Skip to main content
Log in

Macronutrient and Energy Contributions of Insects to the Diet of a Frugivorous Monkey (Cercopithecus ascanius)

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

Most extant primates feed on insects to some degree, yet the nutritional contributions of insects to primate diets are poorly characterized. Like many small-bodied frugivorous primates, redtail monkeys (Cercopithecus ascanius) also eat insects. We quantified the nutritional contributions of insects to the diets of female redtail monkeys in Kibale National Park, Uganda, from July 2010 to June 2012 through full day follows (N = 64) using weight-based estimates of food intake. Female redtail monkeys targeted insects for 41 % of feeding bouts, plant reproductive parts (including ripe fruits, unripe fruits, flowers, seeds) for 15 % of feeding bouts, and leaves (including young leaves, mature leaves, leaf petioles, leaf buds) for 17 % of feeding bouts. However, females spent just under 10 % of feeding time on insects, in contrast to 42 % on plant reproductive parts and 39 % on leaves. Redtail monkeys fed primarily on solitary, as opposed to eusocial, insects. Identification of consumed insects is challenging, but of consumed insects that could be identified 74 % were cicadas (order Homoptera), 14 % caterpillars (order Lepidoptera), and 7 % long-horned grasshoppers (order Orthoptera). On a dry matter basis, insects were fairly low in fat (<10 %, except for caterpillars) and high in crude protein content (mean ca. 69 %) compared to other foods, and contained low levels of indigestible chitin. Because insects are small, an insect feeding bout is much shorter than a feeding bout on vegetation or fruit. Despite the small proportion of time spent feeding on insects, redtail monkeys obtained a mean of 24 % of their daily protein intake and 14 % of energy through insectivory, though intake varied widely across females. Our findings demonstrate that female redtail monkeys gain more nutrients than expected given that they spend <10 % of feeding time ingesting insects. The many primates that complement plant diet items with insects may gain substantial nutrition through minimal feeding time.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Altmann, S. A. (1998). Foraging for survival: Yearling baboons in Africa. Chicago: University of Chicago Press.

    Google Scholar 

  • Altmann, J., & Alberts, S. C. (2003). Variability in reproductive success viewed from a life‐history perspective in baboons. American Journal of Human Biology,15(3), 401-409.

  • AOAC. (1990). Official methods of analysis. Arlington, VA: Association of Official Analytical Chemists.

    Google Scholar 

  • Beeson, M., Tame, S., Keeming, E., & Lea, S. (1996). Food habits of guenons (Cercopithecus spp.) in Afro‐montane forest. African Journal of Ecology, 34(2), 202–210.

    Article  Google Scholar 

  • Bohmann, K., Monadjem, A., Noer, C. L., Rasmussen, M., Zeale, M. R., Clare, E., Jones, G., Willerslev, E., & Gilbert, M. T. P. (2011). Molecular diet analysis of two African free-tailed bats (Molossidae) using high throughput sequencing. PLoS One, 6(6), e21441.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bryer, M. A., Chapman, C. A., & Rothman, J. M. (2013). Diet and polyspecific associations affect spatial patterns among redtail monkeys (Cercopithecus ascanius). Behaviour, 150(3–4), 277–293.

    Google Scholar 

  • Bukkens, S. (2005). Insects in the human diet. In M. G. Paoletti (Ed.), Ecological implications of minilivestock: Potential of insects, rodents, frogs and snails (pp. 545–577). Enfield, NH: Science Publishers.

    Google Scholar 

  • Butynski, T. M. (1990). Comparative ecology of blue monkeys (Cercopithecus mitis) in high-and low-density subpopulations. Ecological Monographs, 60(1), 1–26.

  • Chapman, C. A., Chapman, L. J., Cords, M., Gathua, A., Gautier-Hion, A., Lambert, J. E., Rode, K., Tutin, C. E. G., & White, L. J. T. (2002). Variation in the diets of Cercopithecus species: differences within forests, among forests, and across species. In M. Glenn & M. Cords (Eds.), The guenons: Diversity and adaptation in African monkeys (pp. 325–350). New York: Academic/Plenum Publishers.

  • Chapman, C. A., & Lambert, J. E. (2000). Habitat alteration and the conservation of African primates: Case study of Kibale National Park, Uganda. American Journal of Physical Anthropology, 50, 169–185.

    CAS  Google Scholar 

  • Chapman, C. A., Struhsaker, T. T., Skorupa, J., Snaith, T. V., & Rothman, J. M. (2010). Understanding long-term primate community dynamics: Implications for forest change. Ecological Applications, 20, 179–191.

    Article  PubMed  Google Scholar 

  • Cipolletta, C., Spagnoletti, N., Todd, A., Robbins, M. M., Cohen, H., & Pacyna, S. (2007). Termite feeding by Gorilla gorilla gorilla at Bai Hokou, Central African Republic. International Journal of Primatology, 28(2), 457–476.

    Article  Google Scholar 

  • Conklin, N. L., & Wrangham, R. W. (1994). The value of figs to a hind-gut fermenting frugivore: A nutritional analysis. Biochemical Systematics and Ecology, 22(2), 137–151.

    Article  Google Scholar 

  • 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(12), 2601–2622.

    Article  CAS  Google Scholar 

  • Conklin-Brittain, N., Knott, C., & Wrangham, R. (2006). Energy intake by wild chimpanzees and orangutans: Methodological considerations and a preliminary comparison. In G. Hohman, M. M. Robbins, & C. Boesch (Eds.), Feeding ecology in apes and other primates (pp. 441–471). Cambridge: Cambridge University Press.

    Google Scholar 

  • Cords, M. (1986). Interspecific and intraspecific variation in diet of two forest guenons, Cercopithecus ascanius and C. mitis. Journal of Animal Ecology, 55, 811–827.

    Article  Google Scholar 

  • Cords, M. (1987). Mixed-species association of Cercopithecus monkeys in the Kakamega Forest, Kenya. University of California Publications in Zoology117, 1-109.

  • Cornelius, C., Dandrifosse, G., & Jeuniaux, C. (1976). Chintinolytic enzymes of the gastric mucosa of Perodicticus potto (Primate Prosimian): Purification and enzyme specificity. International Journal of Biochemistry, 7, 445–448.

    Article  CAS  Google Scholar 

  • Dammhahn, M., & Kappeler, P. M. (2008). Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. International Journal of Primatology, 29(6), 1567–1589.

    Article  Google Scholar 

  • Deblauwe, I., & Janssens, G. P. (2008). New insights in insect prey choice by chimpanzees and gorillas in southeast Cameroon: The role of nutritional value. American Journal of Physical Anthropology, 135(1), 42–55.

    Article  PubMed  Google Scholar 

  • Emery Thompson, M., & Wrangham, R. W. (2008). Diet and reproductive function in wild female chimpanzees (Pan troglodytesschweinfurthii) at Kibale National Park, Uganda. American Journal of Physical Anthropology135(2), 171–181.

  • Emery Thompson, M., Kahlenberg, S. M., Gilby, I. C., & Wrangham, R. W. (2007). Core area quality is associated with variance in reproductive success among female chimpanzees at Kibale National Park. Animal Behaviour73(3), 501–512.

  • Fashing, P. J., Nguyen, N., & Fashing, N. J. (2010). Behavior of geladas and other endemic wildlife during a desert locust outbreak at Guassa, Ethiopia: Ecological and conservation implications. Primates, 51(3), 193–197.

    Article  PubMed  Google Scholar 

  • Finke, M. D. (2007). Estimate of chitin in raw whole insects. Zoo Biology, 26, 105–115.

    Article  CAS  PubMed  Google Scholar 

  • Foley, W. J., McIlwee, A., Lawler, I., Aragones, L., Woolnough, A. P., & Berding, N. (1998). Ecological applications of near infrared reflectance spectroscopy a tool for rapid, cost-effective prediction of the composition of plant and animal tissues and aspects of animal performance. Oecologia, 116, 293–305.

    Article  Google Scholar 

  • Gathua, J. M. (2000). Intraspecific variation in foraging patterns of redtail monkeys (Cercopithecus ascanius) in the Kakamega Forest, Kenya. Ph.D. dissertation, Columbia University, New York.

  • Gautier-Hion, A. (1980). Seasonal variations of diet related to species and sex in a community of Cercopithecus monkeys. Journal of Animal Ecology, 49, 237–269.

    Article  Google Scholar 

  • Goering, H., & Van Soest, P. (1970). Forage fiber analysis. United States Department of Agriculture Handbook 79, 1–20.

  • Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge, MA: Belknap Press of Harvard University Press.

    Google Scholar 

  • Gursky, S. (2000). Effect of seasonality on the behavior of an insectivorous primate, Tarsius spectrum. International Journal of Primatology, 21(3), 477–495.

    Article  Google Scholar 

  • Harcourt, C. (1986). Seasonal variation in the diet of South African galagos. International Journal of Primatology, 7(5), 491–506.

    Article  Google Scholar 

  • Hladik, C. M. (1977). Chimpanzees of Gabon and chimpanzees of Gombe: Some comparative data on the diet. In Primate ecology: Studies of feeding and ranging behaviour in lemurs, monkeys, and apes (pp. 81–501). New York: Academic Press.

    Google Scholar 

  • Isbell, L. A. (1998). Diet for a small primate: Insectivory and gummivory in the (large) patas monkey(Erythrocebus patas pyrrhonotus). American Journal of Primatology, 45(4), 381–398.

    Article  CAS  PubMed  Google Scholar 

  • Isbell, L. A., Rothman, J. M., Young, P. J., & Rudolph, K. (2013). Nutritional benefits of Crematogaster mimosae ants and Acacia drepanolobium gum for patas monkeys and vervets in Laikipia, Kenya. American Journal of Physical Anthropology, 150(2), 286–300.

    Article  PubMed  Google Scholar 

  • Isbell, L. A., & Young, T. P. (2007). Interspecific and temporal variation of ant species within Acacia drepanolobium ant domatia, a staple food of patas monkeys (Erythrocebus patas) in Laikipia, Kenya. American Journal of Primatology, 69(12), 1387–1398.

    Article  PubMed  Google Scholar 

  • Krykbaev, R., Fitz, L. J., Reddy, P. S., Winkler, A., Xuan, D., Yang, X., Fleming, M., & Wolf, S. F. (2010). Evolutionary and biochemical differences between human and monkey acidic mammalian chitinases. Gene, 452(2), 63–71.

    Article  CAS  PubMed  Google Scholar 

  • Lambert, J. E. (2002). Digestive retention times in forest guenons (Cercopithecus spp.) with reference to chimpanzees (Pan troglodytes). International Journal of Primatology, 23(6), 1169–1185.

    Article  Google Scholar 

  • Mallott, E. K., Malhi, R. S., & Garber, P. A. (2015). High‐throughput sequencing of fecal DNA to identify insects consumed by wild Weddell's saddleback tamarins (Saguinus weddelli, Cebidae, Primates) in Bolivia. American Journal of Physical Anthropology, 156(3), 474–481.

    Article  CAS  PubMed  Google Scholar 

  • McCabe, G. M., & Fedigan, L. M. (2007). Effects of reproductive status on energy intake, ingestion rates, and dietary composition of female Cebus capucinus at Santa Rosa, Costa Rica. International Journal of Primatology, 28(4), 837–851.

    Article  Google Scholar 

  • McGrew, W. C. (2001). The other faunivory: primate insectivory and early human diet. In C. B. Stanford & H. T. Bunn (Eds.), Meat-eating and human evolution (pp. 160–178). Oxford: Oxford University Press.

    Google Scholar 

  • McGrew, W. C. (2014). The ‘other faunivory’revisited: Insectivory in human and non-human primates and the evolution of human diet. Journal of Human Evolution, 71, 4–11.

    Article  PubMed  Google Scholar 

  • Nakagawa, N. (2003). Difference in food selection between patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus) in Kala Maloue National Park, Cameroon, in relation to nutrient content. Primates, 44(1), 3–11.

    PubMed  Google Scholar 

  • National Research Council. (2001). Nutrient requirements of dairy cattle. Washington, DC: National Academies Press.

    Google Scholar 

  • National Research Council. (2003). Nutrient requirements of nonhuman primates. Washington, DC: National Academies Press.

    Google Scholar 

  • Nekaris, K., & Rasmussen, D. T. (2003). Diet and feeding behavior of Mysore slender lorises. International Journal of Primatology, 24(1), 33–46.

    Article  Google Scholar 

  • Nishie, H. (2011). Natural history of Camponotus ant-fishing by the M group chimpanzees at the Mahale Mountains National Park, Tanzania. Primates, 52(4), 329–342.

    Article  PubMed  Google Scholar 

  • O'Malley, R. C., & Power, M. L. (2012). Nutritional composition of actual and potential insect prey for the Kasekela chimpanzees of Gombe National Park, Tanzania. American Journal of Physical Anthropology, 149(4), 493–503.

    Article  PubMed  Google Scholar 

  • O'Malley, R. C., & Power, M. L. (2014). The energetic and nutritional yields from insectivory for Kasekela chimpanzees. Journal of Human Evolution, 71, 46–58.

    Article  PubMed  Google Scholar 

  • Paoletti, M. G., Norberto, L., Damini, R., & Musumeci, S. (2007). Human gastric juice contains chitinase that can degrade chitin. Annals of Nutrition and Metabolism, 51, 244–251.

    Article  CAS  PubMed  Google Scholar 

  • Pickett, S. B., Bergey, C. M., & Di Fiore, A. (2012). A metagenomic study of primate insect diet diversity. American Journal of Primatology, 74(7), 622–631.

    Article  CAS  PubMed  Google Scholar 

  • Raubenheimer, D., & Rothman, J. M. (2013). Nutritional ecology of entomophagy in humans and other primates. Annual Review of Entomology, 58, 141–160.

    Article  CAS  PubMed  Google Scholar 

  • Redford, K. H., & Dorea, J. G. (1984). The nutritional value of invertebrates with emphasis on ants and termites as food for mammals. Journal of Zoology (London), 203, 385–395.

    Article  CAS  Google Scholar 

  • Robbins, C. T. (1993). Wildlife feeding and nutrition. San Diego: Academic Press.

    Google Scholar 

  • Rode, K. D., Chapman, C. A., Chapman, L. J., & McDowell, L. R. (2003). Mineral resource availability and consumption by colobus in Kibale National Park, Uganda. International Journal of Primatology, 24(3), 541–573.

    Article  Google Scholar 

  • Rode, K. D., Chapman, C. A., McDowell, L. R., & Stickler, C. (2006). Nutritional correlates of population density across habitats and logging intensities in redtail monkeys (Cercopithecus ascanius). Biotropica, 38, 625–634.

    Article  Google Scholar 

  • Rothman, J. M., Chapman, C. A., Hansen, J. L., Cherney, D. J., & Pell, A. N. (2009). Rapid assessment of the nutritional value of foods eaten by mountain gorillas: Applying near-infrared reflectance spectroscopy to primatology. International Journal of Primatology, 30(5), 729–742.

    Article  Google Scholar 

  • Rothman, J. M., Chapman, C. A., & Pell, A. N. (2008a). Fiber-bound protein in gorilla diets: implications for estimating the intake of dietary protein by primates. American Journal of Primatology, 70, 690–694.

    Article  CAS  PubMed  Google Scholar 

  • 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(3), 542–566.

    Article  Google Scholar 

  • Rothman, J. M., Dierenfeld, E. S., Hintz, H. F., & Pell, A. N. (2008b). Nutritional quality of gorilla diets: Consequences of age, sex and season. Oecologia, 155, 111–122.

    Article  PubMed  Google Scholar 

  • Rothman, J. M., Dierenfeld, E. S., Molina, D. O., Shaw, A. V., Hintz, H. F., & Pell, A. N. (2006). Nutritional chemistry of foods eaten by gorillas in Bwindi Impenetrable National Park, Uganda. American Journal of Primatology, 68(7), 675–691.

    Article  CAS  PubMed  Google Scholar 

  • Rothman, J. M., Raubenheimer, D., Bryer, M. A. H., Takahashi, M., & Gilbert, C. C. (2014). Nutritional contributions of insects to primate diets: Implications for primate evolution. Journal of Human Evolution, 71, 59–69.

    Article  PubMed  Google Scholar 

  • Rudran, R. (1978). Socioecology of the blue monkeys (Cercopithecus mitis stuhlmanii) of the Kibale Forest, Uganda. Smithsonian Contributions to Zoology, 249, 1–83.

    Google Scholar 

  • Shorthouse, J. D., & Rohfritsch, O. (1992). Biology of insect-induced galls. Oxford: Oxford University Press.

    Google Scholar 

  • Srivastava, A. (1991). Insectivory and its significance to langur diets. Primates, 32(2), 237–241.

    Article  Google Scholar 

  • Stampone, M. D., Hartter, J., Chapman, C. A., & Ryan, S. J. (2011). Trends and variability in localized precipitation around Kibale National Park, Uganda, Africa. Research Journal of Environmental and Earth Sciences, 3(1), 14–23.

  • Stevenson, P. R., Quiñones, M. J., & Ahumada, J. A. (2000). Influence of fruit availability on ecological overlap among four neotropical primates at Tinigua National Park, Colombia. Biotropica, 32(3), 533–544.

    Article  Google Scholar 

  • Stone, A. I. (2007). Responses of squirrel monkeys to seasonal changes in food availability in an eastern Amazonian forest. American Journal of Primatology, 69(2), 142–157.

    Article  PubMed  Google Scholar 

  • Struhsaker, T. T. (1978). Food habits of five monkey species in the Kibale Forest, Uganda. In D. J. Chivers & J. Herbert (Eds.), Recent advances in primatology (Behaviour, Vol. 1, pp. 225–247). London: Academic Press.

    Google Scholar 

  • Struhsaker, T. T. (1980). Comparison of the behaviour and ecology of red colobus and redtail monkeys in the Kibale Forest, Uganda. African Journal of Ecology18(1), 33–51.

  • Tashiro, Y. (2006). Frequent insectivory by two guenons (Cercopithecus lhoesti and Cercopithecus mitis) in the Kalinzu Forest, Uganda. Primates, 47(2), 170–173.

    Article  PubMed  Google Scholar 

  • Tutin, C. E. (1999). Fragmented living: Behavioural ecology of primates in a forest fragment in the Lopé Reserve, Gabon. Primates, 40(1), 249–265.

    Article  CAS  PubMed  Google Scholar 

  • Tutin, C. E., Ham, R. M., White, L. J., & Harrison, M. J. (1997). The primate community of the Lopé Reserve, Gabon: Diets, responses to fruit scarcity, and effects on biomass. American Journal of Primatology, 42(1), 1–24.

    Article  CAS  PubMed  Google Scholar 

  • Van Soest, P., Robertson, J., & Lewis, B. (1991). Methods for dietary fiber, neutral detergent fiber, and non-starch polysaccharides in relation to animal nutrition. Journal of Dairy Science, 74, 3583–3597.

    Article  PubMed  Google Scholar 

  • Veiga, L. M., & Ferrari, S. F. (2006). Predation of arthropods by southern bearded sakis (Chiropotes satanas) in eastern Brazilian Amazonia. American Journal of Primatology, 68(2), 209–215.

    Article  PubMed  Google Scholar 

  • Webster, T. H., McGrew, W. C., Marchant, L. F., Payne, C. L., & Hunt, K. D. (2014). Selective insectivory at Toro-Semliki, Uganda: Comparative analyses suggest no ‘savanna’chimpanzee pattern. Journal of Human Evolution, 71, 20–27.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the Uganda Wildlife Authority and the Uganda National Council for Science and Technology for permission to conduct this research. We are grateful to Hillary Musinguzi, Richard Mutegeki, Moses Musana, and Peter Irumba for their help with data collection. Thank you to Joanna Setchell and two anonymous reviewers for providing helpful comments to earlier versions of this manuscript. Thank you to Caley Johnson, Jenny Paltan, and Rebecca DelliCarpini for help with nutritional analyses, and Kristin Sabbi and Santiago Cassalett for help with statistical analyses. Thank you to Thomas Struhsaker for his advice on observing redtail monkey insectivory. Thank you to Heikki Roininen for providing preliminary identification of some of the insects eaten by redtail monkeys. This research was funded by Hunter College of the City University of New York, The Wieland Fund for Field Anthropology to M. A. H. Bryer; NSF Grant 0922709 to J. M. Rothman, C. A. Chapman, and J. E. Lambert; and Gravida, the National Research Centre for Growth and Development, New Zealand to D. Raubenheimer.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Margaret A. H. Bryer.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bryer, M.A.H., Chapman, C.A., Raubenheimer, D. et al. Macronutrient and Energy Contributions of Insects to the Diet of a Frugivorous Monkey (Cercopithecus ascanius). Int J Primatol 36, 839–854 (2015). https://doi.org/10.1007/s10764-015-9857-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-015-9857-x

Keywords

Navigation