Are Primates Ecosystem Engineers?

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.

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References

  1. Anderson, J. R. (1984). Ethology and ecology of sleep in monkeys and apes. Advances in the Study of Behavior, 14, 166–229.

    Article  Google 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.

    Article  Google 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.

    PubMed  Article  Google Scholar 

  5. Chapman, C. A. (1989a). Primate seed dispersal: the fate of dispersed seeds. Biotropica, 21, 148–154.

    Article  Google Scholar 

  6. Chapman, C. A. (1989b). Spider monkey sleeping sites: use and availability. American Journal Of Primatology, 18, 53–60.

    Article  Google Scholar 

  7. Chapman, C. A. (1995). Primate seed dispersal: coevolution and conservation implications. Evolutionary Anthropology, 4, 74–82.

    Article  Google Scholar 

  8. Chapman, C. A., & Onderdonk, D. A. (1998). Forests without primates: primate/plant codependency. American Journal of Primatology, 45, 127–141.

    PubMed  Article  CAS  Google 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.

  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.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  14. Crain, C. M., & Bertness, M. D. (2006). Ecosystem engineering across environmental gradients: implications for conservation and management. BioScience, 56, 211–218.

    Article  Google Scholar 

  15. Creel, S., & Christianson, D. (2009). Wolf presence and increased willow consumption by Yellowstone elk: implications for trophic cascades. Ecology, 90, 2454–2466.

    PubMed  Article  Google 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.

    PubMed  Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  19. Estes, J. A., & Palmisano, J. F. (1974). Sea otters: their role in structuring nearshore communities. Science, 185, 1058–1060.

    PubMed  Article  CAS  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    PubMed  Article  CAS  Google 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.

    Article  Google Scholar 

  30. Herrera, C. (1985). Determinants of plant-animal coevolution: the case of mutualistic dispersal of seeds by vertebrates. Oikos, 44, 132–141.

    Article  Google 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.

    Article  Google 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.

    Google Scholar 

  34. Jin-Eong, O. (1995). The ecology of mangrove conservation and management. Hydrobiologia, 295, 343–351.

    Article  Google Scholar 

  35. Jones, C. G., Lawton, J. H., & Shachak, M. (1994). Organisms as ecosystem engineers. Oikos, 69, 373–386.

    Article  Google 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.

    PubMed  Article  CAS  Google 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.

    PubMed  Article  Google 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.

    PubMed  Article  CAS  Google 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.

    Article  Google Scholar 

  42. Laws, R. M. (1970). Elephants as agents of habitat and landscape change in East Africa. Oikos, 21, 1–15.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  47. McNaughton, S. J. (1976). Serengeti wildebeest: facilitation of energy flow by grazing. Science, 193, 92–94.

    Article  Google 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.

    Google Scholar 

  51. Naiman, R. J. (1988). Animal influences on ecosystem dynamics. Bioscience, 38, 750–752.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    PubMed  Article  CAS  Google 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.

    Article  Google Scholar 

  59. Pastor, J., Cohen, Y., & Moen, R. (1999). Generation of spatial patterns in boreal forest landscapes. Ecosystems, 2, 439–452.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  67. Power, M. (1997). Ecosystem engineering by organisms: why semantics matters, reply. Trends in Ecology and Evolution, 12, 275–276.

    PubMed  Article  CAS  Google Scholar 

  68. Reichman, O. J., & Seabloom, E. W. (2002). Ecosystem engineering: a trivialized concept? Response. Trends in Ecology and Evolution, 17, 308.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    PubMed  Article  Google Scholar 

  74. Singer, F. J., & Shoenecker, K. E. (2003). Do ungulates accelerate of decelerate nitrogen cycling? Forest Ecology and Management, 181, 189–204.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    PubMed  Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  83. Wilby, A. (2002). Ecosystem engineering: a trivialized concept? Trends in Ecology and Evolution, 17, 307.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

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Acknowledgments

Funding for the research in Kibale was provided by the Canada Research Chairs Program, Natural Science and Engineering Research Council of Canada, and National Geographic. M. D. Wasserman was supported by a Tomlinson Post-Doctoral Grant, J. F. Gogarten was supported by a Graduate Research Fellowship form the National Science Foundation, and T. Bonnell was supported by an FQRNT Fellowship. Thanks to Richard Wrangham for initiating the phenology monitoring with C. Chapman in 1989. Permission to conduct this research was given by the National Council for Science and Technology and the Uganda Wildlife Authority. We thank Lauren Chapman, Marco Campenni, Aerin Jacob, and Amy Zanne for helpful comments on this research.

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Chapman, C.A., Bonnell, T.R., Gogarten, J.F. et al. Are Primates Ecosystem Engineers?. Int J Primatol 34, 1–14 (2013). https://doi.org/10.1007/s10764-012-9645-9

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Keywords

  • Herbivory
  • Keystone modifier
  • Kibale National Park
  • Seed dispersal
  • Tree mortality