International Journal of Primatology

, Volume 34, Issue 6, pp 1137–1152 | Cite as

Predictors of Parasitism in Wild White-Faced Capuchins (Cebus capucinus)

  • Nigel A. Parr
  • Linda M. Fedigan
  • Susan J. Kutz


Parasite infections in wildlife are influenced by many factors including host demography, behavior and physiology, climate, habitat characteristics, and parasite biology and ecology. White-faced capuchins (Cebus capucinus) host a suite of gastrointestinal and pulmonary parasites, yet the mechanisms affecting host susceptibility and parasite transmissibility have not been examined in this host species. We used the information-theoretic approach (Akaike’s information criterion) and traditional null-hypothesis testing to determine which host characteristics, behaviors, or environmental factors affected the presence of two prevalent capuchin parasites (Filariopsis barretoi and Strongyloides sp.) as well as parasite species richness in four groups of wild capuchins from September 2007 to January 2008 and January to August 2009. Older capuchins were more likely to be infected with Filariopsis barretoi and had higher parasite species richness. Age-biased nematode infections may stem from age differences in capuchin behavior and physiology while high species richness likely results from long- term exposure to numerous parasite species. Infections with Strongyloides sp. were more likely to occur in the dry season when capuchins often descend to the forest floor to drink from terrestrial water sources, potentially increasing their risk of infection from soil-borne larvae. Capuchin behaviors were poor predictors of parasitism, as were female rank, host sex, home range size, and habitat quality. Many of our results were atypical for primate parasitology, suggesting that host–parasite interactions, and subsequently infection risk, may differ in highly seasonal habitats such as tropical dry forests where these monkeys occur.


Costa Rica Filariopsis Parasites Parasite species richness Platyrrhini Strongyloides Tropical dry forest 



We thank the following funding agencies for their support of this project: Government of Alberta (N. A. Parr), University of Calgary (N. A. Parr), Natural Sciences and Engineering Research Council of Canada (L. M. Fedigan, S. J. Kutz), Canada Research Chairs program (L. M. Fedigan). We thank Roger Segura Blanco, the staff of the Área de Conservación Guanacaste, and the Ministerio de Ambiente y Energia of Costa Rica for their support and for facilitating this research. We are grateful to Krisztina Mosdossy and Amanda Melin for their roles in collecting behavioral and botanical data, in addition to fecal samples. We are also grateful to Brandon Klüg, Mackenzie Bergstrom, Valerie Schoof, Teresa Holmes, Adrienne Tecza, Sarah Millus, Anne-Sophie Pellier, Reid Jackson, Barb Kowalzik, and Chelsea Lees for assistance in collecting fecal samples. We thank Adrián Guadamuz Chavarria for his help with tree identification and transect data. Finally, we thank Joanna Setchell and two anonymous reviewers for their comments and assistance in greatly improving the manuscript.


  1. Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control, 19(6), 716–723.CrossRefGoogle Scholar
  2. Altizer, S., Nunn, C. L., Thrall, P. H., Gittleman, J. L., Antonovics, J., Cunningham, A. A., et al. (2003). Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics, 34, 517–547.Google Scholar
  3. Altizer, S., Dobson, A., Hosseini, P., Hudson, P., Pascual, M., & Rohani, P. (2006). Seasonality and the dynamics of infectious diseases. Ecology Letters, 9(4), 467–484.PubMedCrossRefGoogle Scholar
  4. Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49(3/4), 227–267.PubMedCrossRefGoogle Scholar
  5. Anderson, R. M., & May, R. M. (1979). Population biology of infectious diseases: Part I. Nature, 280(5721), 361–367.PubMedCrossRefGoogle Scholar
  6. Appleton, C. C., & Henzi, S. P. (1993). Environmental correlates of gastrointestinal parasitism in montane and lowland baboons in Natal, South Africa. International Journal of Primatology, 14(4), 623–635.CrossRefGoogle Scholar
  7. Arneberg, P. (2001). An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence. Ecography, 24(3), 352–358.Google Scholar
  8. Bakuza, J., & Nkwengulila, G. (2009). Variation over time in parasite prevalence among free-ranging chimpanzees at Gombe National Park, Tanzania. International Journal of Primatology, 30(1), 43–53.CrossRefGoogle Scholar
  9. Bergstrom, M. L., & Fedigan, L. M. (2010). Dominance among female white-faced capuchin monkeys (Cebus capucinus): Hierarchical linearity, nepotism, strength and stability. Behaviour, 147(7), 899–931.CrossRefGoogle Scholar
  10. Bordes, F. r., Morand, S., Kelt, D. A., & Vuren, D. H. V. (2009). Home range and parasite diversity in mammals. The American Naturalist, 173(4), 467–474.PubMedCrossRefGoogle Scholar
  11. Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: A practical information-theoretic approach (2nd ed.). New York: Springer Science+Business Media.Google Scholar
  12. Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83(4), 575–583.PubMedCrossRefGoogle Scholar
  13. Campos, F. A., & Fedigan, L. M. (2009). Behavioral adaptations to heat stress and water scarcity in white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica. American Journal of Physical Anthropology, 138(4), 101–111.Google Scholar
  14. Chapman, C. (1987). Flexibility in diets of three species of Costa Rican primates. Folia Primatologica, 49, 90–105.CrossRefGoogle Scholar
  15. Chapman, C. (1988). Patterns of foraging and range use by three species of Neotropical primates. Primates, 29(2), 177–194.CrossRefGoogle Scholar
  16. Chapman, C. A., Gillespie, T. R., & Goldberg, T. L. (2005). Primates and the ecology of their infectious diseases: how will anthropogenic change affect host-parasite interactions? Evolutionary Anthropology, 14(4), 134–144.CrossRefGoogle Scholar
  17. Chapman, C. A., Speirs, M. L., Gillespie, T. R., Holland, T., & Austad, K. M. (2006). Life on the edge: gastrointestinal parasites from the forest edge and interior primate groups. American Journal of Primatology, 68, 397–409.PubMedCrossRefGoogle Scholar
  18. Chinchilla, M., Guerrero, O. M., Gutiérrez-Espeleta, G. A., Sánchez, R., & Campos, I. V. (2007). Parásitos en monos carablanca Cebus capucinus (Primates: Cebidae) de Costa Rica. Parasitología Latinoamericana, 62(3–4), 170–175.Google Scholar
  19. Chinchilla, M., Urbani, B., Valerio, I., & Vanegas, J. C. (2010). Parasitosis intestinal en monos capuchinos cariblancos Cebus capucinus (Primates: Cebidae) de un área protegida en la provincia de Limón, noreste de Costa Rica. Revista de Biología Tropical, 58(4), 1335–1346.PubMedGoogle Scholar
  20. Cogswell, F. (2007). Parasites of non-human primates. In D. G. Baker (Ed.), Flynn's parasites of laboratory animals (2nd ed., pp. 693–743). Ames: Blackwell.CrossRefGoogle Scholar
  21. Coop, R. L., & Holmes, P. H. (1996). Nutrition and parasite interaction. International Journal for Parasitology, 26(8/9), 951–962.PubMedCrossRefGoogle Scholar
  22. Côté, I. M., & Poulin, R. (1995). Parasitism and group size in social animals: a meta-analysis. Behavioral Ecology, 6(2), 159–165.CrossRefGoogle Scholar
  23. Cross, P. C., Drewe, J., Patrek, V., Pearce, G., Samuel, M. D., & Delahay, R. J. (2009). Wildlife population structure and parasite transmission: implications for disease management. In R. J. Delahay, G. C. Smith, & M. R. Hutchings (Eds.), Management of disease in wild mammals (pp. 9–29). Tokyo: Springer Science+Business Media.CrossRefGoogle Scholar
  24. Dobson, A. P., & Hudson, P. J. (1992). Regulation and stability of a free-living host-parasite system: Trichostrongylus tenuis in red grouse. II. Population models. Journal of Animal Ecology, 61(2), 487–498.CrossRefGoogle Scholar
  25. Dupain, J., Van Elsacker, L., Nell, C., Garcia, P., Ponce, F., & Huffman, M. A. (2002). New evidence for leaf swallowing and Oesophagostomum infection in Bonobos (Pan paniscus). International Journal of Primatology, 23(5), 1053–1062.CrossRefGoogle Scholar
  26. Fedigan, L., & Jack, K. (2012). Tracking neotropical monkeys in Santa Rosa: lessons from a regenerating Costa Rican dry forest. In P. M. Kappeler & D. P. Watts (Eds.), Long-term field studies of pgrimates (pp. 165–184). Berlin and Heidelberg: Springer Science+Business Media.CrossRefGoogle Scholar
  27. Fragaszy, D. M. (1990). Sex and age differences in the organization of behavior in wedge-capped capuchins, Cebus olivaceus. Behavioral Ecology, 1(1), 81–94.CrossRefGoogle Scholar
  28. Fragaszy, D. M., Visalberghi, E., & Fedigan, L. M. (2004). The complete capuchin: The biology of the genus Cebus. Cambridge: Cambridge University Press.Google Scholar
  29. Freeland, W. J. (1976). Pathogens and the evolution of primate sociality. Biotropica, 8(1), 12–24.CrossRefGoogle Scholar
  30. Freese, C. H. (1978). The behavior of white-faced capuchins (Cebus capucinus) at a dry-season waterhole. Primates, 19(2), 275–286.CrossRefGoogle Scholar
  31. Getz, W. M., Fortmann-Roe, S., Cross, P. C., Lyons, A. J., Ryan, S. J., & Wilmers, C. C. (2007). LoCoH: Nonparameteric kernel methods for constructing home ranges and utilizaton distributions. PLoS ONE, 2(2), e207.PubMedCrossRefGoogle Scholar
  32. Gilbert, K., & Stouffer, P. (1995). Variation in substrate use by white-faced capuchins. Human Evolution, 10(4), 265–269.CrossRefGoogle Scholar
  33. Gillespie, T. R., & Chapman, C. A. (2008). Forest fragmentation, the decline of an endangered primate, and changes in host–parasite interactions relative to an unfragmented forest. American Journal of Primatology, 70(3), 222–230.PubMedCrossRefGoogle Scholar
  34. Gillespie, T. R., Chapman, C. A., & Grenier, E. C. (2005). Effects of logging on gastrointestinal parasite infections and infection risk in African primates. Journal of Applied Ecology, 42, 699–707.CrossRefGoogle Scholar
  35. Gotoh, S. (2000). Regional differences in the infection of wild Japanese macaques by gastrointestinal helminth parasites. Primates, 41(3), 291–298.CrossRefGoogle Scholar
  36. Hamilton, W. D., & Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science, 218(4570), 384–387.PubMedCrossRefGoogle Scholar
  37. Hausfater, G., & Meade, B. J. (1982). Alternation of sleeping groves by yellow baboons (Papio cynocephalus) as a strategy for parasite avoidance. Primates, 23(2), 287–297.CrossRefGoogle Scholar
  38. Horii, Y., Imada, I., Yanagida, T., Usui, M., & Mori, A. (1982). Parasite changes and their influence on the body weight of Japanese monkeys (Macaca fuscata fuscata) of the Koshima troop. Primates, 23(3), 416–431.CrossRefGoogle Scholar
  39. Hudson, P. J., Dobson, A. P., & Newborn, D. (2002a). Parasitic worms and population cycles of red grouse. In A. Berryman (Ed.), Population cycles. New York: Oxford University Press.Google Scholar
  40. Hudson, P. J., Rizzoli, A., Grenfell, B. T., Heesterbeek, H., & Dobson, A. P. (Eds.). (2002b). The ecology of wildlife diseases. New York: Oxford University Press.Google Scholar
  41. Huffman, M. A. (1997). Current evidence for self-medication in primates: a multidisciplinary perspective. American Journal of Physical Anthropology, 104(S25), 171–200.CrossRefGoogle Scholar
  42. Huffman, M. A., Gotoh, S., Turner, L. A., Hamai, M., & Toshida, K. (1997). Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale mountains, Tanzania. Primates, 38(2), 111–125.CrossRefGoogle Scholar
  43. Janson, C. (1985). Aggressive competition and individual food consumption in wild brown capuchin monkeys (Cebus apella). Behavioral Ecology and Sociobiology, 18(2), 125–138.CrossRefGoogle Scholar
  44. Jones, C. (2005). Behavioral flexibility in primates: Causes and consequences. New York: Springer Science+Business Media.CrossRefGoogle Scholar
  45. Krief, S., Jamart, A., Mahé, S., Leendertz, F. H., Mätz-Rensing, K., Crespeau, F., et al. (2008). Clinical and pathologic manifestation of oesophagostomosis in African great apes: does self-medication in wild apes influence disease progression? Journal of Medical Primatology, 37(4), 188–195.PubMedCrossRefGoogle Scholar
  46. Lindenfors, P., Nunn, C. L., Jones, K. E., Cunningham, A. A., Sechrest, W., & Gittleman, J. L. (2007). Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density. Global Ecology and Biogeography, 16(4), 496–509.CrossRefGoogle Scholar
  47. Lo, C. M., Morand, S., & Galzin, R. (1998). Parasite diversity/host age and size relationship in three coral-reef fishes from French Polynesia. International Journal for Parasitology, 28(11), 1695–1708.PubMedCrossRefGoogle Scholar
  48. Loehle, C. (1995). Social barriers to pathogen transmission in wild animal populations. Ecology, 76(2), 326–335.CrossRefGoogle Scholar
  49. Lok, J. B. (2007). Strongyloides stercoralis: a model for translational research on parasitic nematode biology. In WormBook: The online review of C. elegans biology. Available at:
  50. MacIntosh, A. J. J., Jacobs, A., Garcia, C., Shimizu, K., Mouri, K., Huffman, M. A., et al. (2012). Monkeys in the middle: parasite transmission through the social network of a wild primate. PLoS ONE, 7(12), e51144.PubMedCrossRefGoogle Scholar
  51. MacKinnon, K. C. (2006). Food choice by juvenile capuchin monkeys (Cebus capucinus) in a tropical dry forest. In A. Estrada, P. A. Garber, M. S. M. Pavelka, & L. Luecke (Eds.), New perspectives in the study of Mesoamerican primates: Distribution, ecology, behavior, and conservation (pp. 349–365). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  52. McLennan, M. R., & Huffman, M. A. (2012). High frequency of leaf swallowing and its relationship to intestinal parasite expulsion in “village” chimpanzees at Bulindi, Uganda. American Journal of Primatology, 74(7), 642–650.PubMedCrossRefGoogle Scholar
  53. Melin, A. D. (2011). Polymorphic colour vision and foraging in white-faced capuchins: Insights from field research and simulations of monkey vision. Unpublished Ph.D. Dissertation, University of Calgary.Google Scholar
  54. Melin, A. D., Fedigan, L. M., Young, H. C., & Kawamura, S. (2010). Can color vision variation explain sex differences in invertebrate foraging by capuchin monkeys? Current Zoology, 56(3), 300–312.Google Scholar
  55. Melin, A. D., Hiramatsu, C., Parr, N., Matsushita, Y., Kawamura, S., & Fedigan, L. M. (in press). The behavioural ecology of colour vision: frugivory as a selective force. International Journal of Primatology.Google Scholar
  56. Meyers, L. A., Pourbohloul, B., Newman, M. E. J., Skowronski, D. M., & Brunham, R. C. (2005). Network theory and SARS: predicting outbreak diversity. Journal of Theoretical Biology, 232(1), 71–81.PubMedCrossRefGoogle Scholar
  57. Møller, A. P., Dufva, R., & Allander, K. (1993). Parasites and the evolution of host social behavior. Advances in the Study of Behavior, 22, 65–102.Google Scholar
  58. Müller-Graf, C. D. M., Collins, D. A., & Woolhouse, M. E. J. (1996). Intestinal parasite burden in five troops of olive baboons (Papio cynocephalus anubis) in Gombe Stream National Park, Tanzania. Parasitology, 112(5), 489–497.PubMedCrossRefGoogle Scholar
  59. Nunn, C. L., & Altizer, S. (2006). Infectious diseases in primates. New York: Oxford University Press.CrossRefGoogle Scholar
  60. Nunn, C. L., & Dokey, A. T.-W. (2006). Ranging patterns and parasitism in primates. Biology Letters, 2(3), 351–354.PubMedCrossRefGoogle Scholar
  61. Nunn, C. L., Gittleman, J. L., & Antonovics, J. (2000). Promiscuity and the primate immune system. Science, 290(5494), 1168–1170.PubMedCrossRefGoogle Scholar
  62. Nunn, C. L., Altizer, S., Jones, K. E., & Sechrest, W. (2003). Comparative tests of parasite species richness in primates. The American Naturalist, 162(5), 597–614.PubMedCrossRefGoogle Scholar
  63. Parr, N., Campos, F., Childers, A., Fedigan, L., & Jack, K. (2008). Dry season ranging behaviour and intergroup relations in white-faced capuchins (Cebus capucinus) at Santa Rosa National Park, Costa Rica [abstract]. American Journal of Primatology, 70(S1), 53.Google Scholar
  64. Parr, N. A., Fedigan, L. M., & Kutz, S. J. (2013). A coprological survey of parasites in white-faced capuchins (Cebus capucinus) from Sector Santa Rosa, ACG, Costa Rica. Folia Primatologica, 84(2), 102–114.CrossRefGoogle Scholar
  65. Perry, S. (1996). Female-female social relationships in wild white-faced capuchin monkeys, Cebus capucinus. American Journal of Primatology, 40(2), 167–182.CrossRefGoogle Scholar
  66. Perry, S. (1997). Male–female social relationships in wild white-faced capuchins (Cebus capucinus). Behaviour, 134(7/8), 477–510.CrossRefGoogle Scholar
  67. Perry, S. (1998). Male-male social relationships in wild white-faced capuchins, Cebus capucinus. Behaviour, 135(2), 139–172.CrossRefGoogle Scholar
  68. Peters, R. H., Cloutier, S., Dubé, D., Evans, A., Hastings, P., Kaiser, H., et al. (1988). The allometry of the weight of fruit on trees and shrubs in Barbados. Oecologia, 74(4), 612–616.Google Scholar
  69. Petrželková, K. J., Hasegawa, H., Appleton, C. C., Huffman, M. A., Archer, C. E., Moscovice, L. R., et al. (2010). Gastrointestinal parasites of the chimpanzee population introduced onto Rubondo Island National Park, Tanzania. American Journal of Primatology, 72, 307–316.Google Scholar
  70. Poulin, R., & Morand, S. (2000). The diversity of parasites. Quarterly Review of Biology, 75(3), 277–293.PubMedCrossRefGoogle Scholar
  71. R Core Team. (2013). R: A language and environment for statistical computing. (Version 3.0.1). Vienna: R Foundation for Statistical Computing.Google Scholar
  72. Rose, L. (1994). Sex differences in diet and foraging behavior in white-faced capuchins (Cebus capucinus). International Journal of Primatology, 15(1), 95–114.CrossRefGoogle Scholar
  73. Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science, 308, 648–652.PubMedCrossRefGoogle Scholar
  74. Smith, P. H., Wiles, S. E., Malone, J. B., Jr., & Monahan, C. M. (2007). Collection, preservation, and diagnostic methods. In D. G. Baker (Ed.), Flynn's parasites of laboratory animals (2nd ed.). Ames, IA: Blackwell.Google Scholar
  75. Stoner, K. E., & González Di Pierro, A. M. (2006). Intestinal parasitic infections in Alouatta pigra in tropical rainforest in Lacandona, Chiapas, Mexico: implications for behavioral ecology and conservation. In A. Estrada, P. A. Garber, M. Pavelka, & L. Luecke (Eds.), New perspectives in the study of Mesoamerican primates (pp. 215–240). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  76. Stuart, M. D., & Strier, K. B. (1995). Primates and parasites: a case for a multidisciplinary approach. International Journal of Primatology, 16(4), 577–593.CrossRefGoogle Scholar
  77. Wilson, K., Bjørnstad, O. N., Dobson, A. P., Merler, S., Poglayen, G., Randolph, S. E., et al. (2002). Heterogeneities in macroparasite infections: patterns and processes. In P. Hudson, A. Rizzoli, B. T. Grenfell, H. Heesterbeek, & A. P. Dobson (Eds.), The ecology of wildlife diseases (pp. 6–44). New York: Oxford University Press.Google Scholar
  78. Zuk, M., & McKean, K. A. (1996). Sex differences in parasite infections: patterns and processes. International Journal for Parasitology, 26(10), 1009–1024.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Nigel A. Parr
    • 1
  • Linda M. Fedigan
    • 1
  • Susan J. Kutz
    • 2
  1. 1.Department of AnthropologyUniversity of CalgaryCalgaryCanada
  2. 2.Faculty of Veterinary MedicineUniversity of CalgaryCalgaryCanada

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