Advertisement

International Journal of Primatology

, Volume 35, Issue 5, pp 990–1003 | Cite as

Data Quality and the Comparative Method: The Case of Primate Group Size

  • Samantha K. Patterson
  • Aaron A. SandelEmail author
  • Jordan A. Miller
  • John C. Mitani
Article

Abstract

The comparative method is frequently employed to study primate behavior and evolution. The method is used to infer adaptations, and considerable improvements have been made with respect to its implementation. Despite these advances, scant attention has been given to the nature of the data that are used in comparative analyses. This creates a potential problem as data are often compiled from studies conducted by multiple researchers, whose methods may differ, resulting in variation in data quality. In this article, we investigate the quality of data employed in studies of primate group size. Several issues concerning data quality arise when assembling data on group size. For example, data quality may be compromised if group sizes are estimated from censuses, unhabituated groups, or groups with unrecognized individuals. To mitigate these and other data quality issues, we gathered data from the literature on 23 monkeys and apes using well-defined and biologically relevant criteria for inclusion. We compare our results with those of eight published compilations of group size. Most studies did not provide details regarding the criteria for including data. We found that our group size values were uncorrelated or weakly correlated with those from three other studies and differed in a consistent fashion from those of one other study. Because conclusions derived from comparative analyses are only as accurate as the data that they use, future studies should provide details regarding data collection to ensure their reliability.

Keywords

Comparative analyses Evolutionary biology Primate behavior 

Notes

Acknowledgements

We thank M. Jackson for help with data collection. We thank Joanna Setchell and two anonymous reviewers for comments on the manuscript. We thank R. Reddy, B. Pav, L. Barrett, and B. Hansen for helpful comments and caustic discussions. We thank P. Rodman, T. Struhsaker, and L. Leland for permission to use unpublished data. We also pay tribute to the late F. Bossuyt, whose data on group size of Callicebus moloch we include here. A. A. Sandel was supported by the National Science Foundation Graduate Research Fellowship under Grant No. F031543, and J. A. Miller was supported by a department grant from the National Science Foundation (DGE-0801634).

Supplementary material

10764_2014_9777_MOESM1_ESM.xlsx (22 kb)
ESM 1 (XLSX 21.5 kb)
10764_2014_9777_MOESM2_ESM.docx (47 kb)
ESM 2 (DOCX 47.2 kb)
10764_2014_9777_MOESM3_ESM.docx (65 kb)
ESM 3 (DOCX 64.6 kb)

References

  1. Altmann, J., & Muruthi, P. (1988). Differences in daily life between semiprovisioned and wild-feeding baboons. American Journal of Primatology, 15, 213–221.CrossRefGoogle Scholar
  2. Asquith, P. J. (1989). Provisioning and the study of free-ranging primates: History, effects, and prospects. American Journal of Physical Anthropology, 32, 129–158.CrossRefGoogle Scholar
  3. Beauchamp, G., & Cabana, G. (1990). Group size variability in primates. Primates, 31, 171–182.CrossRefGoogle Scholar
  4. Bergman, T. J. (2010). Experimental evidence for limited vocal recognition in a wild primate: Implications for the social complexity hypothesis. Proceedings of the Royal Society B: Biological Sciences, 277, 3045–3053.PubMedCrossRefPubMedCentralGoogle Scholar
  5. Borries, C., Gordon, A. D., & Koenig, A. (2013). Beware of primate life history data: A plea for data standards and a repository. PLoS ONE, 8, e67200.PubMedCrossRefPubMedCentralGoogle Scholar
  6. Buckland, S. T., Anderson, D. R., Burnham, K. P., Laake, J. L., Borchers, D. L., & Thomas, L. (2001). Introduction to distance sampling: Estimating abundance of biological populations. Oxford: Oxford University Press.Google Scholar
  7. Campbell, C., Fuentes, A., MacKinnon, K., Bearder, S., & Stumpf, R. (2010). Primates in perspective (2nd ed.). New York: Oxford University Press.Google Scholar
  8. Chapman, C. A., & Chapman, L. J. (2000). Determinants of group size in primates: The importance of travel costs. In S. Boinski & P. A. Garber (Eds.), On the move: How and why animals travel in groups (pp. 24–42). Chicago: University of Chicago Press.Google Scholar
  9. Chapman, C. A., & Rothman, J. M. (2009). Within-species differences in primate social structure: evolution of plasticity and phylogenetic constraints. Primates, 50, 12–22.PubMedCrossRefGoogle Scholar
  10. Clutton-Brock, T. H., & Harvey, P. H. (1977). Primate ecology and social organization. Journal of Zoology, 183, 1–39.CrossRefGoogle Scholar
  11. Clutton-Brock, T. H., & Harvey, P. H. (1980). Primates, brains and ecology. Journal of Zoology, 190, 309–323.CrossRefGoogle Scholar
  12. Clutton-Brock, T. H., Harvey, P. H., & Rudder, B. (1977). Sexual dimorphism, socionomic sex ratio and body weight in primates. Nature, 269, 797–800.PubMedCrossRefGoogle Scholar
  13. Crook, J., & Gartlan, S. (1966). Evolution of primate societies. Nature, 210, 1200–1203.PubMedCrossRefGoogle Scholar
  14. Darwin, C. (1859). On the origin of species. London: John Murray.Google Scholar
  15. Dunbar, R. I. M. (1992). Neocortex size as a constraint on group size in primates. Journal of Human Evolution, 22, 469–493.CrossRefGoogle Scholar
  16. Eisenberg, J., Muckenhirn, N., & Rudran, R. (1972). The relation between ecology and social structure in primates. Science, 176, 863–874.PubMedCrossRefGoogle Scholar
  17. Fashing, P. J., & Cords, M. (2000). Diurnal primate densities and biomass in the Kakamega forest: An evaluation of census methods and a comparison with other forests. American Journal of Primatology, 50, 139–152.PubMedCrossRefGoogle Scholar
  18. Freckleton, R. P. (2009). The seven deadly sins of comparative analysis. Journal of Evolutionary Biology, 22, 1367–1375.PubMedCrossRefGoogle Scholar
  19. Garamszegi, L. Z., & Møller, A. P. (2010). Effects of sample size and intraspecific variation in phylogenetic comparative studies: a meta-analytic review. Biological Reviews, 85, 797–805.PubMedGoogle Scholar
  20. Garamszegi, L. Z., & Møller, A. P. (2011). Nonrandom variation in within-species sample size and missing data in phylogenetic comparative studies. Systematic Biology, 60, 876–880.PubMedCrossRefGoogle Scholar
  21. Garamszegi, L. Z., & Møller, A. P. (2012). Untested assumptions about within-species sample size and missing data in interspecific studies. Behavioral Ecology and Sociobiology, 66, 1363–1373.CrossRefGoogle Scholar
  22. Gittleman, J. L. (1989). The comparative approach in ethology: Aims and limitations. In P. P. G. Bateson & P. H. Klopfer (Eds.), Perspectives in ethology (pp. 55–83). New York: Plenum.Google Scholar
  23. Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge, MA: The Belknap Press of Harvard University Press.Google Scholar
  24. Harcourt, A., Harvey, P., Larson, S., & Short, R. (1981). Testis weight, body weight and breeding systems in primates. Nature, 293, 55–57.PubMedCrossRefGoogle Scholar
  25. Harvey, P., & Pagel, M. (1991). The comparative method in evolutionary biology. Oxford: Oxford University Press.Google Scholar
  26. Hassel-Finnegan, H. M., Borries, C., Larney, E., Umponjan, M., & Koenig, A. (2008). How reliable are density estimates for diurnal primates? International Journal of Primatology, 29, 1175–1187.CrossRefGoogle Scholar
  27. Hill, D. A. (1999). Effects of provisioning on the social behaviour of Japanese and rhesus macaques: Implications for socioecology. Primates, 40, 187–198.PubMedCrossRefGoogle Scholar
  28. Hill, R. A., & Lee, P. C. (1998). Predation risk as an influence on group size in cercopithecoid primates: Implications for social structure. Journal of Zoology, 245, 447–456.CrossRefGoogle Scholar
  29. Ives, A. R., Midford, P. E., & Garland, T. (2007). Within-species variation and measurement error in phylogenetic comparative methods. Systematic Biology, 56, 252–270.PubMedCrossRefGoogle Scholar
  30. Janson, C. H., & Goldsmith, M. L. (1995). Predicting group size in primates: Foraging costs and predation risks. Behavioral Ecology, 6, 326–336.CrossRefGoogle Scholar
  31. Kenagy, G. J., & Trombulak, S. C. (1986). Size and function of mammalian testes in relation to body size. Journal of Mammalogy, 67, 1–22.CrossRefGoogle Scholar
  32. Langergraber, K. E., Prufer, K., Rowney, C., Boesch, C., Crockford, C., Fawcett, K., Inoue, E., Inoue-Muruyama, M., Mitani, J. C., Muller, M. N., Robbins, M. M., Schubert, G., Stoinski, T. S., Viola, B., Watts, D., Wittig, R. M., Wrangham, R. W., Zuberbuhler, K., Paabo, S., & Vigilant, L. (2012). Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution. Proceedings of the National Academy of Sciences of the USA, 109, 15716–15721.PubMedCrossRefPubMedCentralGoogle Scholar
  33. Lukas, D., & Clutton-Brock, T. H. (2013). The evolution of social monogamy in mammals. Science, 341, 526–530.PubMedCrossRefGoogle Scholar
  34. MacLean, E. L., Matthews, L. J., Hare, B. A., Nunn, C. L., Anderson, R. C., Aureli, F., Brannon, E. M., Call, J., Drea, C. M., Emery, N. J., Haun, D. B. M., Herrmann, E., Jacobs, L. F., Platt, M. L., Rosati, A. G., Sandel, A. A., Schroepfer, K. K., Seed, A. M., Tan, J., van Schaik, C. P., & Wobber, V. (2012). How does cognition evolve? Phylogenetic comparative psychology. Animal Cognition, 15, 223–238.PubMedCrossRefPubMedCentralGoogle Scholar
  35. MacLean, E. L., Sandel, A. A., Bray, J., Oldenkamp, R. E., Reddy, R. B., & Hare, B. A. (2013). Group size predicts social but not nonsocial cognition in lemurs. PLoS ONE, 8, e66359.PubMedCrossRefPubMedCentralGoogle Scholar
  36. Majolo, B., de Bortoli Vizioli, A., & Schino, G. (2008). Costs and benefits of group living in primates: Group size effects on behaviour and demography. Animal Behaviour, 76, 1235–1247.CrossRefGoogle Scholar
  37. Mitani, J. C., Gros-Louis, J., & Richards, A. F. (1996). Sexual dimorphism, the operational sex ratio, and the intensity of male competition in polygynous primates. American Naturalist, 147, 966–980.Google Scholar
  38. Mitani, J. C., Watts, D. P., & Muller, M. N. (2002). Recent developments in the study of wild chimpanzee behavior. Evolutionary Anthropology: Issues, News, and Reviews, 11, 9–25.CrossRefGoogle Scholar
  39. Nunn, C. L. (2011). The comparative approach in evolutionary anthropology and biology. Chicago: University of Chicago Press.CrossRefGoogle Scholar
  40. Opie, C., Atkinson, Q. D., Dunbar, R. I., & Shultz, S. (2013). Male infanticide leads to social monogamy in primates. Proceedings of the National Academy of Sciences of the USA, 110, 13328–13332.PubMedCrossRefPubMedCentralGoogle Scholar
  41. Plavcan, J. (2001). Sexual dimorphism in primate evolution. Yearbook of Physical Anthropology, 44, 25–53.CrossRefGoogle Scholar
  42. Reader, S. M., & Laland, K. N. (2002). Social intelligence, innovation, and enhanced brain size in primates. Proceedings of the National Academy of Sciences of the USA, 99, 4436–4441.PubMedCrossRefPubMedCentralGoogle Scholar
  43. Revell, L. J., & Graham Reynolds, R. (2012). A new Bayesian method for fitting evolutionary models to comparative data with intraspecific variation. Evolution, 66, 2697–2707.PubMedCrossRefGoogle Scholar
  44. Roberts, E. K., Lu, A., Bergman, T. J., & Beehner, J. C. (2012). A Bruce effect in wild geladas. Science, 335, 1222–1225.PubMedCrossRefGoogle Scholar
  45. Smith, R. J., & Jungers, W. L. (1997). Body mass in comparative primatology. Journal of Human Evolution, 32, 523–559.PubMedCrossRefGoogle Scholar
  46. Smuts, B., Cheney, D., Seyfarth, R., Wrangham, R. W., & Struhsaker, T. (1987). Primate societies. Chicago: University of Chicago Press.Google Scholar
  47. Strier, K. B. (2000). Population viabilities and conservation implications for muriquis (Brachyteles arachnoids) in Brazil's Atlantic Forest. Biotropica, 32, 903–913.Google Scholar
  48. Strier, K. B. (2003). Primatology comes of age: 2002 AAPA luncheon address. Yearbook of Physical Anthropology, 46, 2–13.CrossRefGoogle Scholar
  49. Struhsaker, T. T. (2000). Variation in adult sex ratios of red colobus monkey social groups: Implications for interspecific comparisons. In P. M. Kappeler (Ed.), Primate males (pp. 108–119). Cambridge, U.K.: Cambridge University Press.Google Scholar
  50. Symington, M. M. F. (1990). Fission-fusion social organization in Ateles and Pan. International Journal of Primatology, 11, 47–61.CrossRefGoogle Scholar
  51. Tutin, C. E. G., McGrew, W. C., & Baldwin, J. P. (1983). Social organization of savanna-dwelling chimpanzees, Pan troglodytes verus, at Mt. Assirik, Senegal. Primates, 34, 154–173.CrossRefGoogle Scholar
  52. van Schaik, C. P. (1983). Why are diurnal primates living in groups? Behaviour, 87, 120–144.CrossRefGoogle Scholar
  53. van Schaik, C. P., & Hörstermann, M. (1994). Predation risk and the number of adult males in a primate group: A comparative test. Behavioral Ecology and Sociobiology, 35, 261–272.CrossRefGoogle Scholar
  54. Wrangham, R. W. (1974). Artificial feeding of chimpanzees and baboons in their natural habitat. Animal Behaviour, 22, 83–93.CrossRefGoogle Scholar
  55. Yeager, C. P. (1990). Proboscis monkey (Nasalis larvatus) social organization: Group structure. American Journal of Primatology, 20, 95–106.CrossRefGoogle Scholar
  56. Yeager, C. P. (1991). Proboscis monkey (Nasalis larvatus) social organization: Intergroup patterns of association. American Journal of Primatology, 23, 73–86.CrossRefGoogle Scholar
  57. Yeager, C. P. (1992). Proboscis monkey (Nasalis larvatus) social organization: Nature and possible functions of intergroup patterns of association. American Journal of Primatology, 26, 133–137.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Samantha K. Patterson
    • 1
  • Aaron A. Sandel
    • 1
    Email author
  • Jordan A. Miller
    • 2
  • John C. Mitani
    • 1
  1. 1.Department of AnthropologyUniversity of MichiganAnn ArborUSA
  2. 2.Center for the Advanced Study of Hominid PaleobiologyThe George Washington UniversityWashingtonUSA

Personalised recommendations