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.
Similar content being viewed by others
References
Anderson, J. R. (1984). Ethology and ecology of sleep in monkeys and apes. Advances in the Study of Behavior, 14, 166–229.
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.
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.
Berke, S. K. (2010). Functional groups of ecosystem engineers: a proposed classification with comments on current issues. Integrative and Comparative Biology, 50, 147–157.
Chapman, C. A. (1989a). Primate seed dispersal: the fate of dispersed seeds. Biotropica, 21, 148–154.
Chapman, C. A. (1989b). Spider monkey sleeping sites: use and availability. American Journal Of Primatology, 18, 53–60.
Chapman, C. A. (1995). Primate seed dispersal: coevolution and conservation implications. Evolutionary Anthropology, 4, 74–82.
Chapman, C. A., & Onderdonk, D. A. (1998). Forests without primates: primate/plant codependency. American Journal of Primatology, 45, 127–141.
Chapman, C. A., & Chapman, L. J. (1997). Forest regeneration in logged and unlogged forests of Kibale National Park, Uganda. Biotropica 29, 396–412.
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.
Chapman, L. J., Chapman, C. A., & Wrangham, R. W. (1992). Balanites-wilsoniana: elephant dependent dispersal. Journal of Tropical Ecology, 8, 275–283.
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.
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.
Crain, C. M., & Bertness, M. D. (2006). Ecosystem engineering across environmental gradients: implications for conservation and management. BioScience, 56, 211–218.
Creel, S., & Christianson, D. (2009). Wolf presence and increased willow consumption by Yellowstone elk: implications for trophic cascades. Ecology, 90, 2454–2466.
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.
Dittus, W. P. J. (1985). The influence of leaf-monkeys on their feeding trees in a cyclone-disturbed environment. Biotropica, 17, 100–106.
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.
Estes, J. A., & Palmisano, J. F. (1974). Sea otters: their role in structuring nearshore communities. Science, 185, 1058–1060.
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.
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.
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.
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.
Forsyth, A., & Miyata, K. (1984). Tropical nature: Life and death in the rain forest of central and south America. New York: Touchstone Books.
Fossey, D., & Harcourt, A. H. (1977). Feeding ecology of free-ranging mountain gorillas. In T. H. Clutton-Brock (Ed.), Primate ecology. London: Academic.
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.
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.
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.
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.
Herrera, C. (1985). Determinants of plant-animal coevolution: the case of mutualistic dispersal of seeds by vertebrates. Oikos, 44, 132–141.
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.
Howe, H. F., & Smallwood, J. (1982). Ecology of seed dispersal. Annual Review of Ecology and Systematics, 13, 201–228.
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.
Jin-Eong, O. (1995). The ecology of mangrove conservation and management. Hydrobiologia, 295, 343–351.
Jones, C. G., Lawton, J. H., & Shachak, M. (1994). Organisms as ecosystem engineers. Oikos, 69, 373–386.
Jones, C. G., Lawton, J. H., & Shachak, M. (1997). Ecosystem engineering by organisms: why semantics matters. Trends in Ecology and Evolution, 12, 275.
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.
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.
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.
Lambert, J. E., & Garber, P. A. (1998). Evolutionary and ecological implications of primate seed dispersal. American Journal of Primatology, 45, 9–28.
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.
Laws, R. M. (1970). Elephants as agents of habitat and landscape change in East Africa. Oikos, 21, 1–15.
Leiberman, D., Hall, J. B., Swaine, M. D., & Lieberman, M. (1979). Seed dispersal by baboons in the Shai Hills, Ghana. Ecology, 60, 65–75.
Levey, D. J., Tewksbury, J. J., & Bolker, B. M. (2008). Modelling long-distance seed dispersal in heterogeneous landscapes. Journal of Ecology, 96, 599–608.
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.
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.
McNaughton, S. J. (1976). Serengeti wildebeest: facilitation of energy flow by grazing. Science, 193, 92–94.
McNaughton, S. J. (1977). Grazing as an optimizatino process: grassland-ungulate relationships in the Serengeti. American Naturalist, 113, 691–703.
Milton, K. (1980). The foraging strategies of howler monkeys: A study in primate economics. New York: Columbia University Press.
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.
Naiman, R. J. (1988). Animal influences on ecosystem dynamics. Bioscience, 38, 750–752.
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.
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.
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.
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.
Oates, J. F. (1977). The guereza and its food. In T. H. Clutton-Brock (Ed.), Primate ecology (pp. 275–321). New York: Academic.
Oppenheimer, J. R., & Lang, G. E. (1969). Cebus monkeys: effect on branching of Gustavia trees. Science, 165, 187–188.
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.
Pastor, J., Cohen, Y., & Moen, R. (1999). Generation of spatial patterns in boreal forest landscapes. Ecosystems, 2, 439–452.
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.
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.
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.
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.
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.
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.
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.
Power, M. (1997). Ecosystem engineering by organisms: why semantics matters, reply. Trends in Ecology and Evolution, 12, 275–276.
Reichman, O. J., & Seabloom, E. W. (2002). Ecosystem engineering: a trivialized concept? Response. Trends in Ecology and Evolution, 17, 308.
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.
Ripple, W. J. B., & Beschta, R. L. (2005). Wolves and the ecology of fear: can predation risk structure ecosystems? BioScience, 54, 755–766.
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.
Schupp, E. W. (1993). Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio, 108, 15–29.
Schupp, E. W., Jordano, P., & Gomez, J. M. (2010). Seed dispersal effectiveness revisited: a conceptual review. New Phytologist, 188, 333–335.
Singer, F. J., & Shoenecker, K. E. (2003). Do ungulates accelerate of decelerate nitrogen cycling? Forest Ecology and Management, 181, 189–204.
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.
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.
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.
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.
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.
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.
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.
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.
Wilby, A. (2002). Ecosystem engineering: a trivialized concept? Trends in Ecology and Evolution, 17, 307.
Wrangham, R. W., Chapman, C. A., & Chapman, L. J. (1994). Seed dispersal by forest chimpanzees in Uganda. Journal of Tropical Ecology, 10, 355–368.
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.
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.
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.
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.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10764-012-9645-9