Ecological and Anthropogenic Influences on Patterns of Parasitism in Free-Ranging Primates: A Meta-analysis of the Genus Alouatta

  • Martin M. Kowalewski
  • Thomas R. Gillespie
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


Nonhuman Primate Parasite Species Blood Parasite Howler Monkey Gastrointestinal Parasite 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Acha, P. N. and Szyfres, B. 1986. Zoonosis y Enfermedades Transmisibles Comunes al Hombrey a los Animales, OPAS 503. Oficina Sanitaria Panamericana, Oficina Regional de la Organización Mundial de la Salud, Washington.Google Scholar
  2. Altizer, S., Nunn, C. L., Thrall, P., Gittleman, J. L., Antonovics, J., Cunningham, A., Dobson, A., Ezenwa, V., Pedersen, A. B., Poss, M. and Pulliam, J. R. C. 2003. Social organization and disease risk in mammals: Insights from comparative and theoretical studies. Annual Review of Ecology and Systematics 34:517–547.CrossRefGoogle Scholar
  3. Baker, M. 1996. Fur rubbing: use of medicinal plants by capuchin monkeys (Cebus capucinus). American Journal Primatology 38:263–270.CrossRefGoogle Scholar
  4. Bar, M. E., Alvarez, B. M., Oscherov, E. B., Damborsky, M. P. and Jörg, M. E. 1999. Contribución al conocimiento de los reservorios del Trypanosoma cruzi (Chagas, 1909) en la Provincia de Corrientes, Argentina. Revista da Sociedade Brasileira de Medicina Tropical 32(3):271–276.Google Scholar
  5. Bastone, P., Truyen, U. and Loechelt, M. 2003. Potential of zoonotic transmission of non-primate foamy viruses to humans. Journal of Veterinary Medicine B50(9):417–423.CrossRefGoogle Scholar
  6. Bicca-Marques, J. C. 2003. How do howler monkeys cope with habitat fragmentation? In L. K. Marsh (ed.), Primates in Fragments: Ecology and Conservation (pp. 283–303). New York: Kluwer Academic/Plenum Publishers.Google Scholar
  7. Brack, M. 1987. Agents Transmissible From Simians to Man. New York: Springer-Verlag.Google Scholar
  8. Bravo, S. P. and Sallenave, A. 2003. Foraging behavior and activity patterns of Alouatta caraya in the northeastern Argentinean flooded forest. International Journal of Primatology 24(4):825–846.CrossRefGoogle Scholar
  9. Cabral, J. N. H., Rossato, R. S., de M. Gomes, M. J. T, Araújo, F. A. P, Oliveira, F. and Praetzel, K. 2005. Gastrointestinais de bugios-ruivos (Alouatta guariba clamitans Cabrera 1940) da região extremo-sul de Porto Alegre/RS - Brasil, diagnosticados através da coproscopia: implicações para a conservação da espécie e seus ha. Congresso Brasileiro de Parasitologia, Porto Alegre, RS, Brasil.Google Scholar
  10. Campbell, C. J. 2000. Fur rubbing behavior in free-ranging black-handed spider monkeys (Ateles geoffroyi) in Panama. American Journal of Primatology 51:205–208PubMedCrossRefGoogle Scholar
  11. Carme, B., Aznar, C., Motard, A., Demar, M. and De Thoisy, B. 2002. Serologic Survey of Toxoplasma gondii in Noncarnivorous Free-Ranging Neotropical Mammals in French Guiana. Vector Borne and Zoonotic Diseases 2(1):11–17.PubMedCrossRefGoogle Scholar
  12. Carpenter, C. R. 1964. Naturalistic Behavior of Nonhuman Primates. Pennsylvania State University Press, University Park.Google Scholar
  13. Chapman, C. A., Balcomb, S. R., Gillespie, T. R, Skorupa, J. P. and Struhsaker, T. T. 2000. Long-term effects of logging on primates in Kibale National Park, Uganda: A 28 year comparison. Conservation Biology 14:207–217.CrossRefGoogle Scholar
  14. Chapman, C. A., Gillespie, T. R. and Goldberg, T. L. 2005. Primates and the ecology of their infectious diseases: How will anthropogenic change affect host-pathogen interactions? Evolutionary Anthropology 14:134–144.CrossRefGoogle Scholar
  15. Chapman, C. A., Wasserman, M. D. and Gillespie, T. R., 2006. Behavioural patterns of colobus in logged and unlogged forests: the conservation value of harvested forests. In E. Newton-Fisher, H. Notman, V Reynolds and J.D. Patterson (eds.), Primates of Western Uganda (pp. 373–390) New York: Springer.Google Scholar
  16. Chapman, C. A., Wasserman, M. D., Gillespie, T. R., Speirs, M. L. Lawes, M. J. and Ziegler, T. E. in press. Do nutrition, parasitism, and stress have synergistic effects on red colobus populations living in forest fragments? American Journal of Physical Anthropology.Google Scholar
  17. Clarke, M. R., Crockett, C. M., Zucker, E. L. and Zaldivar, M. 2002. Mantled howler population of hacienda La Pacifica, Costa Rica, between 1991 and 1998: effects of deforestation. American Journal of Primatology 56:155–163.PubMedCrossRefGoogle Scholar
  18. Coppo, J. A., Moreira, R. A. and Lombardero, O. J. 1979. El parasitismo en los primates del CAPRIM. Acta Zoológica Lilloana 35:9–12.Google Scholar
  19. Cortés-Ortiz, L., Birmingham, E., Rico, C., Rodríguez-Luna, E., Sampaio, I. and Ruiz-García, M. 2003. Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Molecular Phylogenetics and Evolution 26:64–81.PubMedCrossRefGoogle Scholar
  20. Crockett, C. M. 1998. Conservation biology of the genus Alouatta. International Journal of Primatology 19(3):549–578.CrossRefGoogle Scholar
  21. Davies, C. R., Ayres, J. M. , Dye, C. and Deane L. M. 1991. Malaria infection rate of Amazonian primates increases with body weight and group size. Functional Ecology 5(5):655–662.CrossRefGoogle Scholar
  22. Deane, L. M. 1992. Simian malaria in Brazil. Memorias do Instituto Oswaldo Cruz 87(Suppl. 3):1–20.PubMedGoogle Scholar
  23. Delgado, A. 2006. Estudio de patrones de uso de sitios de defecación y su posible relación con infestaciones parasitarias en dos grupos de monos aulladores negros y dorados (Alouatta caraya) en el nordeste argentino. Licenciatura Thesis, Universidad Nacional de Córdoba, Argentina (inedit).Google Scholar
  24. Dereure, J., Barnabe, C., Vie, J. C., Madelenat, F. and Raccurt, C. 2001. Trypanosomatidae from wild mammals in the neotropical rainforest of French Guiana. Annals of Tropical Medicine and Parasitology 95(2):157–166.PubMedCrossRefGoogle Scholar
  25. Di Fiore, A. and Campbell, C. J. 2007. The Atelines: variations in ecology, behavior, and social organization..In C. J. Campbell, A. Fuentes, K. C. MacKinnon M. Panger and S. K. Bearder (eds.), Primates in Perspective (pp. 155–185). New York: Oxford Univ. Press.Google Scholar
  26. Dias J. C. P., Silveira, A. C. and Schofield, C. J. 2002. The Impact of Chagas Disease Control in Latin America – A Review. Mem. Inst. Oswaldo Cruz, Rio de Janeiro 97(5):603–612.Google Scholar
  27. Diaz-Ungria, C. 1965. Nematodes de primates venezolanos. Soc. Venezol. Ciencias Nat. 25:393–398.Google Scholar
  28. Duarte, A. M. R. C., Porto, M. A. L., Curado, I., Malafronte, R. S., Hoffmann, E. H. E., de Oliveira, S. G., da Silva, A. M. J., Kloetzel, J. K. and Gomes, A. C. 2006. Widespread occurrence of antibodies against circumsporozoite protein and against blood forms of Plasmodium vivax, P. falciparum and P. malariae in Brazilian wild monkeys. Journal of Medical Primatology 35(2):87–96.PubMedCrossRefGoogle Scholar
  29. Eckert, K. A., Hahn, N. E., Genz, A., Kitchen, D. M., Stuart, M. D., Averbeck, G. A., Stromberg, B. E. and Markowitz, H. 2006. Coprological surveys of Alouatta pigra at two sites in Belize. International Journal of Primatology 27(1):227–238.CrossRefGoogle Scholar
  30. Eisenberg, J. F., Muckenhirn, N. A. and Rudran, R. 1972. The relation between ecology and social structure in primates. Science 176:863–874.PubMedCrossRefGoogle Scholar
  31. Esch, G. and Fernandez, J. C. 1993. A Functional Biology of Parasitism: Ecological and Evolutionary Implications. London: Chapman and Hall.Google Scholar
  32. Estrada, A., Juan-Solano, S., Ortiz Martinez, T. and Coates-Estrada, R. 1999. Feeding and general activity patterns of a howler monkey (Alouatta palliata) troop living in a forest fragment at Los Tuxtlas, Mexico. American Journal of Primatology 48(3):167–183.Google Scholar
  33. Estrada, A., Mendoza, A., Castellanos, L., Pacheco, R., Van Belle, S., Garcia, Y., Muñoz, D. 2002. Population of the black howler monkey (Alouatta pigra) in a fragmented landscape in Palenque, Chiapas, México. American Journal of Primatology 58:45–55.PubMedCrossRefGoogle Scholar
  34. Estrada, A., Saenz, J., Harvey, C., Naranjo, E., Muñoz, D. and Rosales-Meda, M. 2006. Primates in agroecosystems: conservation value of some agricultural practices in Mesoamerican landscapes. In A. Estrada, P. A. Garber, M. S. M. Pavelka and L. Luecke (eds.), New Perspectives in the Study of Mesoamerican Primates: Distribution, Ecology, Behavior, and Conservation (pp. 437–470). New York: Springer.CrossRefGoogle Scholar
  35. Fandeur, T., Volney, B., Peneau, C. and De Thoisy, B. 2000. Monkeys of the rainforest in French Guiana are natural reservoirs for P. brasilianum/P. malariae malaria. Parasitology 120:11–21.PubMedCrossRefGoogle Scholar
  36. Freeland, W. J. 1976. Pathogens and the evolution of primate sociality. Biotropica 8:12–24.CrossRefGoogle Scholar
  37. Fuentes, A. 2004. Human culture, macaque behaviour and global tourism: assessing the context and patterns of pathogen transmission risk in human-macaque interactions. Folia Primatologica 75(1):102–103.Google Scholar
  38. Galindo, P. and Srihongse, S. 1967. Evidence of recent jungle yellow-fever activity in eastern Panama. Bulletin of the World Health Organization 36:151–161.PubMedGoogle Scholar
  39. Garcia, J. L., Svoboda, W. K, Chryssafidis, A. L., de Souza Malanski, L., Shiozawa, M. M., de Moraes Aguiar, L., Teixeira, G. M, Ludwig, G., da Silva, L. R., Hilst, C. and Navarro, T. T. 2005. Sero-epidemiological survey for toxoplasmosis in wild New World monkeys (Cebus spp.; Alouatta caraya) at the Parana river basin, Parana State, Brazil. Veterinary Parasitology 133(4):307–11.PubMedCrossRefGoogle Scholar
  40. Gilbert, K. A. 1994. Endoparasitic infection in red howling monkeys (Alouatta seniculus) in the Central Amazonian basis: a cost of sociality? Ph. D. Thesis, The State University of New Jersey at New Brunswick Rutgers.Google Scholar
  41. Gilbert, K. A. and Stouffer, P.C. 1989. Use of a ground water source by mantled howler monkeys (Alouatta palliata). Biotropica 21(4):380.CrossRefGoogle Scholar
  42. Gillespie, T. R., Greiner, E. C. and Chapman, C. A. 2004. Gastrointestinal parasites of the guenons of western Uganda. Journal of Parasitology 90:1356–1360.PubMedCrossRefGoogle Scholar
  43. Gillespie, T. R., Chapman, C. A. and Greiner, E. C. 2005a. Effects of logging on gastrointestinal parasite infections and infection risk in African primates. Journal of Applied Ecology 42:699–707.CrossRefGoogle Scholar
  44. Gillespie, T.R., Greiner, E.C. and Chapman, C.A. 2005b. Gastrointestinal parasites of the colobine monkeys of Uganda. Journal of Parasitology 91:569–573.CrossRefGoogle Scholar
  45. Gillespie, T. R. 2006. Non-invasive assessment of gastro-intestinal parasite infections in free-ranging primates. International Journal of Primatology 27:1129–1143CrossRefGoogle Scholar
  46. Gillespie, T. R. and Chapman C. A. 2006. Prediction of parasite infection dynamics in primate metapopulations based on attributes of forest fragmentation. Conservation Biology 20:441–448.PubMedCrossRefGoogle Scholar
  47. Godoy, K. C. I. , Odalia-Rimoli, A. and Rimoli, J. 2004. Infecção por endoparasitos em um grupo de Bugios-Pretos (Alouatta caraya), em um fragmento florestal no Estado de Mato Grosso do Sul. Neotropical primates 12(2):63–68Google Scholar
  48. Gregory, R. D. 1990. Parasites and host geographic range as illustrated by waterfowl. Functional Ecology 4:645–654.CrossRefGoogle Scholar
  49. Gurevitch, J., Moorow, L. L., Wallace A. and Walsh, J. S. 1992. A meta-analysis of competition in field experiments. American Naturalist 140:539–572.CrossRefGoogle Scholar
  50. Hayami, M., Komuro, A., Nozawa, K., Shotake, T., Ishikawa, K., Yamamoto, K., Ishida, T., Honjo, S. and Hinuma, Y. 1984. Prevalence of antibody to adult T-cell leukemia virus- associated antigens (ATLA) in Japanese monkeys and other non-human primates. International Journal of Cancer 33:179–183.CrossRefGoogle Scholar
  51. Hedges, L. V. and Olkin, I. 1985. Statistical Methods for Meta-Analysis. Orlando, FL: Academic Press.Google Scholar
  52. Hochachka, V. W. and Dhondt, A. A. 2000. Density-dependent decline of host abundance resulting from a new infectious disease. Proceedings of the National Academy of Science 97:5303–5306.CrossRefGoogle Scholar
  53. Hosmer, D. W. and Lemeshow, S. 1989. Applied logistic regression, New York: Wiley.Google Scholar
  54. Hudson, P.J., Dobson, A.P. and Newborn, D. 1998. Prevention of population cycles by parasite removal. Science 282:2256–2258.PubMedCrossRefGoogle Scholar
  55. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H. and Dobson, A. P. 2002. The Ecology of Wildlife Disease. Oxford: Oxford University Press.Google Scholar
  56. Huffman. M. A. 1997. Current evidence for self-medication in primates: a multidisciplinary perspective. Yearbook Physical Anthropology 40:171–200.Google Scholar
  57. Johns, A. D. and Skorupa, J. P. 1987. Responses of rain-forest primates to habitat disturbance: A review. International Journal of Primatology 8(2):157–191.CrossRefGoogle Scholar
  58. Johnson, D. E. 1998. Applied Multivariate Statistical Analysis. Belmont, CA: Duxbury Press.Google Scholar
  59. Kleiman, D. G. and Rylands, A. B. 2002. Lion Tamarins: Biology and Conservation, Washington, DC: Smithsonian Institution Press.Google Scholar
  60. Kowalewski, M. M., Bravo, S. P. and Zunino, G. E. 1995. Aggression between Alouatta caraya in forest patches in northern Argentina. Neotropical Primates 3(4):179–181.Google Scholar
  61. Kowalewski, M. M. and Zunino, G. E. 1999. Impact of deforestation on a population of Alouatta caraya in northern Argentina. Folia Primatologica 70(3):163–166.CrossRefGoogle Scholar
  62. Kowalewski, M. M. and Zunino, G. E. 2004. Birth seasonality in Alouatta caraya in Northern Argentina. International Journal of Primatology 25(2):383–400.CrossRefGoogle Scholar
  63. Kowalewski, M. M. and Zunino, G. E. 2005. Testing the parasite avoidance behavior hypothesis with Alouatta caraya. Neotropical Primates 13(1):22–26.CrossRefGoogle Scholar
  64. Kumm, H. W. and Laemmert Jr., H. W. 1950. The geographical distribution of immunity to yellow fever among the primates of Brazil. American Journal of Tropical Medicine 30:733–748.Google Scholar
  65. Liang, S. Y., Linthicum, K. J. and Gaydos, J. C. 2002. Climate change and the monitoring of vector-borne diseases. Journal of the American Medical Association 287:2286–2286.PubMedCrossRefGoogle Scholar
  66. Lilly, A. A., Mehlman P. T. and Doran D. 2002. Intestinal parasites in gorillas, chimpanzees, and humans at Mondika Research site, Dzanga-Ndoki National Park, Central African Republic. International Journal of Primatology 23(3):555–573.CrossRefGoogle Scholar
  67. Lourenco de Oliveira, R. and Deane, L. M. 1995. Simian malaria at two sites in the Brazilian Amazon. I. The infection rates of Plasmodium brasilianum in non-human primates. Memorias do Instituto Oswaldo Cruz 90(3):331–339.PubMedGoogle Scholar
  68. Marsh, L. K. 1999. Ecological effect of the black howler monkey (Alouatta pigra) on fragmented forest in the Community Baboon Sanctuary. Ph. D. Thesis, Washington University, St. Louis.Google Scholar
  69. Marsh, L. K. 2003. The nature of fragmentation. In L. K. Marsh (ed.), Primates in Fragments: Ecology and Conservation.Marsh (pp. 1–10). New York: Kluwer Academic/Plenum Publ.Google Scholar
  70. Martins, S. de Souza 2000. Efeitos da fragmentação de habitat sobre a prevalência de parasitoses intestinais em Alouatta belzebul (Primates, Platyrrhini) na Amazônia Oriental. 2002. 86 f. Dissertação (Mestrado) – Curso de Mestrado em Zoologia, Universidade Federal do Pará, Museu Paraense Emílio Goeldi, Belém.Google Scholar
  71. McGrew, W. C., Tutin, C. E. G., Collins, D. A. and File, S. K. 1989. Intestinal parasites of sympatric Pan troglodytes and Papio spp. at two sites: Gombe (Tanzania) and Mt. Assirik (Senegal). American Journal of Primatology 17(2):147–155.CrossRefGoogle Scholar
  72. Michaud, C., Tantalean, M., Ique, C., Montoya, E. and Gonzalo, A. 2003. A survey for helminth parasites in feral New World non-human primate populations and its comparison with parasitological data from man in the region. Journal of Medical Primatology 32(6):341–345.PubMedCrossRefGoogle Scholar
  73. Milton, K. 1996. Effects of bot fly (Alouattamyia baeri) parasitism on a free-ranging howler (Alouatta palliata) population in Panama. Journal of Zoology (Lond) 239:39–63.Google Scholar
  74. Monath, T. P. 2001. Yellow fever. Lancet Infectious Diseases 1:11–20.PubMedCrossRefGoogle Scholar
  75. Muller-Graf, C. D. M., Collins, D. A. and Woolhouse, M. E. J. 1997. Schistosoma mansoni infection in a natural population of olive baboons (Papio cynocphalus anubis) in Gombe Stream National Park. Parasitology 115:621–627.PubMedCrossRefGoogle Scholar
  76. Muñoz, D., Estrada, A., Naranjo, E. and Ochoa, S. 2006. Foraging ecology of howler monkeys in a cacao (Theobroma cacao) plantation in Comalcalco, Mexico. American Journal of Primatology 68(2):127–142.PubMedCrossRefGoogle Scholar
  77. Norconk, M. A. and Grafton, B. W. 2003. Changes in forest composition and potential feeding tree availability on a small land-bridge island in Lago Guri, Venezuela. In L. K.Marsh (ed.), Primates in Fragments: Ecology and Conservation (pp. 211–227). New York: Kluwer Academic/Plenum Publ.Google Scholar
  78. Nunn, C. L., Altizer, S., Jones, K. E. and Sechrest, W. 2003. Comparative Tests of parasite species richness in Primates. American Naturalist 162:597–614.PubMedCrossRefGoogle Scholar
  79. Nunn, C. L. and Altizer, S. M. 2005. The Global Mammal Parasite Database: An online resource for infectious disease records in wild primates. Evolutionary Anthropology 14:1–2.CrossRefGoogle Scholar
  80. Nunn, C. L. and Heymann, E. W. 2005. Malaria infection and host behavior: A comparative study of Neotropical primates. Behavioral Ecology and Sociobiology 59:30–37.CrossRefGoogle Scholar
  81. Nunn, C. L., Altizer, S. M., Sechrest, W. and Cunningham, A. A. 2005. Latitudinal gradients of parasite species richness in primates. Diversity and Distributions 11:249–256CrossRefGoogle Scholar
  82. Nunn, C. L. and Altizer, S. M. 2006. Infectious Diseases in Primates: Behavior, Ecology and Evolution. New York: Oxford University Press.Google Scholar
  83. Nunn, C. L. and Dokey A. T.-W. 2006. Ranging patterns and parasitism in primates. Biology Letters 2:351–354.PubMedCrossRefGoogle Scholar
  84. Ocaido, M., Dranzoa, C. and Cheli, P. 2003. Gastrointestinal parasites of baboons (Papio anubis) interacting with humans in West Bugwe Forest Reserve, Uganda. African. Journal of Ecology 41(4):356–359.Google Scholar
  85. Palmer, S. R., Soulsby, L, and Simpson, D. I. H. 1998. Zoonoses. Biology, clinical practice and public health control. Oxford: Oxford University Press.Google Scholar
  86. Pedersen, A. B., Altizer, S. M., Poss, M., Cunningham, A. A. and Nunn C. L. 2005. Patterns of host specificity and transmission among parasites of wild primates. International Journal for Parasitology 35:647–657.PubMedCrossRefGoogle Scholar
  87. Phillips, K. A., Haas, M. E., Grafton, B. W. and Yrivarren, M. 2004. Survey of the gastrointestinal parasites of the primate community at Tambopata National Reserve, Peru. Journal of Zoology 264(2):149–151.CrossRefGoogle Scholar
  88. Plumptre, A. J. and Reynolds, V. 1994. The effect of selective logging on the primate populations in the Budongo Forest Reserve, Uganda. Journal of Applied Ecology 31(4):631–641CrossRefGoogle Scholar
  89. Pollard, A. J. and Dobson, A. R. 2000. Emerging infectious diseases in the 21st century. Current Opinion in Infectious Diseases 13:265–275.PubMedGoogle Scholar
  90. Pope, B. L. 1966. Some parasites of the howler monkey of northern Argentina. Journal of Parasitology 52:166–168.PubMedCrossRefGoogle Scholar
  91. Pope, T. R. 1998. Effects of demographic change on group kin structure and gene dynamics of populations of red howling monkeys. Journal of Mammalogy 79(3):692–712.CrossRefGoogle Scholar
  92. Poulin, R. 1994. Meta-analysis of parasite induced behavioural changes. Animal Behaviour 48:137–146.CrossRefGoogle Scholar
  93. Pozo-Montuy, G. and Serio-Silva, J. C. 2007. Movement and resource use by a group of Alouatta pigra in a forest fragment in Balancán, México. Primates 48(2):102–107.PubMedCrossRefGoogle Scholar
  94. Prieto, O. H., Santa Cruz, A. M., Scheibler, N., Borda, J. T. and Gomez, L. G. 2002. Incidence and external morphology of the nematode Trypanoxyuris (Hapaloxyuris) callithricis, isolated from black-and-gold howler monkeys (Alouatta caraya) in Corrientes, Argentina. Laboratory Primate Newsletter 41(3):12–14.Google Scholar
  95. Rivera, A. and Calme, S. (2006). Forest fragmentation and its effects on the feeding ecology of black howlers (Alouatta pigra) from the Calakmul area is Mexico. In A. Estrada, P. A. Garber, M. S. M. Pavelka and L. Luecke (eds.), New Perspectives in the Study of Mesoamerican Primates: Distribution, Ecology, Behavior, and Conservation (pp. 189–213). New York:Springer.CrossRefGoogle Scholar
  96. Rudran, R. and Fernandez-Duque, E. 2003. Demographic changes over thirty years in a red howler population in Venezuela. International Journal of Primatology 24(5):925–947.CrossRefGoogle Scholar
  97. Santa Cruz, A. C. M., Borda, J. T., Patiño, E. M., Gomez, L. and Zunino, G. E. 2000a. Habitat fragmentation and parasitism in howler monkeys (Alouatta caraya). Neotropical Primates 8(4):146–148.Google Scholar
  98. Santa Cruz, A. C. M., Prieto, O. H., Roux, J. P., Patiño, E .M., Borda, J. T., Gomez, L. and Schiebler, N. 2000b. Endo y ectoparasitosis en el mono aullador (Alouatta caraya) (Humboldt, 1812), Mammalia, Cebidae, Informe Preliminar. Comunicaciones Científicasy Tecnológicas, Universidad Nacional del Nordeste.Google Scholar
  99. Santa Cruz, A.C.M., Borda, J.T., Patiño, E.M., Prieto, O.H., Scheibler, N., González, A.O., Comolli, J.A., Zunino, G.E. and Gómez, L.G. 2003. Criptosporidiosis en mono aullador (Alouatta caraya Humboldt, 1812) en semicautiverio en Corrientes, Argentina. Comunicaciones Científicas y Tecnológicas, Universidad Nacional del Nordeste.Google Scholar
  100. Santos, M. V. S., Ueta, M. T. and Setz, E. Z. F. 2005. Levantamento de helmintos intestinais em bugio- ruivo, Alouatta guariba (Primates, atelidae), na mata de ribeirão cachoeira no Distrito de Souzas/Campinas, SP. Congresso Brasileiro de Parasitologia, Porto Alegre, RS, Brasil.Google Scholar
  101. Semple, S., Cowlishaw, G. and Bennett, P. M. 2002. Immune system evolution among anthropoid primates: parasites, injuries and predators. Proceedings of the Royal Society of London. Series B 269:1031–1037.Google Scholar
  102. Solomons, N. W. and Scott, M. E. 1994. Nutrition status of host populations influences parasitic infections. In M. E. Scott and G. Smith (eds.), Parasitic and infectious diseases (pp. 101–114). New York: Academic Press.Google Scholar
  103. Stoner, K. E. 1995. Dental pathology in Pongo satyrus borneensis. American Journal of Physical Anthropology 98(3):307–321.PubMedCrossRefGoogle Scholar
  104. Stoner, K. E. 1996. Prevalence and intensity of intestinal parasites in mantled howling monkeys (Alouatta palliata) in northeastern Costa Rica: Implications for conservation biology. Conservation Biology 10(2):539–546.CrossRefGoogle Scholar
  105. Stoner K. E., Gonzalez-Di Pierro, A. M. and Maldonado-Lopez, S. 2005. Infecciones de parásitos intestinales de primates: implicaciones para la conservación. Universidad y Ciencia (Sp. issue II):61–72.Google Scholar
  106. Stoner, K. E. and Gonzalez -Di Perro, A. M. 2006. Intestinal parasite infections in Alouatta pigra in tropical rainforest in Lacandona, Chiapas, Mexico: implications for behavioral ecology and conservation. In A. Estrada, P. A. Garber, M. S. M. Pavelka and L. Luecke (eds.), New Perspectives in the Study of Mesoamerican Primates: Distribution, Ecology, Behavior, and Conservation (pp. 215–240). New York: Springer.CrossRefGoogle Scholar
  107. Stuart, M. D., Greenspan, L. L., Glander, K. E. and Clarke, M. 1990. A coprological survey of parasites of wild mantled howling monkeys, Alouatta palliata palliata. Journal of Wildlife Disease 26:547–549.Google Scholar
  108. Stuart, M. D., Strier, K. B., and Pierberg, S. M. 1993. A coprological survey of wild muriquis, Brachyteles arachnoides, and brown howling monkeys, Alouatta fusca. Proceedings of the Helminthological Society of Washington 60(1):111–115.Google Scholar
  109. Stuart, M. D. and Strier, K. B. 1995. Primates and parasites: A case for a multidisciplinary approach. International Journal of Primatology 16(4):577–593.CrossRefGoogle Scholar
  110. Stuart, M. D., Pendergast, V., Rumfelt, S., Pierberg, S., Greenspan, L., Glander, K. and Clarke M. 1998. Parasites of wild howlers (Alouatta spp.). International Journal of Primatology 19(3):493–512.CrossRefGoogle Scholar
  111. Taylor, L. H., Latham, S. M. and Woolhouse, E. J. 2001. Risk factors for human disease emergence. Philosophical Transactions of the Royal Society of London. Series B 356:983–989.PubMedCrossRefGoogle Scholar
  112. Thatcher, V. E. and Porter, J. A. Jr. 1968. Some helminth parasites of Panamanian primates. Transactions of the American Microscopical Society 87(2):186–196.PubMedCrossRefGoogle Scholar
  113. Travi, B. L., Colillas, O. J. and Segura, E. L. 1986. Natural trypanosome infection in Neotropical monkeys with special reference to Saimiri sciureus. In D. M. Taub and F. A. King (eds.), Current Perspectives in Primate Biology (pp. 296–306). New York: Van Nostrand Rehinold.Google Scholar
  114. Vandamme, A. 2004. Frequent “natural” zoonotic transmission of simian foamy virus to humans. Aids reviews 6(2):118.Google Scholar
  115. Vasconcelos, P. F. C., Sperb, A. F., Monteiro, H. A. O., Tortes, M. A. N., Sousa, M. R. S., Vasconcelos, H. B., Mardini, L. B. L. F. and Rodrigues, S. G. 2003. Isolations of yellow fever virus from Haemagogus leucocelaenus in Rio Grande do Sul State, Brazil. Transactions of the Royal Society of Tropical Medicine and Hygiene 97:60–62.PubMedCrossRefGoogle Scholar
  116. Venturini, L., Santa Cruz, A. M., González, J. A., Comolli, J. A., Toccalino, P. A. and Zunino, G. E. 2003. Presencia de Giardia duodenalis (Sarcomastigophora, Hexamitidae) en mono aullador (Alouatta caraya) de vida silvestre. Comunicaciones Científicas y Tecnológicas, Universidad Nacional del Nordeste.Google Scholar
  117. Vitazkova, S. K. and Wade, S. E. 2006. Parasites of free-ranging black howler monkeys (Alouatta pigra) from Belize and Mexico. American Journal of Primatology 68(11):1089–1097.PubMedCrossRefGoogle Scholar
  118. Volney, B., Pouliquen, J. F., De Thoisy, B. and Fandeur, T. 2002. A sero-epidemiological study of malaria in human and monkey populations in French Guiana. Acta Tropica 82(1):11–23.PubMedCrossRefGoogle Scholar
  119. Wallis, J. and Lee, D. R. 1999. Primate conservation: the prevention of disease transmission. International Journal of Primatology 20:803–826.CrossRefGoogle Scholar
  120. Walther B. A., Cotgreave, P., Gregory, R. D., Price, R .D. and Clayton, D. H. 1995. Sampling effort and parasite species richness. Parasitology Today 11:306–310.PubMedCrossRefGoogle Scholar
  121. Wolfe, N. D., Escalante, A. A., Karesh, W. B., Kilbourn, A., Spielman, A. and Lal, A. A. 1998. Wild primate populations in emerging infectious disease research: the missing link? Emerging Infectious Diseases 4:149–158.PubMedCrossRefGoogle Scholar
  122. Yamashita J. 1963. Ecological relationships between parasites and primates. 1:Helminth parasites and primates. Primates 4:1–96.CrossRefGoogle Scholar
  123. Young, O. P. 1981. Chasing behavior between males within a howler monkey troop. Primates 22:424–426.CrossRefGoogle Scholar
  124. Zar, J. H. 1999. Biostatistical Analysis. 4th Edition. New Jersey: Prentice-Hall.Google Scholar
  125. Zunino, G. E., Kowaleski, M., Oklander, L. and Gonzalez, V. 2007. Habitat fragmentation and population size of the black and gold howler monkey (Alouatta caraya) in a semideciduous forest in northern Argentina. American Journal of Primatology 69(9):966–975.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Martin M. Kowalewski
    • 1
  • Thomas R. Gillespie
  1. 1.Estacion Biologica Corrientes-MACN, Corrientes, Argentina Department of AnthropologyUniversity of IllinoisUrbana-ChampaignUSA

Personalised recommendations