International Journal of Primatology

, Volume 34, Issue 6, pp 1081–1104 | Cite as

Sampling Effort in Neotropical Primate Diet Studies: Collective Gains and Underlying Geographic and Taxonomic Biases

  • Joseph E. Hawes
  • Armando M. Calouro
  • Carlos A. Peres


Primates are among the most observable and best studied mammalian orders, yet the distribution of sampling effort by primatologists has inevitably concentrated on a few genera and a limited number of study sites. We present the first systematic review of sampling effort and associated biases in wild primate field research, focusing on dietary studies across the Neotropics. Our literature review of all 24 neotropical primate ecospecies spans 42 years (1969–2011) and covers 290 dietary studies at 164 study sites across 17 countries. We use a standardized measure of sampling effort to assimilate data sets derived from multiple methodologies and attempt to understand the distribution of effort (total equivalent to 193,804 h) using geographic variables and primate species traits. Results indicate that there are both geographic and taxonomic biases, with sampling effort generally skewed towards large-bodied species occupying large geographic ranges, and concentrated at a select few primatology research hubs. We also note that full primate assemblages at any given study site are rarely investigated. Our assessment thus reveals severely undersampled primate taxa and geographic regions that must be considered in future research. Current biases could be ameliorated by deliberately targeting poorly studied genera anywhere in their geographic distribution, well-studied genera in poorly studied regions, and striving to study multiple sympatric taxa within a single site. Although continued inequalities in sampling effort are probably inevitable, this study shows that this need not inhibit successful compilations and meta-analyses, provided that adequate data on feeding records and sampling effort can be made available.


Diet Feeding ecology Mesoamerica Platyrrhini South America 



This study was funded by a NERC doctoral studentship to JEH. We wish to thank all researchers who have contributed to the current knowledge of primate field studies across the Neotropics. We thank J. Setchell, E. Heymann, and four anonymous reviewers for comments on earlier versions of the manuscript. This paper was co-written during a CAPES-funded visiting fellowship by CAP to Museu Goeldi, Brazil.

Supplementary material

10764_2013_9738_MOESM1_ESM.docx (125 kb)
ESM 1 (DOCX 125 kb)


  1. Alfaro, J. W. L., Silva, J. S. E., & Rylands, A. B. (2012). How different are robust and gracile capuchin monkeys? An argument for the use of Sapajus and Cebus. American Journal of Primatology, 74, 273–286.PubMedCrossRefGoogle Scholar
  2. Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour, 49, 227–266.PubMedCrossRefGoogle Scholar
  3. Antonelli, A., & Rodriguez, V. (2009). Brazil should facilitate research permits. Conservation Biology, 23, 1068–1069.PubMedCrossRefGoogle Scholar
  4. Arino, O., Bicheron, P., Achard, F., Latham, J., Witt, R., & Weber, J.-L. (2008). GlobCover: the most detailed portrait of earth. ESA Bulletin, 136, 24–31.Google Scholar
  5. Beyer, H. L. (2004). Hawth’s analysis tools for ArcGIS. Available at
  6. Bowler, M., & Bodmer, R. E. (2011). Diet and food choice in Peruvian red uakaris (Cacajao calvus ucayalii): selective or opportunistic seed predation? International Journal of Primatology, 32, 1109–1122.CrossRefGoogle Scholar
  7. Brito, D., Grelle, C. E. V., & Boubli, J. P. (2008). Is the Atlantic Forest protected area network efficient in maintaining viable populations of Brachyteles hypoxanthus? Biodiversity and Conservation, 17, 3255–3268.CrossRefGoogle Scholar
  8. Center for International Earth Science Information Network (CIESIN)/Columbia University, and Centro Internacional de Agricultura Tropical (CIAT). (2005). Gridded population of the world, version 3 (GPWv3): Population density grid. Palisades, NY: NASA Socioeconomic Data and Applications Center (SEDAC). Available at
  9. Chapman, C. A. (1989). Primate seed dispersal: the fate of dispersed seeds. Biotropica, 21, 148–154.CrossRefGoogle Scholar
  10. Chapman, C. A., Gautier-Hion, A., Oates, J. F., & Onderdonk, D. A. (1999). African primate communities: Determinants of structure and threats to survival. In J. G. Fleagle, C. H. Janson, & K. Reed (Eds.), Primate communities (pp. 1–37). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  11. Clutton-Brock, T. H. (1977). Primate ecology: Studies of feeding and ranging behaviour in lemurs, monkeys and apes. London: Academic Press.Google Scholar
  12. Coimbra-Filho, A., & Mittermeier, R. A. (Eds.). (1981). Ecology and behaviour of neotropical primates, Vol. 1. Rio de Janeiro: Academia Brasileira De Ciencias.Google Scholar
  13. Cristóbal-Azkarate, J., & Arroyo-Rodríguez, V. (2007). Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: effects of habitat fragmentation and implications for conservation. American Journal of Primatology, 69, 1013–1029.PubMedCrossRefGoogle Scholar
  14. Cunha, A. A., Grelle, C. E. V., & Boubli, J. P. (2009). Distribution, population size and conservation of the endemic muriquis (Brachyteles spp.) of the Brazilian Atlantic forest. Oryx, 43, 254–257.CrossRefGoogle Scholar
  15. Dew, J. L. (2003). Feeding ecology and seed dispersal. In J. M. Setchell & D. J. Curtis (Eds.), Field and laboratory methods in primatology: A practical guide (pp. 174–183). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  16. ESA. (2008). GlobCover Land Cover v2 2008 database. European Space Agency, European Space Agency GlobCover Project, led by MEDIAS-France. Available at
  17. Estrada, A., & Coates-Estrada, R. (1996). Tropical rain forest fragmentation and wild populations of primates at Los Tuxtlas, Mexico. International Journal of Primatology, 17, 759–783.CrossRefGoogle Scholar
  18. Estrada, A., Garber, P. A., Pavelka, M. S. M., & Luecke, L. (Eds.). (2006). New perspectives in the study of Mesoamerican primates: Distribution, ecology, behavior, and conservation. New York: Springer Science+Business Media.Google Scholar
  19. Felton, A. M., Felton, A., Lindenmayer, D. B., & Foley, W. J. (2009). Nutritional goals of wild primates. Functional Ecology, 23, 70–78.CrossRefGoogle Scholar
  20. Galetti, M., Giacomini, H. C., Bueno, R. S., Bernardo, C. S. S., Marques, R. M., Bovendorp, R. S., et al. (2009). Priority areas for the conservation of Atlantic forest large mammals. Biological Conservation, 142, 1229–1241.Google Scholar
  21. Garber, P. A., Estrada, A., Bicca-Marques, J. C., Heymann, E. W., & Strier, K. B. (Eds.). (2009). South American primates: Comparative perspectives in the study of behavior, ecology, and conservation. New York: Springer Science+Business Media.Google Scholar
  22. Gaston, K. J., & Blackburn, T. M. (1996). Conservation implications of geographic range size-body size relationships. Conservation Biology, 10, 638–646.CrossRefGoogle Scholar
  23. González-Zamora, A., Arroyo-Rodríguez, V., Chaves, Ó. M., Sánchez-López, S., Stoner, K. E., & Riba-Hernández, P. (2009). Diet of spider monkeys (Ateles geoffroyi) in Mesoamerica: current knowledge and future directions. American Journal of Primatology, 71, 8–20.PubMedCrossRefGoogle Scholar
  24. Google Inc. (2012). Google earth (Version Available at
  25. Hawes, J. E., & Peres, C. A. (2013). Ecological correlates of trophic status and frugivory in neotropical primates. Oikos. doi: 10.1111/j.1600-0706.2013.00745.x (in press).
  26. Heymann, E. W., & Aquino, R. (2010). Peruvian red uakaries (Cacajao calvus ucayalii) are not flooded-forest specialists. International Journal of Primatology, 31, 751–758.PubMedCrossRefGoogle Scholar
  27. Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965–1978.CrossRefGoogle Scholar
  28. Hohmann, G., Robbins, M. M., & Boesch, C. (2006). Feeding ecology in apes and other primates: Ecological, physical, and behavioral aspects. Cambridge: Cambridge University Press.Google Scholar
  29. IUCN. (2011). The IUCN red list of threatened species. Version 2011.2. Available at (Accessed November 10, 2011).
  30. Kappeler, P. M., & Watts, D. P. (Eds.). (2012). Long-term field studies of primates. Berlin and Heidelberg: Springer-Verlag.Google Scholar
  31. Kierulff, M. C. M., & Rylands, A. B. (2003). Census and distribution of the golden lion tamarin (Leontopithecus rosalia). American Journal of Primatology, 59, 29–44.PubMedCrossRefGoogle Scholar
  32. Kodric-Brown, A., & Brown, J. H. (1993). Incomplete data sets in community ecology and biogeography: a cautionary tale. Ecological Applications, 3, 736.CrossRefGoogle Scholar
  33. Lehner, P. N. (1998). Handbook of ethological methods. Cambridge: Cambridge University Press.Google Scholar
  34. Link, A., & Di Fiore, A. (2006). Seed dispersal by spider monkeys and its importance in the maintenance of neotropical rain-forest diversity. Journal of Tropical Ecology, 22, 235–246.CrossRefGoogle Scholar
  35. Mace, G. M., Collar, N. J., Gaston, K. J., Hilton-Taylor, C., Akçakaya, H. R., Leader-Williams, N., et al. (2008). Quantification of extinction risk: IUCN's system for classifying threatened species. Conservation Biology, 22, 1424–1442.PubMedCrossRefGoogle Scholar
  36. Martín-López, B., Montes, C., Ramírez, L., & Benayas, J. (2009). What drives policy decision-making related to species conservation? Biological Conservation, 142, 1370–1380.CrossRefGoogle Scholar
  37. Mittermeier, R. A., Rylands, A. B., Coimbra-Filho, A., & Foseca, G. A. B. (Eds.). (1988). Ecology and behavior of neotropical primates, Vol. 2. Washington, DC: World Wildlife Fund.Google Scholar
  38. Mittermeier, R. A., & Van Roosmalen, M. G. M. (1981). Preliminary observations on habitat utilization and diet in eight Surinam monkeys. Folia Primatologica, 36, 1–39.CrossRefGoogle Scholar
  39. National Research Council. (2003). Nutrient requirements of nonhuman primates, 2nd revised edition. Washington, DC: The National Academies Press.Google Scholar
  40. Nelson, B. W., Ferreira, C. A. C., da Silva, M. F., & Kawasaki, M. L. (1990). Endemism centres, refugia and botanical collection density in Brazilian Amazonia. Nature, 345, 714–716.CrossRefGoogle Scholar
  41. Olesen, J. M., Bascompte, J., Dupont, Y. L., & Jordano, P. (2007). The modularity of pollination networks. Proceedings of the National Academy of Sciences of the USA, 104, 19891–19896.PubMedCrossRefGoogle Scholar
  42. Olson, D. M., Dinerstein, E., Wikramanayake, E. D., Burgess, N. D., Powell, G. V. N., Underwood, E. C., et al. (2001). Terrestrial ecoregions of the world: a new map of life on earth. BioScience, 51, 933.CrossRefGoogle Scholar
  43. Palminteri, S., Powell, G., Asner, G. P., & Peres, C. A. (2012). LiDAR measurements of canopy structure predict spatial distribution of a tropical mature forest primate. Remote Sensing of Environment, 127, 98–105.CrossRefGoogle Scholar
  44. Palminteri, S., Powell, G., Endo, W., Kirkby, C., Yu, D., & Peres, C. A. (2011). Usefulness of species range polygons for predicting local primate occurrences in Southeastern Peru. American Journal of Primatology, 73, 53–61.PubMedCrossRefGoogle Scholar
  45. Patterson, B. D., Ceballos, G., Sechrest, W., Tognelli, M. F., Brooks, T., Luna, L., et al. (2007). Digital distribution maps of the mammals of the Western Hemisphere, version 3.0. Arlington: NatureServe.Google Scholar
  46. Peres, C. A. (1993). Diet and feeding ecology of saddle-back (Saguinus fuscicollis) and moustached (Saguinus mystax) tamarins in an Amazonian terra firme forest. Journal of Zoology, 230, 567–592.CrossRefGoogle Scholar
  47. Peres, C. A. (1994a). Diet and feeding ecology of gray woolly monkeys (Lagothrix lagotricha cana) in central Amazonia: comparisons with other atelines. International Journal of Primatology, 15, 333–372.CrossRefGoogle Scholar
  48. Peres, C. A. (1994b). Primate responses to phenological changes in an Amazonian terra firme forest. Biotropica, 26, 98–112.CrossRefGoogle Scholar
  49. Peres, C. A. (1997). Effects of habitat quality and hunting pressure on arboreal folivore densities in neotropical forests: a case study of howler monkeys (Alouatta spp.). Folia Primatologica, 68, 199–222.CrossRefGoogle Scholar
  50. Peres, C. A., & Janson, C. H. (1999). Species coexistence, distribution, and environmental determinants of neotropical primate richness: A community-level zoogeographic analysis. In J. G. Fleagle, C. H. Janson, & K. E. Reed (Eds.), Primate communities (pp. 55–74). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  51. Peres, C. A., & Lake, I. R. (2003). Extent of nontimber resource extraction in tropical forests: accessibility to game vertebrates by hunters in the Amazon basin. Conservation Biology, 17, 521–535.CrossRefGoogle Scholar
  52. Pickett, S. B., Bergey, C. M., & Di Fiore, A. (2012). A metagenomic study of insect diet diversity. American Journal of Primatology, 74, 622–631.PubMedCrossRefGoogle Scholar
  53. Pinto, L. P. D. S., & Rylands, A. B. (1997). Geographic distribution of the golden-headed lion tamarin, Leontopithecus chrysomelas: implications for its management and conservation. Folia Primatologica, 68, 161–180.CrossRefGoogle Scholar
  54. Pitman, N. C. A., Widmer, J., Jenkins, C. N., Stocks, G., Seales, L., Paniagua, F., et al. (2011). Volume and geographical distribution of ecological research in the Andes and the Amazon, 1995–2008. Tropical Conservation Science, 4, 64–81.Google Scholar
  55. Porter, L. M., & Garber, P. A. (2004). Goeldi’s monkeys: a primate paradox? Evolutionary Anthropology: Issues, News, and Reviews, 13, 104–115.CrossRefGoogle Scholar
  56. Porter, L. M., Sterr, S. M., & Garber, P. A. (2007). Habitat use and ranging behavior of Callimico goeldii. International Journal of Primatology, 28, 1035–1058.CrossRefGoogle Scholar
  57. Purvis, A., Gittleman, J. L., Cowlishaw, G., & Mace, G. M. (2000). Predicting extinction risk in declining species. Proceedings of the Royal Society of London B: Biological Sciences, 267, 1947–1952. Google Scholar
  58. R Development Core Team. (2010). R: A language and environment for statistical computing. Vienna, R Foundation for Statistical Computing.Google Scholar
  59. Reddy, S., & Dávalos, L. M. (2003). Geographical sampling bias and its implications for conservation priorities in Africa. Journal of Biogeography, 30, 1719–1727.CrossRefGoogle Scholar
  60. Rehg, J. A. (2010). Plant feeding patches: patterns of use by associating Callimico goeldii, Saguinus labiatus, and S. fuscicollis. Neotropical Primates, 17, 18–21.CrossRefGoogle Scholar
  61. Rosenberger, A. L. (2011). Evolutionary morphology, platyrrhine evolution, and systematics. Anatomical Record, 294, 1955–1974.CrossRefGoogle Scholar
  62. Rylands, A. B., Coimbra-Filho, A. F., & Mittermeier, R. A. (2009). The systematics and distributions of the marmosets (Callithrix, Callibella, Cebuella, and Mico) and Callimico (Callimico) (Callitrichidae, Primates). In S. M. Ford, L. M. Porter, & L. C. Davis (Eds.), The smallest anthropoids (pp. 25–61). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  63. Rylands, A. B., Mallinson, J., Kleiman, D. G., Coimbra-Filho, A. F., Mittermeier, R. A., Gusmão Câmara, I., et al. (2002). A history of lion tamarin research and conservation. In D. G. Kleiman & A. B. Rylands (Eds.), Lion tamarins: Biology and conservation (pp. 3–41). Washington, DC: Smithsonian Institution Press.Google Scholar
  64. Rylands, A. B., & Mittermeier, R. A. (2009). The diversity of the new world primates (Platyrrhini): An annotated taxonomy. In P. A. Garber, A. Estrada, J. C. Bicca-Marques, E. W. Heymann, & K. B. Strier (Eds.), South American primates: Comparative perspectives in the study of behavior, ecology, and conservation (pp. 23–54). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  65. Schulman, L., Toivonen, T., & Ruokolainen, K. (2007). Analysing botanical collecting effort in Amazonia and correcting for it in species range estimation. Journal of Biogeography, 34, 1388–1399.CrossRefGoogle Scholar
  66. 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, 1–7.PubMedCrossRefGoogle Scholar
  67. Smith, R. J., & Jungers, W. L. (1997). Body mass in comparative primatology. Journal of Human Evolution, 32, 523–559.Google Scholar
  68. Smuts, B. B., Cheney, D. L., Seyfarth, R. M., Wrangham, R. W., & Struhsaker, T. T. (1987). Primate societies. Chicago: University of Chicago Press.Google Scholar
  69. Soini, P. (1986). A synecological study of a primate community in the Pacaya-Samiria National Reserve, Peru. Primate Conservation, 7, 63–71.Google Scholar
  70. Stallings, J. (1985). Distribution and status of primates in Paraguay. Primate Conservation, 6, 51–58.Google Scholar
  71. Stocks, G., Seales, L., Paniagua, F., Maehr, E., & Bruna, E. M. (2008). The geographical and institutional distribution of ecological research in the tropics. Biotropica, 40, 397–404.CrossRefGoogle Scholar
  72. Strier, K. B. (2010). Primate behavioral ecology (4th ed.). Upper Saddle River: Prentice Hall.Google Scholar
  73. Strier, K. B., & Mendes, S. L. (2009). Long-term field studies of South American primates. In P. A. Garber, A. Estrada, J. C. Bicca-Marques, E. W. Heymann, & K. B. Strier (Eds.), South American primates: Comparative perspectives in the study of behavior, ecology, and conservation (pp. 139–156). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  74. TEAM. (2011). Tropical ecology assessment & monitoring network: early warning system for nature. Terrestrial vertebrates – Manaus, Data Set Identifier: TEAM-DataPackage-20110620040207_3415.Google Scholar
  75. Terborgh, J. (1983). Five new world primates: A study in comparative ecology. Princeton: Princeton University Press.Google Scholar
  76. ter Steege, H., Pitman, N. C. A., Phillips, O. L., Chave, J., Sabatier, D., Duque, A., et al. (2006). Continental-scale patterns of canopy tree composition and function across Amazonia. Nature, 443, 444–447.PubMedCrossRefGoogle Scholar
  77. Villalba, J. S., Prigioni, C. M., & Sappa, A. C. (1995). Sobre la posible presencia de Alouatta caraya en Uruguay. Neotropical Primates, 3, 173–174.Google Scholar
  78. Voss, R. S., & Fleck, D. W. (2011). Mammalian diversity and Matses ethnomammalogy in Amazonian Peru part 1: primates. Bulletin of the American Museum of Natural History, 351, 1–81.CrossRefGoogle Scholar
  79. Whitehead, P. F., & Jolly, C. J. (2000). Old world monkeys. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  80. Wildman, D. E., Jameson, N. M., Opazo, J. C., & Yi, S. V. (2009). A fully resolved genus level phylogeny of neotropical primates (Platyrrhini). Molecular Phylogenetics and Evolution, 53, 694–702.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Joseph E. Hawes
    • 1
  • Armando M. Calouro
    • 2
  • Carlos A. Peres
    • 1
  1. 1.School of Environmental SciencesUniversity of East AngliaNorwichU.K.
  2. 2.Centro de Ciências Biológicas e da NaturezaUniversidade Federal do Acre69920-223 Rio BrancoBrazil

Personalised recommendations