International Journal of Primatology

, Volume 34, Issue 1, pp 1–14 | Cite as

Are Primates Ecosystem Engineers?

  • Colin A. Chapman
  • Tyler R. Bonnell
  • Jan F. Gogarten
  • Joanna E. Lambert
  • Patrick A. Omeja
  • Dennis Twinomugisha
  • Michael D. Wasserman
  • Jessica M. Rothman
Article

Abstract

Animals can play important roles in structuring the plant communities in which they live. Some species are particularly influential in that they modify the physical environment by changing, maintaining, and/or creating new habitats; the term ecosystem engineer has been used to describe such species. We here assess the two major foraging strategies of primates, frugivory and folivory, in terms of the potential for primates to function as ecosystem engineers. We argue that whereas the role of primates as seed dispersers has received a great deal of attention, the potential role that folivorous primates play in structuring their environment through herbivory has received much less attention. Further, while quantifying if frugivorous primates are ecosystem engineers through their seed dispersal has proved very difficult, it is not as difficult to ascertain whether folivorous primates are ecosystem engineers. We document situations in which folivorous primates act as ecosystem engineers by 1) eating the leaves and/or bark of trees to the extent that they kill trees, 2) feeding on trees to the degree that they slow their growth relative to nonpreferred tree species, 3) eating the flowers of species to the extent that it does not set fruit, or 4) feeding on plants in such a way as to increase their productivity and abundance. Because evidence from the literature is very limited, where possible we present new evidence of these processes from the colobus monkeys at our long-term field site in Kibale National Park, Uganda. We conclude by discussing promising research programs that could be established to refine our understanding of the role primates play in shaping the structure of plant communities, especially tropical forests.

Keywords

Herbivory Keystone modifier Kibale National Park Seed dispersal Tree mortality 

References

  1. Anderson, J. R. (1984). Ethology and ecology of sleep in monkeys and apes. Advances in the Study of Behavior, 14, 166–229.CrossRefGoogle Scholar
  2. Andresen, E. (2000). Ecological roles of mammals: the case of seed dispersal. In A. Entwistle & N. Dunstone (Eds.), Priorities for the conservation of mammalian diversity (pp. 2–26). Cambridge: Cambridge University Press.Google Scholar
  3. Balcomb, S. R., & Chapman, C. A. (2003). Bridging the gap: influence of seed deposition on seedling recruitment in a primate-tree interaction. Ecological Monographs, 73, 625–642.CrossRefGoogle Scholar
  4. Berke, S. K. (2010). Functional groups of ecosystem engineers: a proposed classification with comments on current issues. Integrative and Comparative Biology, 50, 147–157.PubMedCrossRefGoogle Scholar
  5. Chapman, C. A. (1989a). Primate seed dispersal: the fate of dispersed seeds. Biotropica, 21, 148–154.CrossRefGoogle Scholar
  6. Chapman, C. A. (1989b). Spider monkey sleeping sites: use and availability. American Journal Of Primatology, 18, 53–60.CrossRefGoogle Scholar
  7. Chapman, C. A. (1995). Primate seed dispersal: coevolution and conservation implications. Evolutionary Anthropology, 4, 74–82.CrossRefGoogle Scholar
  8. Chapman, C. A., & Onderdonk, D. A. (1998). Forests without primates: primate/plant codependency. American Journal of Primatology, 45, 127–141.PubMedCrossRefGoogle Scholar
  9. Chapman, C. A., & Chapman, L. J. (1997). Forest regeneration in logged and unlogged forests of Kibale National Park, Uganda. Biotropica 29, 396–412.Google Scholar
  10. Chapman, C. A., & Chapman, L. J. (2000). Constraints on group size in redtail monkeys and red colobus: Testing the generality of the ecological constraints model. International Journal of Primatology 21, 565–585.Google Scholar
  11. Chapman, L. J., Chapman, C. A., & Wrangham, R. W. (1992). Balanites-wilsoniana: elephant dependent dispersal. Journal of Tropical Ecology, 8, 275–283.CrossRefGoogle Scholar
  12. Chapman, C. A., Chapman, L. J., Jacob, A. L., Rothman, J. M., Omeja, P. A., Reyna-Hurtado, R., et al. (2010a). Tropical tree community shifts: implications for wildlife conservation. Biological Conservation, 143, 366–374.CrossRefGoogle Scholar
  13. Chapman, C. A., Struhsaker, T. T., Skorupa, J. P., Snaith, T. V., & Rothman, J. M. (2010b). Understanding long-term primate community dynamics: implications of forest change. Ecological Applications, 20, 179–191.CrossRefGoogle Scholar
  14. Crain, C. M., & Bertness, M. D. (2006). Ecosystem engineering across environmental gradients: implications for conservation and management. BioScience, 56, 211–218.CrossRefGoogle Scholar
  15. Creel, S., & Christianson, D. (2009). Wolf presence and increased willow consumption by Yellowstone elk: implications for trophic cascades. Ecology, 90, 2454–2466.PubMedCrossRefGoogle Scholar
  16. Di Fiore, A., & Suarez, S. A. (2007). Route-based travel and shared routes in sympatric spider and woolly monkeys: cognitive and evolutionary implications. Animal Cognition, 10, 317–329.PubMedCrossRefGoogle Scholar
  17. Dittus, W. P. J. (1985). The influence of leaf-monkeys on their feeding trees in a cyclone-disturbed environment. Biotropica, 17, 100–106.CrossRefGoogle Scholar
  18. Dublin, H. T., Sinclair, A. R. E., & McGlade, J. (1990). Elephants and fire as causes of multiple stable states in the Serengeti Mara woodlands. Journal of Animal Ecology, 59, 1147–1164.CrossRefGoogle Scholar
  19. Estes, J. A., & Palmisano, J. F. (1974). Sea otters: their role in structuring nearshore communities. Science, 185, 1058–1060.PubMedCrossRefGoogle Scholar
  20. Estrada, A., & Coates-Estrada, R. (1984). Fruit eating and seed dispersal by howling monkeys (Alouatta palliata) in the tropical rain forest of Los Tuxtlas, Mexico. American Journal of Primatology, 6, 77–91.CrossRefGoogle Scholar
  21. Fashing, P., & Cords, M. (2000). Diurnal primate densities and biomass in the Kakamega Forest: An evaluation of census methodology. American Journal of Primatology, 50(2), 139–152.Google Scholar
  22. Feeley, K. J., & Terborgh, J. W. (2005). The effects of herbivore density on soil nutrients and tree growth in tropical fragments. Ecology, 86, 116–124.CrossRefGoogle Scholar
  23. Feeley, K. J., & Terborgh, J. W. (2006). Direct versus indirect effects of habitat reduction on the loss of avian species from tropical forest fragments. Animal Conservation, 11, 353–360.CrossRefGoogle Scholar
  24. Forsyth, A., & Miyata, K. (1984). Tropical nature: Life and death in the rain forest of central and south America. New York: Touchstone Books.Google Scholar
  25. Fossey, D., & Harcourt, A. H. (1977). Feeding ecology of free-ranging mountain gorillas. In T. H. Clutton-Brock (Ed.), Primate ecology. London: Academic.Google Scholar
  26. Gautier-Hion, A., Duplantier, J. M., Quris, R., Feer, F., Sourd, C., Decous, J. P., et al. (1985). Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia, 65, 324–337.CrossRefGoogle Scholar
  27. Gilmore, D. P., DaCosta, C. P., & Duarte, D. P. F. (2001). Sloth biology: an update on theri physiological ecology, bahvior, and role as vectors of arthropodes and arboviruses. Brazilian Journal of Medical and Biological Research, 34, 9–25.PubMedCrossRefGoogle Scholar
  28. Gogarten, J. F., Brown, L. M., Chapman, C. A., Marina, C., Doran-Sheehy, D., Fedigan, L. M., et al. (2012). Seasonal mortality patterns in non-human primates: Implications for variation in selection pressures across environments. Evolution 66, 3252–3266.Google Scholar
  29. Harris, T. R., & Chapman, C. A. (2007). Variation in the diet and ranging behavior of black-and-white colobus monkeys: implications for theory and conservation. Primates, 28, 208–221.CrossRefGoogle Scholar
  30. Herrera, C. (1985). Determinants of plant-animal coevolution: the case of mutualistic dispersal of seeds by vertebrates. Oikos, 44, 132–141.CrossRefGoogle Scholar
  31. Hladik, C. M. (1977). A comparative study of the feeding strategies of two sympatric species of leaf monkeys: Presbytis senex and Presbytis entellus. In T. H. Clutton-Brock (Ed.), Primate ecology (pp. 324–353). Cambridge: Cambridge University Press.Google Scholar
  32. Howe, H. F., & Smallwood, J. (1982). Ecology of seed dispersal. Annual Review of Ecology and Systematics, 13, 201–228.CrossRefGoogle Scholar
  33. Janson, C. H., & Chapman, C. A. (1999). Resources and the determination of primate community structure. In J. G. Fleagle, C. H. Janson, & K. E. Reed (Eds.), Primate communities (pp. 237–267). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  34. Jin-Eong, O. (1995). The ecology of mangrove conservation and management. Hydrobiologia, 295, 343–351.CrossRefGoogle Scholar
  35. Jones, C. G., Lawton, J. H., & Shachak, M. (1994). Organisms as ecosystem engineers. Oikos, 69, 373–386.CrossRefGoogle Scholar
  36. Jones, C. G., Lawton, J. H., & Shachak, M. (1997). Ecosystem engineering by organisms: why semantics matters. Trends in Ecology and Evolution, 12, 275.PubMedCrossRefGoogle Scholar
  37. Jordano, P., Forget, P. M., Lambert, J. E., Bohning-Gaese, K., Traveset, A., & Wright, S. (2011). Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction. Biology Letters, 7, 321–323.PubMedCrossRefGoogle Scholar
  38. Kaplin, B. A., & Lambert, J. E. (2002). Effectiveness of seed dispersal by Cercopithecus monkeys: Implications for seed input into degraded areas. In D. J. Levey, W. R. Silva, & M. Galetti (Eds.), Seed dispersal and frugivory: Ecology, evolution and conservation (pp. 351–364). New York: CABI Publishing.Google Scholar
  39. Lambert, J. E. (1997). Fruit processing and seed dispersal by chimpanzees (Pan troglodytes schweinfurthii) and redtail monkeys (Cercopithecus ascanius schmidti) in the Kibale National Park. Urbana: Uganda. University of Illinois.Google Scholar
  40. Lambert, J. E., & Garber, P. A. (1998). Evolutionary and ecological implications of primate seed dispersal. American Journal of Primatology, 45, 9–28.PubMedCrossRefGoogle Scholar
  41. Lawes, M. J., & Chapman, C. A. (2006). Does the herb Acanthus pubescens and/or elephants suppress tree regeneration in disturbed Afrotropical forests? Forest Ecology and Management, 221, 274–284.CrossRefGoogle Scholar
  42. Laws, R. M. (1970). Elephants as agents of habitat and landscape change in East Africa. Oikos, 21, 1–15.CrossRefGoogle Scholar
  43. Leiberman, D., Hall, J. B., Swaine, M. D., & Lieberman, M. (1979). Seed dispersal by baboons in the Shai Hills, Ghana. Ecology, 60, 65–75.CrossRefGoogle Scholar
  44. Levey, D. J., Tewksbury, J. J., & Bolker, B. M. (2008). Modelling long-distance seed dispersal in heterogeneous landscapes. Journal of Ecology, 96, 599–608.CrossRefGoogle Scholar
  45. Ludwig, D., Jones, D. D., & Holling, C. S. (1978). Qualitative analysis of insect outbreak systesm: spruce-budworm and forest. Journal of Animal Ecology, 47, 315–332.CrossRefGoogle Scholar
  46. McConkey, K. R., Aldy, F., Ario, A., & Chivers, D. J. (2002). Selection of fruit by Gibbons (Hylobates muelleri × agilis) in the rain forests of Central Borneo. International Journal of Primatology, 23, 123–145.CrossRefGoogle Scholar
  47. McNaughton, S. J. (1976). Serengeti wildebeest: facilitation of energy flow by grazing. Science, 193, 92–94.CrossRefGoogle Scholar
  48. McNaughton, S. J. (1977). Grazing as an optimizatino process: grassland-ungulate relationships in the Serengeti. American Naturalist, 113, 691–703.Google Scholar
  49. Milton, K. (1980). The foraging strategies of howler monkeys: A study in primate economics. New York: Columbia University Press.Google Scholar
  50. Montgomery, G. G., & Sunquist, M. E. (1975). Impact of sloths on neotropical energy flow and nutrient cycling. In E. Medina & F. Golly (Eds.), Trends in tropical ecology (pp. 69–98). New York: Springer.CrossRefGoogle Scholar
  51. Naiman, R. J. (1988). Animal influences on ecosystem dynamics. Bioscience, 38, 750–752.CrossRefGoogle Scholar
  52. Nathan, R., & Muller-Landau, H. C. (2000). Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends in Ecology & Evolution, 15, 278–285.CrossRefGoogle Scholar
  53. Neves, N. D. S., Feer, F., Salmon, S., Chateil, C., & Ponge, J.-F. (2010). The impact of red howler monkey latrines on the distribution of main nutrients and on topsoil profiles in a tropical rain forest. Austral Ecology, 35, 549–559.CrossRefGoogle Scholar
  54. Nunes-Iturri, G., & Howe, H. F. (2007). Bushmeat and the fate of trees with seeds dispersed by large primates in a lowland rain forest in western Amazonia. Biotropica, 39, 348–354.CrossRefGoogle Scholar
  55. Oates, J. F. (1974). The ecology and behaviour of the black-and-white colobus monkey (Colobus guereza Ruppell) in East Africa. London: University of London.Google Scholar
  56. Oates, J. F. (1977). The guereza and its food. In T. H. Clutton-Brock (Ed.), Primate ecology (pp. 275–321). New York: Academic.Google Scholar
  57. Oppenheimer, J. R., & Lang, G. E. (1969). Cebus monkeys: effect on branching of Gustavia trees. Science, 165, 187–188.PubMedCrossRefGoogle Scholar
  58. Pacheco, L. F., & Simonetti, J. A. (2000). Genetic structure of a mimosoid tree deprived of its seed disperser, the spider monkey. Conservation Biology, 14, 1766–1775.CrossRefGoogle Scholar
  59. Pastor, J., Cohen, Y., & Moen, R. (1999). Generation of spatial patterns in boreal forest landscapes. Ecosystems, 2, 439–452.CrossRefGoogle Scholar
  60. Pavelka, M. S. M., & Behie, A. M. (2005). The effect of hurricane iris on the food supply of black howlers (Alouatta pigra) in southern Belize. Biotropica, 37, 102–108.CrossRefGoogle Scholar
  61. Pavelka, M. S. M., Brusselers, O. T., Nowak, D., & Behie, A. M. (2003). Population reduction and social disorganization in Alouatta pigra following a hurricane. International Journal Of Primatology, 24, 1037–1055.CrossRefGoogle Scholar
  62. Peres, C. A., & Dolman, P. M. (2000). Density compensation in neotropical primate communities: evidence from 56 hunted and nonhunted Amazonian forest of varying productivity. Oecologia, 122, 175–189.CrossRefGoogle Scholar
  63. Persson, I.-L., Bergstrom, R., & Danell, K. (2007). Browse biomass production an.regrowth capacity after biomass loss in deciduous and coniferous trees: responses to moose browsing along a productivity gradient. Oikos, 116, 1639–1650.CrossRefGoogle Scholar
  64. Plumptre, A. J. (1993). The effects of trampling damage by herbivores on the vegetation of the Parc National des Volcans, Rwanda. African Journal of Ecology, 32, 115–129.CrossRefGoogle Scholar
  65. Potvin, C., Lechowicz, M. J., & Tardif, S. (1990). The statistical-analysis of ecophysiological response curves obtained from experiments involving repeated measures. Ecology, 71, 1389–1400.CrossRefGoogle Scholar
  66. Poulsen, J. R., Clark, C. J., Connor, E. F., & Smith, T. B. (2002). Differential resource use by primates and hornbills: implications for seed dispersal. Ecology, 83, 228–240.CrossRefGoogle Scholar
  67. Power, M. (1997). Ecosystem engineering by organisms: why semantics matters, reply. Trends in Ecology and Evolution, 12, 275–276.PubMedCrossRefGoogle Scholar
  68. Reichman, O. J., & Seabloom, E. W. (2002). Ecosystem engineering: a trivialized concept? Response. Trends in Ecology and Evolution, 17, 308.CrossRefGoogle Scholar
  69. Riba-Hernandez, P., & Stoner, K. E. (2005). Massive destruction of Symphonia globulifera (Clusiaceae) flowers by Central American spider monkeys (Ateles geoffroyi). Biotropica, 37, 274–278.CrossRefGoogle Scholar
  70. Ripple, W. J. B., & Beschta, R. L. (2005). Wolves and the ecology of fear: can predation risk structure ecosystems? BioScience, 54, 755–766.CrossRefGoogle Scholar
  71. Russo, S. S., & Chapman, C. A. (2011). Primate seed dispersal: Linking behavioural ecology and forest community structure. In C. J. Campbell, A. F. Fuentes, J. C. MacKinnon, M. Panger, & S. Bearder (Eds.), Primates in perspective (pp. 523–534). Oxford: Oxford University Press.Google Scholar
  72. Schupp, E. W. (1993). Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio, 108, 15–29.Google Scholar
  73. Schupp, E. W., Jordano, P., & Gomez, J. M. (2010). Seed dispersal effectiveness revisited: a conceptual review. New Phytologist, 188, 333–335.PubMedCrossRefGoogle Scholar
  74. Singer, F. J., & Shoenecker, K. E. (2003). Do ungulates accelerate of decelerate nitrogen cycling? Forest Ecology and Management, 181, 189–204.CrossRefGoogle Scholar
  75. Stevenson, P. R. (2011). The abundance of large Ateline monkeys is positively associated with the diversity of plants regenerating in Neotropical forests. Biotropica, 42, 512–519.CrossRefGoogle Scholar
  76. Stoner, K. E., Riba-Hernandez, P., Vulinec, K., & Lambert, J. E. (2007). The role of mammals in creating a modifying seed shadows in tropical forests and some possible consequences of their elimination. Biotropica, 39, 316–327.CrossRefGoogle Scholar
  77. Struhsaker, T. T. (1978). Interrelations of red colobus monkeys and rain-forest trees in the Kibale Forest, Uganda. In G. G. Montgomery (Ed.), The ecology of arboreal folivore (pp. 397–422). Washington: Smithsonian Institution Press.Google Scholar
  78. Stuart, N. O. E., Hatton, J. C., & Spencer, D. H. N. (1985). The effect of long-term exclusion of large herbivores on vegetation in Murchison Falls National Park, Uganda. Biological Conservation, 22, 229–245.Google Scholar
  79. Terborgh, J., Pitman, M., Silman, H., Schichter, P., & Nunez, V. (2002). Maintenance of tree diversity in tropical forests. In D. Levey, W. Silva, & M. Galetti (Eds.), Seed dispersal and frugivory: Ecology, evolution and conservation (pp. 1–18). Wallingford: CABI Publishing.Google Scholar
  80. VanNimwegen, R. E., Kretzer, J., & Cully, J. F. (2008). Ecosystem engineering by a colonial mammal: how praire dogs structure rodent communities. Ecology, 89, 3298–3305.PubMedCrossRefGoogle Scholar
  81. Watts, D. P. (1987). Effects of mountain gorilla foraging activities on the productivity of their food plant species. African Journal of Ecology, 25, 155–163.CrossRefGoogle Scholar
  82. Watts, D. P. (1998). Long-term habitat use by mountain gorillas (Gorilla gorilla beringei). 2. Reuse of foraging areas in relation to resource abundance, quality, and depletion. International Journal of Primatology, 19, 681–702.CrossRefGoogle Scholar
  83. Wilby, A. (2002). Ecosystem engineering: a trivialized concept? Trends in Ecology and Evolution, 17, 307.CrossRefGoogle Scholar
  84. Wrangham, R. W., Chapman, C. A., & Chapman, L. J. (1994). Seed dispersal by forest chimpanzees in Uganda. Journal of Tropical Ecology, 10, 355–368.CrossRefGoogle Scholar
  85. Wright, S. J. (2003). The myriad consequences of hunting for vertebrates and plants in tropical forests. Perspectives in Plant Ecology, Evolution, and Systematics, 6, 73–86.CrossRefGoogle Scholar
  86. Wright, J. P., & Jones, C. G. (2006). The concept of organisms as ecosystem engineers ten years on: progress, limitations, and challenges. BioScience, 56, 203–209.CrossRefGoogle Scholar
  87. Wright, J. S., Hernandez, A., & Condit, R. (2007). The bushmeat harvest alters seedling banks by favoring lianas, large seeds and seeds dispersed by bats, birds, and wind. Biotropica, 39, 363–371.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Colin A. Chapman
    • 1
    • 2
  • Tyler R. Bonnell
    • 3
  • Jan F. Gogarten
    • 4
  • Joanna E. Lambert
    • 5
  • Patrick A. Omeja
    • 6
  • Dennis Twinomugisha
    • 6
  • Michael D. Wasserman
    • 7
  • Jessica M. Rothman
    • 8
    • 9
  1. 1.McGill School of Environment and Department of AnthropologyMcGill UniversityMontrealCanada
  2. 2.Wildlife Conservation SocietyBronxUSA
  3. 3.Department of GeographyMcGill UniversityMontrealCanada
  4. 4.Department of BiologyMcGill UniversityMontrealCanada
  5. 5.Department of AnthropologyUniversity of TexasSan AntonioUSA
  6. 6.Makerere University Biological Field StationKampalaUganda
  7. 7.Department of AnthropologyMcGill UniversityMontrealCanada
  8. 8.Department of AnthropologyHunter College of the City University of New YorkNew YorkUSA
  9. 9.New York Consortium in Evolutionary PrimatologyNew YorkUSA

Personalised recommendations