Abstract
The muriqui or woolly spider monkey (Brachyteles arachnoids) is an endangered primate endemic to the Atlantic Forest of Brazil, <5% of which remains. The known muriqui population consists of <700 individuals separated into approximately 15 geographically isolated forest fragments. I present data on the distribution of genetic variation within and between two such remnant populations (FE and FBR) and summarize the implications of these results for long-range management of species genetic diversity. Eleven of 32 allozyme loci were polymorphic, representing an overall level of polymorphism of 34.4% and a mean heterozygosity per locus of 11%. Both values are among the highest reported for New World monkeys. Genetic differentiation between the two localities is highly significant (FST = 0.413, p < 0.001). Genetic distance between them is an order of magnitude greater than that between other populations of platyrrhine subspecies, but this could be an artifact of the small sample size from FBR. High levels of genetic diversity apparently characteristic of this species persist because (1) fragmentation and size reduction of muriqui populations has occurred very rapidly relative to the muriqui life span—although both polymorphism and heterozygosity were lost between generations in the largest population, the high genetic diversity present in the parent population was still in evidence; and (2) genetic diversity before population fragmentation by human activity was not distributed uniformly throughout the species' historic distribution. Thus, remnant muriqui populations are important genetic reservoirs of alleles that are unique or rare in the species gene pool as a whole. These results emphasize the need for the integration of conservation management efforts throughout the species range.
Similar content being viewed by others
REFERENCES
Aguirre, A. C. (1971). O mono Brachyteles arachnoides (E. Geoffroy). Situação atual da espécie no Brasil, Academia Brasiliera de Ciências, Rio de Janeiro, Brazil.
Ayala, F. J., Powell, J. R., Tracey, M. L., Mourao, C. A., and Perez-Salas, S. (1972). Enzyme variability in the Drosophila willistoni group. IV. Genetic variation in natural populations of Drosophila willistoni. Genetics 70: 113-139.
Chesser, R. K. (1991). Gene diversity and female philopatry. Genetics 127: 437-447.
Coimbra-Filho, A. F., Pissinatti, A., and Rylands, A. B. (1994). Muriquis at the Rio de Janeiro Primate Center. Neotrop. Primates 2: 5-7.
Coimbra-Filho, A. F., Pissinatti, A., and Rylands, A. B. (1993). Breeding muriquis Brachyteles arachnoides in captivity: The experience of the Rio de Janeiro Primate Center (CPRJ-FEEMA). Dodo J. Wildl. Preserv. Trusts 29.
Fonseca, G. A. B. d. (1983). The Role of Deforestation and Private Reserves in the Conservation of the Woolly Spider Monkey (Brachyteles arachnoides), Master's thesis, University of Florida, Gainesville.
Fonseca, G. A. B. d. (1985a). Observations on the ecology of the muriqui (Brachyteles arachnoides E. Geoffroy 1806): implications for its conservation. Primate Conserv. 5: 48-52.
Fonseca, G. A. B. d. (1985b). The vanishing Brazilian Atlantic forest. Biol. Conserv. 34: 17-34.
Forman, L., Kleiman, D. G., Bush, R. M., Dietz, J. M., Ballou, J. D., Phillips, L. G., Coimbra-Filho, A. F., and O'Brien, S. J. (1986). Genetic variation within and among lion tamarins. Am. J. Phys. Anthropol. 7: 1-11.
Harris, H. (1980). The Principles of Human Biochemical Genetics, Elsevier/North-Holland, Amsterdam.
Harris, H., and Hopkinson, D. A. (1976). Handbook of Enzyme Electrophoresis in Human Genetics, North-Holland, Amsterdam.
Lemos de Sá, R. M. (1988). Situação de uma população de mono-carvoeiros, Brachyteles arachnoides, em fragmento de Mata Atlântica (M.G.), e implicações para sua conservação, Master's thesis, Universidade de Brasília, Brasília.
Lemos de Sá, R. M., and Glander, K. E. (1993). Capture techniques and morphometrics for the woolly spider monkey, or muriqui (Brachyteles arachnoides, E. Geoffroy 1806). Am. J. Primatol. 29: 145-153.
Lemos de Sá, R. M., Pope, T. R., Struhsaker, T. T., and Glander, K. E. (1990). A pilot study of genetic and morphological variation in the muriqui (Brachyteles arachnoides). Primate Conserv. 11: 26-30.
Lemos de Sá, R. M., Pope, T. R., Struhsaker, T. T., and Glander, K. E. (1993). Sexual dimorphism in canine length of woolly spider monkeys (Brachyteles arachnoides, E. Geoffroy 1806). Int. J. Primatol. 14: 755-762.
Lima, M. M. C., Sampaio, M. I. C., Schneider, M. P. C., Scheffrahn, W., Schneider, H., and Salzano, F. M. (1990). Chromosome and protein variation in red howler monkeys. Rev. Brasil. Genet. 13: 789-802.
Martuscelli, P., Petroni, L. M., and Olmos, F. (1994). Fourteen new localities for the muriqui Brachyteles arachnoides. Neotrop. Primates 2: 12-15.
Mendes, F. D. C. (1994). Muriqui conservation: The urgent need of an integrated management plan. Neotrop. Primates 2: 16-19.
Milton, K. (1984). Habitat, diet, and activity patterns of free-ranging woolly spider monkeys (Brachyteles arachnoides E. Geoffroy 1808). Int. J. Primatol. 5: 491-514.
Milton, K. (1985). Mating patterns of woolly spider monkeys, Brachyteles arachnoides: Implications for female choice. Behav. Ecol. Sociobiol. 17: 53-59.
Mittermeier, R. A. (1987). Rescuing Brazil's muriqui—monkey in peril. Natl. Geogr. 171: 386-395.
Mittermeier, R. A., Valle, C. M. C., Alves, M. C., Santos, I. B., Pinto, C. A. M., Strier, K. B., Young, A. L., Veado, E. M., Constable, I. D., Paccagnella, S. G., and Lemos de Sá, R. M. (1987). Current distribution of the muriqui in the Atlantic forest region of eastern Brazil. Primate Conserv. 8: 143-149.
Murphy, R. W., Sites, J. W., Buth, D. G., and Haufler, C. H. (1990). Proteins I: Isozyme electrophoresis. In Hillis, D. M. and Moritz, C. (eds.), Molecular Systematics, Sinauer, Sunderland, MA.
Napier, J. R., and Napier, P. H. (1967). A Handbook of Living Primates, Academic Press, London.
Nei, M. (1972). Genetic distance between populations. Am. Nat. 106: 283-291.
Nei, M. (1977). F-statistics and the analysis of gene diversity in subdivided populations. Ann. Hum. Genet. 41: 225-233.
Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89.
Nishimura, A., Fonseca, G. A. B. d., Mittermeier, R. A., Young, A. L., Strier, K. B., and Valle, C. M. C. (1988). The muriqui, genus Brachyteles. In Mittermeier, R. A., Rylands, A. B., Coimbra-Filho, A., and Fonseca, G. A. B. d. (eds.), Ecology and Behavior of Neotropical Primates, World Wildlife Fund, Washington, DC, pp. 577-610.
Pope, T. R. (1992). The influence of dispersal patterns and mating system on genetic differentiation within and between populations of the red howler monkey (Alouatta seniculus). Evolution 46: 1112-1128.
Pope, T. R. (1996). Socioecology, population fragmentation, and patterns of genetic loss in endangered primates. In Avis, J. C., and Hamrick, J. L. (eds.), Conservation Genetics: Case Histories from Nature, Chapman and Hall, New York, pp. 119-159.
Rylands, A. B., Coimbra-Filho, A. F., and Mittermeier, R. A. (1993). Systematics, geographic distribution, and some notes on the conservation status of the Callitrichidae. In Rylands, A. B. (ed.), Marmosets and Tamarins: Systematics, Behavior, and Ecology, Oxford University Press, New York, pp. 11-17.
Rylands, A. B., Mittermeier, R. A., and Luna, E. R. (1995). A species list for the New World primates (Platyrrhini): Distribution by country, endemism, and conservation status according to the Mace-Lande system. Neotrop. Primates 3(Suppl.): 113-160.
Sampaio, M. I. C., Schneider, M. P. C., and Schneider, H. (1993). Contribution of genetic distance studies to the taxonomy of Ateles, particularly Ateles paniscus and Ateles paniscus chamek. Int. J. Primatol. 14: 895-903.
Schneider, H., Sampaio, M. I. C., Schneider, M. P. C., Ayres, J. M., Barroso, C. M. L., Hamel, A. R., Silva, B. T. F., and Salzano, F. M. (1991). Coat color and biochemical variation in Amzzonian wild populations of Alouatta belzebul. Am. J. Phys. Anthropol. 85: 85-93.
Selander, R. K., Smith, M. H., Yang, S. Y., Johnson, W. E., and Gentry, J. R. (1971). Biochemical polymorphism and systematics in the genus Peromyscus. I. Variation in the old field mouse (Peromyscus polionotus). Stud. Genet. VI Univ. Texas Publ. 7103: 49-90.
Smouse, P. E. V., Vitzthum, V. J., and Neel, J. V. (1981). The impact of random and lineal fission on the genetic divergence of small human groups: A case study of the Yanomama. Genetics 98: 179-197.
Strier, K. B. (1986). The Behavior and Ecology of the Woolly Spider Monkey, or Muriqui (Brachyteles arachnoides E. Geoffroy 1806), Ph.D. dissertation, Harvard University, Cambridge, MA.
Strier, K. B. (1991). Demography and conservation of an endangered primate, Brachyteles arachnoides. Conserv. Biol. 5: 214-218.
Thorpe, J. P. (1982). The molecular clock hypothesis: Biochemical evolution, genetic differentiation and systematics. Annu. Rev. Ecol. Syst. 13: 139-168.
Vieira, C. O. C. (1944). Os simios do estado de São Paulo. Papeis Avulsos Zool. São Paulo 4: 1-31.
Workman, P. L., and Niswander, J. D. (1970). Population studies of southwestern Indian tribes. II. Local genetic differentiation in the Papago. Am. J. Hum. Genet. 22: 724-749.
Wright, S. (1965). The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19: 395-420.
Wright, S. (1980). Genic and organismic selection. Evolution 34: 825-842.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Pope, T.R. Genetic Variation in Remnant Populations of the Woolly Spider Monkey (Brachyteles arachnoides) . International Journal of Primatology 19, 95–109 (1998). https://doi.org/10.1023/A:1020311111401
Issue Date:
DOI: https://doi.org/10.1023/A:1020311111401