Using Giving-Up Densities to Test for Dietary Preferences in Primates: An Example with Samango Monkeys ( Cercopithecus (nictitans) mitis erythrarchus)

Abstract

Teasing apart the components of diet selection is important for understanding an animal’s ecology. We used giving-up densities (GUDs) in artificial food patches to test whether free-ranging samango monkeys (Cercopithecus (nictitans) mitis erythrarchus) treat food and water as complementary resources and to examine dietary preferences. To assess the influence of water on the value of food, we measured harvest of peanuts from food patches augmented with water. To examine dietary preferences, we measured the harvest of peanuts (as a standard for comparing other food classes), raisins, alfalfa pellets, and either mealworms or cat food mixed into sawdust in separate food patches. In addition, we observed the samangos’ order of selection of each food. To differentiate preference from ease of encounter, we measured selectivity for peanuts in triplets of food patches containing 1) peanuts, 2) peanuts mixed with a test food (raisins, alfalfa, or mealworms), and 3) the test food. Water did not influence samango foraging. After peanuts, the samangos treated alfalfa and raisins as approximately equal. The samangos foraged on mealworms lightly and rejected cat food. When each food was mixed with peanuts, the monkeys exhibited an expanding specialist dietary strategy in which they altered their rates of encounter with their preferred foods at high resource densities. Samango monkeys at our study site are not water limited, they consistently favor high-energy foods, and they least often choose animal protein. We conclude that patch-use experiments coupled with direct observations provide a useful means for examining dietary strategy, food preferences, and water limitation.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Abu Baker, M. A., & Brown, J. S. (2009). Patch area, substrate depth, and richness affect giving-up densities: a test with mourning doves and cottontail rabbits. Oikos, 118, 1721–1731.

    Article  Google Scholar 

  2. Abu Baker, M. A., & Brown, J. S. (2010). Islands of fear: effects of wooded patches on habitat suitability of the striped mouse in a South African grassland. Functional Ecology, 24, 1313–1322.

    Article  Google Scholar 

  3. Altendorf, K. B., Laundré, J. W., López González, C. A., & Brown, J. S. (2001). Assessing effects of predation risk on foraging behavior of mule deer. Journal of Mammalogy, 82, 430–439.

    Article  Google Scholar 

  4. Barton, R. A., Whiten, A., Strum, S. C., Byrne, R. W., & Simpson, A. J. (1992). Habitat use and resource availability in baboons. Animal Behaviour, 43, 831–844.

    Article  Google Scholar 

  5. Beeson, M. (1989). Seasonal dietary stress in a forest monkey (Cercopithecus mitis). Oecologia, 78, 565–570.

    Article  Google Scholar 

  6. Bowers, M. A., Jefferson, J. L., & Kuebler, M. G. (1993). Variation in giving-up densities of foraging chipmunks (Tamias striatus) and squirrels (Sciurus carolinensis). Oikos, 66, 229–236.

    Article  Google Scholar 

  7. Brown, J. S. (1988). Patch use as an indicator of habitat preference, predation risk, and competition. Behavioral Ecology and Sociobiology, 22, 37–47.

    Article  Google Scholar 

  8. Brown, J. S. (1992). Patch use under predation risk I: models and predictions. Annales Zoologici Fennici, 29, 301–309.

    Google Scholar 

  9. Brown, J. S. (2000). Foraging ecology of animals in response to heterogeneous environments. In J. Hutchings & A. Stewart (Eds.), The ecological consequences of environmental heterogeneity (pp. 181–215). Oxford: Blackwell Scientific.

    Google Scholar 

  10. Brown, J. S., & Kotler, B. P. (2004). Hazardous duty pay and the foraging cost of predation. Ecology Letters, 7, 999–1014.

    Article  Google Scholar 

  11. Brown, J. S., & Mitchell, W. A. (1989). Diet selection on depletable resources. Oikos, 54, 33–43.

    Article  Google Scholar 

  12. Brown, J. S., & Morgan, R. A. (1995). Effects of foraging behavior and spatial scale on diet selectivity: a test with fox squirrels. Oikos, 74, 122–136.

    Article  Google Scholar 

  13. Brugiere, D., Gautier, J., Moungazi, A., & Gautier-Hion, A. (2002). Primate diet and biomass in relation to vegetation composition and fruiting phenology in a rain forest in Gabon. International Journal of Primatology, 23, 999–1024.

    Article  Google Scholar 

  14. Bruorton, M. R., Davis, C. L., & Perrin, M. R. (1991). Gut microflora of vervet and samango monkeys in relation to diet. Applied and Environmental Microbiology, 57, 573–578.

    PubMed  CAS  Google Scholar 

  15. Buzzard, P. J. (2006). Ecological partitioning of Cercopithecus campbelli, C. petaurista, and C. diana in the Taï Forest. International Journal of Primatology, 27, 529–558.

    Article  Google Scholar 

  16. Chapman, C. A. (1988). Patterns of foraging and range use by three species of neotropical primates. Primates, 29, 177–194.

    Article  Google Scholar 

  17. Charnov, E. L. (1976). Optimal foraging theory, the marginal value theorem. Theoretical Population Biology, 9, 129–136.

    PubMed  Article  CAS  Google Scholar 

  18. Chesson, J. (1983). The estimation and analysis of preference and its relationship to foraging models. Ecology, 64, 1297–1304.

    Article  Google Scholar 

  19. Cordeiro, N. J. (1994). Opportunist killers – blue monkeys feed on forest birds. Folia Primatologica, 63, 84–87.

    Article  Google Scholar 

  20. 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 

  21. Culver, D. C., & Beattie, A. J. (1978). Myrmecochory in Viola: dynamics of seed-ant interactions in some West Virginia species. Journal of Ecology, 66, 53–72.

    Article  Google Scholar 

  22. Di Bitetti, M. S., & Janson, C. H. (2001). Social foraging and the finder’s share in capuchin monkeys, Cebus apella. Animal Behaviour, 62, 47–56.

    Article  Google Scholar 

  23. Emerson, S. E., Brown, J. S., & Linden, J. D. (2011). Identifying Sykes’ monkeys’, Cercopithecus albogularis erythrarchus, axes of fear through patch use. Animal Behaviour, 81, 455–462.

    Article  Google Scholar 

  24. Emerson, S. E., Brown, J. S., Whelan, C. J., & Schmidt, K. A. (2012). Scale-dependent neighborhood effects: shared doom and associational refuge. Oecologia, 168, 659–670.

    PubMed  Article  Google Scholar 

  25. Fairgrieve, C., & Muhumuza, G. (2003). Feeding ecology and dietary differences between blue monkey (Cercopithecus mitis stuhlmanni Matschie) groups in logged and unlogged forest, Budongo Forest Reserve, Uganda. African Journal of Ecology, 41, 141–149.

    Article  Google Scholar 

  26. Garb, J., Kotler, B. P., & Brown, J. S. (2000). Foraging and community consequences of seed size for coexisting crested lark and Allenby’s gerbil. Oikos, 88, 291–300.

    Article  Google Scholar 

  27. Gautier-Hion, A. (1983). Leaf consumption by monkeys in western and eastern Africa: comparison. African Journal of Ecology, 21, 107–113.

    Article  Google Scholar 

  28. Hahn, N. (2006). Floristic diversity of the Soutpansberg, Limpopo Province, South Africa. Ph.D. thesis, University of Pretoria, Pretoria, South Africa.

  29. Hay, M. E., & Fuller, P. J. (1981). Seed escape from heteromyid rodents: the importance of microhabitat and seed preference. Ecology, 62, 1395–1399.

    Article  Google Scholar 

  30. Heikamp, B. (2008). The role of cheek pouches in seed dispersal: An analysis of dispersal methods within a free ranging group of Sykes’ monkeys (Cercopithecus albogularis) in the Western Soutpansberg, South Africa. Diploma Thesis. Julius Maximilians University, Würzburg, Germany.

  31. Heller, R. (1980). On optimal diet in a patchy environment. Theoretical Population Biology, 17, 201–214.

    PubMed  Article  CAS  Google Scholar 

  32. Hochman, V., & Kotler, B. P. (2006). Effects of food quality, diet preference and water on patch use by Nubian ibex. Oikos, 112, 547–554.

    Article  Google Scholar 

  33. Hochman, V., & Kotler, B. P. (2007). Patch use, apprehension, and vigilance behavior of Nubian ibex under perceived risk of predation. Behavioral Ecology, 18, 368–374.

    Article  Google Scholar 

  34. Houle, A., Vickery, W., & Chapman, C. (2006). Testing mechanisms of coexistence among two species of frugivorous primates. Journal of Animal Ecology, 75, 1034–1044.

    PubMed  Article  Google Scholar 

  35. Iredale, S. K., Nevill, C. H., & Lutz, C. K. (2010). The influence of observer presence on baboon (Papio spp.) and rhesus macaque (Macaca mulatta) behavior. Applied Animal Behaviour Science, 122, 53–57.

    PubMed  Article  Google Scholar 

  36. Isbell, L. A., & Young, T. (1993). Human presence reduces predation in a free-ranging vervet monkey population in Kenya. Animal Behaviour, 45, 1233–1235.

    Article  Google Scholar 

  37. Janmaat, K. R. L., Chapman, C. A., Meijer, R., & Zuberbühler, K. (2012). The use of fruiting synchrony by foraging mangabey monkeys: a ‘simple tool’ to find fruit. Animal Cognition, 15, 83–96.

    PubMed  Article  CAS  Google Scholar 

  38. Jones, L. D., Cooper, R. W., & Harding, R. S. (1972). Composition of mealworm Tenebrio molitor larvae. The Journal of Zoo Animal Medicine, 3, 34–41.

    Article  Google Scholar 

  39. Kaplin, B. A. (2001). Ranging behavior of two species of guenons (Cercopithecus lhoesti and C. mitis doggetti ) in the Nyungwe Forest Reserve, Rwanda. International Journal of Primatology, 22, 521–548.

    Article  Google Scholar 

  40. Kaplin, B. A., & Moermond, T. C. (1998). Variation in seed handling by two species of forest monkeys in Rwanda. American Journal of Primatology, 45, 83–101.

    PubMed  Article  CAS  Google Scholar 

  41. Kotler, B. P., Dickman, C. R., & Brown, J. S. (1998). The effects of water on patch use by two Simpson Desert granivores (Corvus coronoides and Pseudomys hermannsburgensis). Australian Journal of Ecology, 23, 574–578.

    Article  Google Scholar 

  42. Lambert, J. E. (1998). Primate digestion: interactions among anatomy, physiology, and feeding ecology. Evolutionary Anthropology, 7, 8–20.

    Article  Google Scholar 

  43. Lambert, J. E. (1999). Seed handling in chimpanzees (Pan troglodytes) and redtail monkeys (Cercopithecus ascanius): implications for understanding hominoid and cercopithecine fruit-processing strategies and seed dispersal. American Journal of Physical Anthropology, 109, 365–386.

    PubMed  Article  CAS  Google Scholar 

  44. Lambert, J. E. (2001). Red-tailed guenons (Cercopithecus ascanius) and Strychnos mitis: evidence for plant benefits beyond seed dispersal. International Journal of Primatology, 22, 189–201.

    Article  Google Scholar 

  45. Lambert, J. E. (2007). Primate nutritional ecology. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 482–495). Oxford: Oxford University Press.

    Google Scholar 

  46. Lambert, J. E., & Chapman, C. A. (2005). The fate of primate dispersed seeds: Deposition pattern, dispersal distance, and implications for conservation. In P. M. Forget, J. E. Lambert, P. Hulme, & S. Vander Wall (Eds.), Seed fate: Predation, dispersal and seedling establishment (pp. 137–150). Wallingford: CAB International Publishers.

    Google Scholar 

  47. Lawes, M. J. (1991). Diet of samango monkeys (Cercopithecus mitis erythrarchus) in the Cape Vidal dune forest, South Africa. Journal of Zoology, 224, 149–173.

    Article  Google Scholar 

  48. Makin, D. F., Payne, H. F. P., Kerley, G. I. H., & Shrader, A. M. (2012). Foraging in a 3-D world: How does predation risk affect space use of vervet monkeys? Journal of Mammalogy, 93, 422–428.

    Article  Google Scholar 

  49. Manly, B. F. J. (1974). A model for certain types of selection experiments. Biometrics, 30, 281–294.

    Article  Google Scholar 

  50. Morris, D. W., Kotler, B. P., Brown, J. S., Sundararaj, V., & Ale, S. B. (2009). Behavioral indicators for conserving mammalian diversity. The Year in Ecology and Conservation Biology, 1162, 334–356.

    Google Scholar 

  51. Nagy, K. A., & Milton, K. (1979). Aspects of dietary quality, nutrient assimilation and water balance in wild howler monkeys (Alouatta palliata). Oecologia, 39, 249–258.

    Article  Google Scholar 

  52. Olsson, O., Brown, J. S., & Smith, H. G. (2002). Long- and short-term state-dependent foraging under predation risk: An indication of habitat quality. Animal Behaviour, 63, 1–9.

    Article  Google Scholar 

  53. Oyugi, J. O., & Brown, J. S. (2003). Giving-up densities and habitat preferences of European starlings and American robins. Condor, 105, 130–135.

    Article  Google Scholar 

  54. Rudran, R. (1978). Socioecology of the blue monkeys (Cercopithecus mitis stuhlmanni) of the Kibale Forest, Uganda. Smithsonian Contributions to Zoology, 249, 88 p. Washington, DC: Smithsonian Institution Press.

  55. Schmidt, K. A., Brown, J. S., & Morgan, R. (1998). Plant defenses as complementary resources: a test with squirrels. Oikos, 81, 130–142.

    Article  Google Scholar 

  56. Shrader, A., Kotler, B. P., Brown, J. S., & Kerley, G. I. H. (2008). Providing water for goats in arid landscapes: Effects on feeding effort with regard to time period, herd size and secondary compounds. Oikos, 117, 466–472.

    Article  Google Scholar 

  57. Skinner, J. D., & Chimimba, C. T. (2005). The mammals of the Southern African sub-region (3rd ed.). Cambridge: Cambridge University Press.

    Google Scholar 

  58. Sterck, E. H. M., & Steenbeek, R. (1997). Female dominance relationships and food competition in the sympatric Thomas langur and long-tailed macaque. Behaviour, 134, 749–774.

    Article  Google Scholar 

  59. Tilman, D. (1982). Resource competition and community structure. Princeton: Princeton University Press.

    Google Scholar 

  60. Turner, V. L. (2003). Effects of seed preference and selectivity by Microtus and Peromyscus at an Illinois prairie restoration. Ph.D. dissertation. University of Illinois at Chicago.

  61. Valone, T. J., & Brown, J. S. (1989). Measuring patch assessment abilities of desert granivores. Ecology, 70, 1800–1810.

    Article  Google Scholar 

  62. van Schaik, C. P., Marshall, A. J., & Wich, S. A. (2009). Geographic variation in orangutan behavior and biology: Its functional interpretation and its mechanistic basis. In S. A. Wich, S. S. Utami Atmoko, T. Mitra Setia, & C. P. van Schaik (Eds.), Orangutans: Geographic variation in behavioral ecology and conservation (pp. 351–361). New York: Oxford University Press.

    Google Scholar 

  63. Vogel, E. R., Haag, L., Mitra-Setia, T., van Schaik, C. P., & Dominy, N. J. (2009). Foraging and ranging behavior during a fallback episode: Hylobates albibarbis and Pongo pygmaeus wurmbii compared. American Journal of Physical Anthropology, 140, 1096–8644.

    Article  Google Scholar 

  64. Wahome, J. M., Cords, M., & Rowell, T. E. (1988). Blue monkeys eat mice. Folia Primatologica, 51, 158–160.

    Article  CAS  Google Scholar 

  65. Whelan, C. J., & Jedlicka, D. M. (2007). Augmenting population monitoring programs with behavioral indicators during ecological restorations. Israel Journal of Ecology and Evolution, 53, 279–295.

    Article  Google Scholar 

  66. Wittig, R. M., & Boesch, C. (2003). Food competition and linear dominance hierarchy among female chimpanzees of the Taï National Park. International Journal of Primatology, 24, 847–867.

    Article  Google Scholar 

  67. Worman, C. O., & Chapman, C. A. (2005). Seasonal variation in the quality of a tropical ripe fruit and the response of three frugivores. Journal of Tropical Ecology, 21, 689–697.

    Article  Google Scholar 

  68. Wrangham, R. W., & Waterman, P. G. (1981). Feeding behaviour of vervet monkeys on Acacia tortilis and Acacia xanthophloea: With special reference to reproductive strategies and tannin production. Journal of Animal Ecology, 50, 715–731.

    Article  Google Scholar 

  69. Wrangham, R. W., Conklin-Brittain, N., & Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. I. Antifeedants. International Journal of Primatology, 19, 949–970.

    Article  Google Scholar 

Download references

Acknowledgments

This project was supported by the Animal Behavior Society and the UIC LEAP IGERT. We thank Ian and Retha Gaigher of the Lajuma Research Centre for their accommodation of and assistance with this research. We thank M. Abu Baker, L. Coret, E. Cottin, B. Samphire, L. Toft, A. McIntosh, N. Pedersen, E. M. Rambuda, M. Brown, S. Sullivan, and E. Hancock for their field assistance. We also thank two anonymous reviewers and J. Rothman for suggestions that improved an earlier version of the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Sara E. Emerson.

Mean Giving Up Densities and Rankings of Foods in Experiments 1–5

Mean Giving Up Densities and Rankings of Foods in Experiments 1–5

 

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Emerson, S.E., Brown, J.S. Using Giving-Up Densities to Test for Dietary Preferences in Primates: An Example with Samango Monkeys ( Cercopithecus (nictitans) mitis erythrarchus). Int J Primatol 33, 1420–1438 (2012). https://doi.org/10.1007/s10764-012-9631-2

Download citation

Keywords

  • Cercopithecus (nictitans) mitis erythrarchus
  • Diet selection
  • Giving-up density
  • Primate foraging
  • Samango monkey