureli F, Schaffner CM, Boesch C, Bearder SK, Call J, Chapman CA, Connor R, Di Fiore A, Dunbar RIM, Henzi SP, Holekamp K, Korstjens AH, Layton R, Lee PC, Lehmann J, Manson JH, Ramos-Fernandez G, Strier KB, van Schaik CP (2008) Fission-fusion dynamics: new research frameworks. Curr Anthropol 49:627–654CrossRefGoogle Scholar
  7. Bianchi RC, Mendes SL (2007) Ocelot (Leopardus pardalis) predation on primates in Caratinga Biological Station, Southeast Brazil. Am J Primatol 69:1173–1178CrossRefGoogle Scholar
  8. Boubli JP, Couto-Santos F, Strier KB (in press) Structure and floristic composition of a semideciduous Atlantic Forest fragment in Minas Gerais, Brazil: implications for the conservation of the critically endangered northern muriqui, Brachyteles hypoxanthus. EcotropicaGoogle Scholar
  9. Boubli JP, Tokuda M, Possamai CB, Fidelis J, Guedes D, Strier KB (2005) Dinâmica intergrupal de muriquis-do-norte, Brachyteles hypoxanthus, na Estação Biológica de Caratinga, MG: o comportamento de uma unidade de machos (all male band) no vale do Jaó. Paper presented at the XI Congresso Brasileiro de Primatologia, Porto Alegre, BrasilGoogle Scholar
  10. Campbell CJ (2006) Lethal intragroup aggression by adult male spider monkeys (Ateles geoffroyi). Am J Primatol 68:1197–1201PubMedCrossRefGoogle Scholar
  11. Castro MI (2001) RPPN Feliciano Miguel Abdala – a protected area for the northern muriqui. Neotrop Primates 9:128–129Google Scholar
  12. Charpentier MJE, Tung J, Altmann J, Alberts SC (2008) Age at maturity in wild baboons: genetic, environmental and demographic influences. Mol Ecol 17:2026–2040PubMedCrossRefGoogle Scholar
  13. Coimbra-Filho AF (1972) Mamíferos ameaçados de extinção no Brasil. In: Academia Brasileira de Ciências (ed) Espécies da Fauna Brasileira Ameaçadas de Extinção. Academia Brasileira de Ciências, Rio de Janeiro, pp 13–98Google Scholar
  14. Crockett CM, Pope TR (1993) Consequences of sex differences in dispersal for juvenile red howler monkeys. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: life history, development, and behavior. Oxford University Press, New York, pp 104–118Google Scholar
  15. Di Fiore A, Fleischer RG (2005) Social behavior, reproductive strategies, and population genetic structure of Lagothrix poeppigii. Int J Primatol 26:1137–1173CrossRefGoogle Scholar
  16. Di Fiore A, Strier KB (2004) Flexibility in social organization in atelin primates. Folia Primatol 75(suppl 1):140–141Google Scholar
  17. Di Fiore A, Link A, Schmitt CA, Spehar SN (2009) Dispersal patterns in sympatric woolly and spider monkeys: integrating molecular and observational data. Behaviour 146:437–470CrossRefGoogle Scholar
  18. Di Fiore A, Link A, Campbell CJ (2011) The atelines: behavioral and socioecological diversity in a New World radiation. In: Campbell CJ, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM (eds) Primates in perspectives, 2nd edn. Oxford University Press, New York, pp 155–188Google Scholar
  19. Dias LG, Strier KB (2003) Effects of group size on ranging patterns in Brachyteles arachnoids hypoxanthus. Int J Primatol 24:209–221CrossRefGoogle Scholar
  20. Fagundes V, Paes MF, Chaves PB, Mendes SL, Possamai CB, Boubli JP, Strier KB (2008) Genetic structure in two northern muriqui populations (Brachyteles hypoxanthus, Primates, Atelidae) as inferred from fecal DNA. Genet Mol Biol 31:166–171CrossRefGoogle Scholar
  21. Ferrari SF, Digby LJ (1996) Wild Callithrix groups: stable extended families? Am J Primatol 38:19–27CrossRefGoogle Scholar
  22. Groves CP (2001) Primate taxonomy. Smithsonian Institution Press, Washington, DCGoogle Scholar
  23. Hohmann G (2001) Association and social interactions between strangers and residents in bonobos (Pan paniscus). Primates 42:91–99CrossRefGoogle Scholar
  24. Janson CH, van Schaik CP (1993) Ecological risk aversion in juvenile primates: slow and steady wins the race. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: life history, development, and behavior. Oxford University Press, New York, pp 57–74Google Scholar
  25. Joffe TH (1997) Social pressures have selected for an extended juvenile period in primates. J Hum Evol 32:593–605PubMedCrossRefGoogle Scholar
  26. Koehler A, Pereira LCM, Nicola PA (2002) New locality for the woolly spider monkey, Brachyteles arachnoides (E. Geoffroy, 1806) in Paraná state, and the urgency of strategies for conservation. Estudos de Biologia 24:25–28Google Scholar
  27. Martins WP, Strier KB (2004) Age at first reproduction in philopatric female muriquis (Brachyteles arachnoides hypoxanthus). Primates 45:63–67PubMedCrossRefGoogle Scholar
  28. Mendes SL, de Melo FR, Boubli JP, Dias LG, Strier KB, Pinto LPS, Fagundes V, Cosenza B, De Marco Jr P (2005a) Directives for the conservation of the northern muriqui, Brachyteles hypoxanthus (Primates, Atelidae). Neotrop Primates 13(suppl):7–18Google Scholar
  29. Mendes SL, Santos RR, Carmo LP (2005b) Conserving the northern muriqui in Santa Maria de Jetibá, Espírito Santo. Neotrop Primates 13(suppl):31–35Google Scholar
  30. Mittermeier RA, Coimbra-Filho AF, Constable ID, Rylands AB, Valle C (1982) Conservation of primates in the Atlantic forest region of eastern Brazil. Int Zoo Yrbk 22:2–17CrossRefGoogle Scholar
  31. Mittermeier RA, Valladares-Pádua C, Rylands AB, Eudey AA, Butynski TM, Ganzhorn JU, Kormos R, Aguiar JM, Walker S (2006) Primates in Peril: the world’s 25 most endangered primates, 2004–2006. Primate Conserv 20:1–28CrossRefGoogle Scholar
  32. Moore J (1992) Dispersal, nepotism, and primate social behavior. Int J Primatol 13:361–378CrossRefGoogle Scholar
  33. Mourthé IMC, Guedes D, Fidelis J, Boubli JP, Mendes SL, Strier KB (2007) Ground use by northern muriquis (Brachyteles hypoxanthus). Am J Primatol 69:706–712PubMedCrossRefGoogle Scholar
  34. Nishimura A (1979) In search of woolly spider monkey. Kyoto Univ Overseas Res Rep New World Monkeys 1:21–37Google Scholar
  35. Nishimura A (2003) Reproductive parameters of wild female Lagothrix lagotricha. Int J Primatol 24:707–722CrossRefGoogle Scholar
  36. Perry S, Godoy I, Lammers W (2011) The Lomas Barbudal Monkey Project: Two Decades of Research on Cebus capucinus. In: Kappeler PM (ed) Long-term field studies of primates. Springer, HeidelbergGoogle Scholar
  37. Possamai CB, Young RJ, Mendes SL, Strier KB (2007) Socio-sexual behavior of female northern muriquis (Brachyteles hypoxanthus). Am J Primatol 69:766–776PubMedCrossRefGoogle Scholar
  38. Printes RC, Strier KB (1999) Behavioral correlates of dispersal in female muriquis (Brachyteles arachnoides). Int J Primatol 20:941–960CrossRefGoogle Scholar
  39. Printes RC, Costa CG, Strier KB (1996) Possible predation on two infant muriquis, Brachyteles arachnoides, at the Estação Biologica de Caratinga, Minas Gerais, Brasil. Neotrop Primates 4:85–86Google Scholar
  40. Robbins AM, Stoinski TS, Fawcett KA, Robbins MM (2009) Does dispersal cause reproductive delays in female mountain gorillas? Behaviour 146:525–549CrossRefGoogle Scholar
  41. Rylands AB, Mittermeier RA (2009) The diversity of the New World primates (Platyrrhini): an annotated taxonomy. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (eds) South American primates: comparative perspectives in the study of behavior, ecology, and conservation. Springer, New York, pp 23–54Google Scholar
  42. Rylands AB, Mittermeier RA, Rodriguez Luna E (1995) A species list for the New World primates (Platyrrhini): distribution by country, endemism, and conservation status according to the Mace-Land system. Neotrop Primates 3(suppl):113–160Google Scholar
  43. Santos SMC, Nogueira CP, Carvalho ARD, Strier KB (2004) Levantamento coproparasitológico em muriqui (Brachyteles arachnoides hypoxanthus). In: Mendes SL, Chiarello AG (eds) A primatologia no Brasil-8. IPEMA/Socieda de Brasileira de Primatologia, Vitória, Espírito Santo, pp 327–332Google Scholar
  44. Strier KB (1990) New World primates, new frontiers: insights from the woolly spider monkey, or muriqui (Brachyteles arachnnoides). Int J Primatol 11:7–19CrossRefGoogle Scholar
  45. Strier KB (1992a) Atelinae adaptations: behavioral strategies and ecological constraints. Am J Phys Anthropol 88:515–524PubMedCrossRefGoogle Scholar
  46. Strier KB (1992b) Causes and consequences of nonaggression in woolly spider monkeys, or muriqui (Brachyteles arachnnoides). In: Silverberg J, Gray JP (eds) Aggression and peacefulness in humans and other primates. Oxford University Press, New York, pp 100–116Google Scholar
  47. Strier KB (1994) Brotherhoods among atelins: kinship, affiliation, and competition. Behaviour 130:151–167CrossRefGoogle Scholar
  48. Strier KB (1997a) Mate preferences of wild muriqui monkeys (Brachyteles arachnoides): reproductive and social correlates. Folia Primatol 68:120–133CrossRefGoogle Scholar
  49. Strier KB (1997b) Behavioral ecology and conservation biology of primates and other animals. Adv Stud Behav 26:101–158CrossRefGoogle Scholar
  50. Strier KB (1999a) The atelines. In: Dolhinow P, Fuentes A (eds) The nonhuman primates. McGraw Hill, New York, pp 109–114Google Scholar
  51. Strier KB (1999b) Faces in the forest: the endangered muriqui monkeys of Brazil. Harvard University Press, Cambridge, MAGoogle Scholar
  52. Strier KB (2000a) Population viabilities and conservation implications for muriquis (Brachyteles arachnoides) in Brazil’s Atlantic forest. Biotropica 32:903–913Google Scholar
  53. Strier KB (2000b) From binding brotherhoods to short-term sovereignty: the dilemma of male Cebidae. In: Kappeler PM (ed) Primate males: causes and consequences of variation in group composition. Cambridge University Press, Cambridge, pp 72–83Google Scholar
  54. Strier KB (2003a) Primatology comes of age: 2002 AAPA luncheon address. Yrbk Phys Anthropol 122:2–13CrossRefGoogle Scholar
  55. Strier KB (2003b) 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, OK, pp 45–63Google Scholar
  56. Strier KB (2005) Reproductive biology and conservation of muriquis. Neotrop Primates 13(suppl):41–46Google Scholar
  57. Strier KB (2009) Seeing the forest through the seeds: mechanisms of primate behavioral diversity from individuals to populations and beyond. Curr Anthropol 50:213–228PubMedCrossRefGoogle Scholar
  58. Strier KB (2010) Long-term field studies: positive impacts and unintended consequences. Am J Primatol 72:772–778PubMedCrossRefGoogle Scholar
  59. Strier KB (2011) Social plasticity and demographic variation in primates. In: Sussman RW, Cloninger CR (eds) Origins of altruism and cooperation. Springer, New YorkGoogle Scholar
  60. 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
  61. Strier KB, Fonseca GAB (1996/1997) The endangered muriquis of Brazil’s Atlantic forest. Primate Conserv 17:131–137Google Scholar
  62. Strier KB, Mendes SL (2003) Research center. In: Fonseca MT (ed) 20 anos da Estação Biológica de Caratinga: reserva privada do patrimônio natural. Conservation International do Brasil, Belo Horizonte, pp 18–22Google Scholar
  63. Strier KB, Mendes SL (2009) Long-term field studies of South American primates. In: Garber PA, Estrada A, Bicca-Marques JC, Heymann EW, Strier KB (eds) South American primates: comparative perspectives in the study of behavior, ecology, and conservation. Springer, New York, pp 139–155Google Scholar
  64. Strier KB, Ziegler TE (1997) Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys, Brachyteles arachnoides. Am J Primatol 42:299–310PubMedCrossRefGoogle Scholar
  65. Strier KB, Ziegler TE (2000) Lack of pubertal influences on female dispersal in muriqui monkeys, Brachyteles arachnoides. Anim Behav 59:849–860PubMedCrossRefGoogle Scholar
  66. Strier KB, Mendes FDC, Rímoli J, Rímoli AO (1993) Demography and social structure of one group of muriquis (Brachyteles arachnoides). Int J Primatol 14:513–526CrossRefGoogle Scholar
  67. Strier KB, Carvalho DS, Bejar NO (2000) Prescription for peacefulness. In: Aureli F, de Waal FBM (eds) Natural conflict resolution. University of California Press, Berkeley, pp 315–317Google Scholar
  68. Strier KB, Dib LT, Figueira JEC (2002) Social dynamics of male muriquis (Brachyteles arachnoides hypoxanthus). Behaviour 139:315–342CrossRefGoogle Scholar
  69. Strier KB, Pinto LPS, Paglia A, Boubli JP, Mendes SL, Marini-Filho OJ, Rylands AB (2005) The ecology and conservation of the muriqui (Brachyteles): reports from 2002–2005. Introduction. Neotrop Primates 13(suppl):3–5Google Scholar
  70. Strier KB, Boubli JP, Possamai CB, Mendes SL (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 130:227–237PubMedCrossRefGoogle Scholar
  71. Stuart MD, Strier KB, Pierberg SM (1993) A coprological survey of parasites of wild muriquis, Brachyteles arachnoides, and brown howling monkeys, Alouatta fusca. J Helminthol Soc Wash 60:111–115Google Scholar
  72. Sugiyama Y (2004) Demographic parameters and life history of chimpanzees at Bossou, Guinea. Am J Phys Anthropol 124:154–165PubMedCrossRefGoogle Scholar
  73. Tabacow FP, Mendes SL, Strier KB (2009a) Spread of a terrestrial tradition in an arboreal primate. Am Anthropol 111:238–249CrossRefGoogle Scholar
  74. Tabacow FP, Possamai CB, de Melo FR, Mendes SL, Strier KB (2009b) New sightings of northern muriqui (Brachyteles hypoxanthus) females in forest fragments surrounding the Estação Biológica de Caratinga-RPPN Feliciano Miguel Abdala, Minas Gerais, Brasil. Neotrop Primates 16:67–69CrossRefGoogle Scholar
  75. Talebi MG, Beltrão-Mendes R, Lee PC (2009) Intra-community coalitionary lethal attack of an adult male southern muriqui (Brachyteles arachnoides). Am J Primatol 71:860–867PubMedCrossRefGoogle Scholar
  76. Valle CMC, Santos IB, Alves MC, Pinto CA, Mittermeier RA (1984) Preliminary observations on the behavior of the monkey (Brachyteles arachnoides) in a natural environment (Fazenda Montes Claros, Município de Caratinga, Minas Gerais, Brasil). In: Thiago de Mello M (ed) A primatologia no Brasil. Sociedade Brasileira de Primatologia, Belo Horizonte, pp 271–283Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of Wisconsin-MadisonMadisonUSA
  2. 2.Departamento de Ciências BiológicasUniversidade Federal do Espírito SantoVitóriaBrazil

Personalised recommendations