International Journal of Primatology

, Volume 37, Issue 6, pp 738–751 | Cite as

Do Fruit Nutrients Affect Subgrouping Patterns in Wild Spider Monkeys (Ateles geoffroyi)?

  • Laura Busia
  • Colleen M. Schaffner
  • Jessica M. Rothman
  • Filippo Aureli


One of the main costs of group living is feeding competition. Fission–fusion dynamics are thought to be a strategy to avoid overt competition for food resources. We tested whether food abundance and quality affected such dynamics in a species characterized by a high degree of fission–fusion dynamics. We collected data on 22 adult and subadult spider monkeys (Ateles geoffroyi) living in a large community in the protected area of Otoch Ma’ax Yetel Kooh, Yucatan, Mexico. We recorded subgroup size and fission events as well as fruit abundance during 12 mo and conducted nutritional analyses on the fruit species that the study subjects consumed most. We found no effect of fruit abundance or nutritional quality of recently visited food patches on individual fission decisions, but the amount of protein in the food patches visited over the course of the day was a good predictor of subgroup size. While the absence of support for a relationship between fruit characteristics and fission decisions may be due to the short temporal scale of the analysis, our findings relating subgroup size to the amount of protein in the visited food patches over the course of the day may be explained by individual spider monkeys attempting to obtain sufficient protein intake from their fruit-based diet.


Ateles Feeding competition Fission–fusion dynamics Food abundance Nutrient quality 



We thank Anthony R. Denice for his outstanding contribution in data collection; Augusto Canul, Eulogio Canul, Juan Canul, and Macedonio Canul for their valuable assistance during fieldwork; and tree climbers Octaviano “Tavo” Ciau Dzul and Benito Yam Cocom for their indispensable assistance during fruit sample collection. We are deeply grateful to Joanna M. Setchell, Annika Felton, and an anonymous reviewer for valuable comments on previous versions of the manuscript. We are grateful to Sandra Smith for her overall support and to Gabriel Ramos-Fernandez and Laura G. Vick for sharing the management of the long-term project. We are also indebted to Chester Zoo and The National Geographic Society for financially supporting the long-term project, the Primate Society of Great Britain for a research grant, and the Consejo Nacional por la Ciencia y la Tecnologia (CONACyT) for L. Busia’s PhD studentship (CVU no. 490429) and for equipment (no. I0101/152/2014 C-133/2014).


  1. Anderson, D. P., Nordheim, E. V., Boesch, C., & Moermond, T. C. (2002). Factors influencing fission-fusion grouping in chimpanzees in the Taï National Park, Côte d’Ivoire. In C. Boesch, G. Hohmann, & L. F. Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos (pp. 90–101). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  2. Asensio, N., Korstjens, A. H., & Aureli, F. (2009). Fissioning minimizes ranging costs in spider monkeys: A multiple-level approach. Behavioral Ecology and Sociobiology, 63, 649–659.CrossRefGoogle Scholar
  3. Aureli, F., Schaffner, C. M., Boesch, C., Bearder, S. K., Call, J., et al. (2008). Fission-fusion dynamics: new research frameworks. Current Anthropology, 49, 627–654.CrossRefGoogle Scholar
  4. Basabose, A. K. (2004). Fruit availability and chimpanzee party size at Kahuzi Montane Forest, Democratic Republic of Congo. Primates, 45, 211–219.CrossRefPubMedGoogle Scholar
  5. Bates, D., Maechler, M., Bolker, B., & Walker, S. (2014). lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7.
  6. Boesch, C., & Boesch-Achermann, H. (2000). The chimpanzees of the Taї forest: behavioural ecology and evolution. Oxford: Oxford University Press.Google Scholar
  7. Chancellor, R. L., Rundus, A. S., & Nyandwi, S. (2012). The influence of seasonal variation on chimpanzee (Pan troglodytes schweinfurthii) fallback food consumption, nest group size, and habitat use in Gishwati, a montane rain forest fragment in Rwanda. International Journal of Primatology, 33, 115–133.CrossRefGoogle Scholar
  8. Chapman, C. A. (1990). Ecological constraints on group size in three species of neotropical primates. Folia Primatologica, 55, 1–9.CrossRefGoogle Scholar
  9. Chapman, C. A., & Chapman, L. J. (1999). Implications of small scale variation in ecological conditions for the diet and density of red colobus monkeys. Primates, 40, 215–231.CrossRefPubMedGoogle Scholar
  10. Chapman, C. A., & Chapman, L. J. (2000). Determinants of group size in primates: the importance of travel costs. In S. Boinski & P. Garber (Eds.), On the move: how and why animals travel in groups (pp. 24–42). Chicago: University of Chicago Press.Google Scholar
  11. Chapman, C. A., Chapman, L. J., Wangham, R., Hunt, K., Gebo, D., & Gardner, L. (1992). Estimators of fruit abundance of tropical trees. Biotropica, 24, 527–531.CrossRefGoogle Scholar
  12. Chapman, C. A., Wrangham, R. W., & Chapman, L. J. (1995). Ecological constraints on group size: an analysis of spider monkey and chimpanzee subgroups. Behavioral Ecology and Sociobiology, 36, 59–70.CrossRefGoogle Scholar
  13. Chapman, C. A., Chapman, L. J., Naughton-Treves, L., Lawes, M. J., & McDowell, L. R. (2004). Predicting folivorous primate abundance: validation of a nutritional model. American Journal of Primatology, 62, 55–69.CrossRefPubMedGoogle Scholar
  14. Chapman, C. A., Rothman, J. M., & Lambert, J. E. (2012). Food as a selective force in primates. In J. C. Mitani, J. Call, P. M. Kappeler, R. A. Palombit, & J. B. Silk (Eds.), The evolution of primate societies (pp. 149–168). Chicago: University of Chicago Press.Google Scholar
  15. Conklin-Brittain, N. L., Dierenfeld, E. S., Wrangham, R. W., Norconk, M., & Silver, S. C. (1999). Chemical protein analysis: a comparison of kjeldahl crude protein and total ninhydrin protein from wild, tropical vegetation. Journal of Chemical Ecology, 25, 2601–2622.CrossRefGoogle Scholar
  16. Croft, D. P., James, R., & Krause, J. (2008). Exploring animal social networks. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
  17. Dew, J. L. (2005). Foraging, food choice, and food processing by sympatric ripe-fruit specialists: Lagothrix lagotricha poeppigii and Ateles belzebuth belzebuth. International Journal of Primatology, 26, 1107–1135.CrossRefGoogle Scholar
  18. Di Fiore, A., & Rodman, P. S. (2001). Time allocation patterns of lowland woolly monkeys (Lagothrix lagotricha poeppigii) in a neotropical terra firma forest. International Journal of Primatology, 22, 449–480.CrossRefGoogle Scholar
  19. Di Fiore, A., Link, A., & Dew, J. L. (2008). Diets of wild spider monkeys. In C. Campbell (Ed.), Spider monkeys: the biology, behavior and ecology of the genus Ateles (pp. 55–81). New York: Cambridge University Press.Google Scholar
  20. Dobson, A. J., & Barnett, A. G. (2008). An introduction to generalized linear models. Boca Raton, FL: Chapman & Hall/CRC.Google Scholar
  21. Dunbar, R. I. M. (1985). Reproductive decisions: an economic analysis of gelada baboon social strategies. Princeton, NJ: Princeton University Press.CrossRefGoogle Scholar
  22. Fashing, P. J., Dierenfeld, E., & Mowry, C. B. (2007). Influence of plant and soil chemistry on food selection, ranging patterns, and biomass of Colobus guereza in Kakamega Forest, Kenya. International Journal of Primatology, 28, 673–703.CrossRefGoogle Scholar
  23. Fedigan, L. M., & Baxter, M. J. (1984). Sex differences and social organization in free-ranging spider monkeys (Ateles geoffroyi). Primates, 25, 279–294.CrossRefGoogle Scholar
  24. Felton, A. M., Felton, A., Lindenmayer, D. B., & Foley, W. J. (2009a). Nutritional goals of wild primates. Functional Ecology, 23, 70–78.CrossRefGoogle Scholar
  25. Felton, A. M., Felton, A., Raubenheimer, D., Simpson, S. J., Foley, W. J., et al. (2009b). Protein content of diets dictates the daily energy intake of a free-ranging primate. Behavioral Ecology, 20, 685–670.CrossRefGoogle Scholar
  26. Fimbel, C., Vedder, A., Dierenfeld, E., & Mulindahabi, F. (2001). An ecological basis for large group size in Colobus angolensis in the Nyungwe Forest, Rwanda. African Journal of Ecology, 39, 83–92.CrossRefGoogle Scholar
  27. Forstmeier, W., & Schielzeth, H. (2011). Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse. Behavioral Ecology and Sociobiology, 65, 47–55.CrossRefPubMedGoogle Scholar
  28. Gillespie, T. R., & Chapman, C. A. (2001). Determinants of group size in the red colobus monkey (Procolobus badius): An evaluation of the generality of the ecological-constraints model. Behavioral Ecology and Sociobiology, 50, 329–338.CrossRefGoogle Scholar
  29. Gogarten, J. F., Jacob, A. L., Ghai, R. R., Rothman, J. M., Twinomugisha, D., et al. (2015). Group size dynamics over 15+ years in an African forest primate community. Biotropica, 47, 101–112.CrossRefGoogle Scholar
  30. Hamard, M., Cheyne, S. M., & Nijman, V. (2010). Vegetation correlates of gibbon density in the peat-swamp forest of the Sabangau catchment, Central Kalimantan, Indonesia. American Journal of Primatology, 72, 607–616.PubMedGoogle Scholar
  31. Hanya, G., & Chapman, C. A. (2013). Linking feeding ecology and population abundance: a review of food resource limitation on primates. Ecological Research, 28, 183–190.CrossRefGoogle Scholar
  32. Hanya, G., Kiyono, M., Yamada, A., Suzuki, K., Furukawa, M., et al. (2006). Not only annual food abundance but also fallback food quality determines the Japanese macaque density: evidence from seasonal variations in home range size. Primates, 47, 275–278.CrossRefPubMedGoogle Scholar
  33. Hanya, G., Stevenson, P., van Noordwijk, M., Te Wong, S., Kanamori, T., et al. (2011). Seasonality in fruit availability affects frugivorous primate biomass and species richness. Ecography, 34, 1009–1017.CrossRefGoogle Scholar
  34. Hashimoto, C., Furuichi, T., & Tashiro, Y. (2001). What factors affect the size of chimpanzee parties in the Kalinzu Forest, Uganda? Examination of fruit abundance and number of estrous females. International Journal of Primatology, 22, 947–959.CrossRefGoogle Scholar
  35. Hashimoto, C., Suzuki, S., Takenoshita, Y., Yamagiwa, J., Basabose, A. K., & Furuichi, T. (2003). How fruit abundance affects the chimpanzee party size: A comparison between four study sites. Primates, 44, 77–81.PubMedGoogle Scholar
  36. Heithaus, M. R., & Dill, L. M. (2002). Food availability and tiger shark predation risk influence bottlenose dolphin habitat use. Ecology, 83, 480–491.CrossRefGoogle Scholar
  37. Hosamani, R., & Desai, S. R. (2013). Solar based temperature controlled fruit drying system. International Journal of Research in Instrumentation Engineering, 2, 4–7.Google Scholar
  38. Itoh, N., & Nishida, T. (2007). Chimpanzee grouping patterns and food availability in Mahale Mountains National Park, Tanzania. Primates, 48, 87–96.CrossRefPubMedGoogle Scholar
  39. Janson, C. H. (1988). Intra-specific food competition and primate social structure: a synthesis. Behaviour, 105, 1–17.CrossRefGoogle Scholar
  40. Janson, C. H., & Chapman, C. A. (1999). Resources and primate community structure. In J. G. Fleagle, C. H. Janson, & K. Reed (Eds.), Primate communities (pp. 237–267). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  41. Janson, C. H., & Goldsmith, M. L. (1995). Predicting group size in primates: Foraging costs and predation risks. Behavioral Ecology, 6, 326–336.CrossRefGoogle Scholar
  42. Janson, C. H., & van Schaik, C. P. (1988). Recognizing the many faces of primate food competition: Methods. Behaviour, 105, 165–186.CrossRefGoogle Scholar
  43. Johnson, C. A., Raubenheimer, D., Chapman, C. A., Tombak, K. J., Reid, A. J., & Rothman, J. M. (2015). Macronutrient balancing affects patch departure by guerezas (Colobus guereza). American Journal of Primatology. doi: 10.1002/ajp.22495.Google Scholar
  44. Klein, L. L., & Klein, D. B. (1977). Feeding behaviour of the Colombian spider monkey. In T. H. Clutton-Brock (Ed.), Primate ecology: studies of feeding and ranging behaviour in lemurs, monkeys and apes (pp. 153–181). London: Academic.CrossRefGoogle Scholar
  45. Koenig, A. (2002). Competition for resources and its behavioral consequences among female primates. International Journal of Primatology, 23, 759–783.CrossRefGoogle Scholar
  46. Krause, J., & Ruxton, G. D. (2002). Living in groups. New York: Oxford University Press.Google Scholar
  47. Kummer, H. (1971). Primate societies: group techniques of ecological adaptation. Chicago: Aldine.Google Scholar
  48. Lee, D. J., & Putnam, G. B. (1973). The response of rainbow trout to varying protein/energy ratios in a test diet. The Journal of Nutrition, 103, 916–922.PubMedGoogle Scholar
  49. Lehmann, J., & Boesch, C. (2004). To fission or to fusion: effects of community size on wild chimpanzee (Pan troglodytes verus) social organisation. Behavioral Ecology and Sociobiology, 56, 207–216.CrossRefGoogle Scholar
  50. Milton, K. (1979). Factors influencing leaf choice by howler monkeys: a test of some hypotheses of food selection by generalist herbivores. American Naturalist, 114, 362–378.CrossRefGoogle Scholar
  51. Milton, K. (1981). Food choice and digestive strategies of two sympatric primate species. American Naturalist, 117, 496–505.CrossRefGoogle Scholar
  52. Milton, K. (1984). Habitat, diet, and activity patterns of free-ranging woolly spider monkeys (Brachyteles arachnoides E. Geoffroyi 1806). International Journal of Primatology, 5, 491–514.CrossRefGoogle Scholar
  53. Milton, K., & Dintzis, F. (1981). Nitrogen-to-protein conversion factors for tropical plant samples. Biotropica, 12, 177–181.CrossRefGoogle Scholar
  54. National Research Council. (2003). Nutrient requirements of nonhuman primates. Washington, DC: National Academies Press.Google Scholar
  55. Newton-Fisher, N. E., Reynolds, V., & Plumptre, A. J. (2000). Food supply and chimpanzee (Pan troglodytes schweinfurthii) party size in the Budongo Forest Reserve, Uganda. International Journal of Primatology, 21, 613–628.CrossRefGoogle Scholar
  56. O’Brien, R. M. (2007). A caution regarding rules of thumb for variance inflation factors. Quality & Quantity, 41, 673–690.CrossRefGoogle Scholar
  57. Onderdonk, D. A., & Chapman, C. A. (2000). Coping with forest fragmentation: the primates of Kibale ational park, Uganda. International Journal of Primatology, 21, 587–611.CrossRefGoogle Scholar
  58. Pinheiro, J., Bates, D., DebRoy, S., & Sarkar, D., R Core Team (2014). nlme: Linear and nonlinear mixed effects models. R package version 3.1-117.
  59. Ramos-Fernandez, G. (2005). Vocal communication in a fission–fusion society: Do spider monkeys stay in touch with close associates? International Journal of Primatology, 26, 1077–1092.CrossRefGoogle Scholar
  60. Ramos-Fernandez, G., & Ayala Orozco, B. (2003). Population size and habitat use of spider monkeys at Punta Laguna, Mexico. In L. K. In Marsh (Ed.), Primates in fragments (pp. 191–209). New York: Kluwer Academic/Plenum Press.CrossRefGoogle Scholar
  61. R Core Team. (2014). R: a language and environment for statistical computing.
  62. Rebecchini, L., Schaffner, C. M., & Aureli, F. (2011). Risk is a component of social relationships in spider monkeys. Ethology, 117, 691–699.CrossRefGoogle Scholar
  63. Rosenberger, A. L., & Strier, K. B. (1989). Adaptive radiation of the ateline primates. Journal of Human Evolution, 18, 717–750.CrossRefGoogle Scholar
  64. Rothman, J. M., Chapman, C. A., & Pell, A. N. (2008). Fiber-bound nitrogen in gorilla diets: Implications for estimating dietary protein intake of primates. American Journal of Primatology, 70, 690–694.CrossRefPubMedGoogle Scholar
  65. Rothman, J. M., Chapman, C. A., & Van Soest, P. J. (2012). Methods in primate nutritional ecology: a user’s guide. International Journal of Primatology, 33, 542–566.CrossRefGoogle Scholar
  66. Schaffner, C. M., Rebecchini, L., Ramos-Fernandez, G., Vick, L. G., & Aureli, F. (2012). Spider monkeys (Ateles geoffroyi yucatenensis) cope with the negative consequences of hurricanes through changes in diet, activity budget, and fission–fusion dynamics. International Journal of Primatology, 33, 922–936.CrossRefGoogle Scholar
  67. Shimooka, Y., Campbell, C. J., Di Fiore, A., Felton, A. M., Izawa, K., et al. (2008). Demography and group composition of Ateles. In C. Campbell (Ed.), Spider monkeys: behavior, ecology & evolution of the genus Ateles (pp. 329–348). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  68. Simpson, S. J., & Raubenheimer, D. (2005). Obesity: the protein leverage hypothesis. Obesity Reviews, 6(2), 133–142.Google Scholar
  69. Smith, J. E., Kolowski, J. M., Graham, S. E. D., & Holekamp, K. E. (2008). Social and ecological determinants of fission–fusion dynamics in the spotted hyena. Animal Behavior, 76, 619–636.CrossRefGoogle Scholar
  70. Smith-Aguilar, S. E., Ramos-Fernández, G., & Getz, W. M. (2016). Seasonal changes in socio-spatial structure in a group of free-living spider monkeys (Ateles geoffroyi). PloS One, 11, e0157228.CrossRefPubMedPubMedCentralGoogle Scholar
  71. Strier, K. B. (1992). Atelinae adaptations: behavioral strategies and ecological constraints. American Journal of Physical Anthropology, 88, 515–524.CrossRefPubMedGoogle Scholar
  72. Sueur, C., Deneubourg, J. L., Petit, O., & Couzin, I. D. (2010). Differences in nutrient requirements imply a non-linear emergence of leaders in animal groups. PLoS Computational Biology, 6, e1000917.CrossRefPubMedPubMedCentralGoogle Scholar
  73. Sueur, C., MacIntosh, A. J., Jacobs, A. T., Watanabe, K., & Petit, O. (2013). Predicting leadership using nutrient requirements and dominance rank of group members. Behavioral Ecology and Sociobiology, 67, 457–470.CrossRefGoogle Scholar
  74. Symington, M. M. (1988). Food competition and foraging party size in the black spider monkey (Ateles paniscus chamek). Behaviour, 105, 117–134.CrossRefGoogle Scholar
  75. Symington, M. M. (1990). Fission-fusion social organization in Ateles and Pan. International Journal of Primatology, 11, 47–61.CrossRefGoogle Scholar
  76. Terborgh, J., & Janson, C. H. (1986). The socioecology of primate groups. Annual Review of Ecology and Systematics, 17, 111–135.CrossRefGoogle Scholar
  77. van Schaik, C. P. (1999). The socioecology of fission-fusion sociality in orangutans. Primates, 40, 69–86.CrossRefPubMedGoogle Scholar
  78. van Schaik, C. P., & van Hooff, J. A. R. A. M. (1983). On the ultimate causes of primate social systems. Behaviour, 85, 91–117.CrossRefGoogle Scholar
  79. van Schaik, C. P., van Noordwijk, M. A., Wersono, B., & Sutriono, E. (1983). Party size and early detection of predators. Primates, 24, 211–221.CrossRefGoogle Scholar
  80. van Soest, P. J., Robertson, J. B., & Lewis, B. A. (1991). Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science, 74, 3583–3597.CrossRefPubMedGoogle Scholar
  81. Wallace, R. B. (2005). Seasonal variations in diet and foraging behavior of Ateles chamek in a southern Amazonian tropical forest. International Journal of Primatology, 26, 1053–1075.CrossRefGoogle Scholar
  82. Wallace, R. B. (2008). The influence of feeding patch size and relative fruit density on the foraging behavior of the black spider monkey Ateles chamek. Biotropica, 40, 501–506.CrossRefGoogle Scholar
  83. Wallis, I. R., Edwards, M. J., Windley, H., Krockenberger, A. K., Felton, A., et al. (2012). Food for folivores: nutritional explanations linking diets to population density. Oecologia, 169, 281–291.CrossRefPubMedGoogle Scholar
  84. Wasserman, M. D., & Chapman, C. A. (2003). Determinants of colobine monkey abundance: the importance of food energy, protein and fibre content. Journal of Animal Ecology, 72,(4), 650–659.Google Scholar
  85. Williamson, D. K., & Dunbar, R. (1999). Energetics, time budgets and group size. In P. C. Lee (Ed.), Comparative primate socioecology (pp. 320–338). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  86. Worman, C. O. D., & Chapman, C. A. (2006). Densities of two frugivorous primates with respect to forest and fragment tree species composition and fruit availability. International Journal of Primatology, 27, 203–225.CrossRefGoogle Scholar
  87. Wrangham, R. W. (1980). An ecological model of female-bonded primate groups. Behaviour, 75, 262–300.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Laura Busia
    • 1
  • Colleen M. Schaffner
    • 1
  • Jessica M. Rothman
    • 2
  • Filippo Aureli
    • 1
    • 3
  1. 1.Instituto de NeuroetologiaUniversidad VeracruzanaXalapaMexico
  2. 2.Department of AnthropologyHunter College of the City University of New YorkNew YorkUSA
  3. 3.Research Centre in Evolutionary Anthropology and PalaeoecologyLiverpool John Moore UniversityLiverpoolUK

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