Seed-spitting primates and the conservation and dispersion of large-seeded trees

International Journal of Primatology

Volumn 26, Issue 3, 2005, Pages 631-649

  Dominy, Nathaniel J ^a   Duncan, Brean W ^b  

^a UNIVERSITY OF CHICAGO   (United States)

^b DYNAMAC CORPORATION   (United States)

Author keywords

Cercopithecinae; Frugivory; Scatter clump hypothesis; Seed dispersal

Indexed keywords

CONSERVATION; SEED DISPERSAL;

BALANITES; BALANITES WILSONIANA; CERCOPITHECINAE; CERCOPITHECUS; CHRYSOPHYLLUM GORUNGOSANUM; ELEPHANTIDAE; PAN (APE); PAN TROGLODYTES; PRIMATES; UVARIOPSIS CONGENSIS;

EID: 20744436869     PISSN: 01640291     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10764-005-4370-2     Document Type: Conference Paper

References (102)

1. Alexandre, D.-Y. (1978). Le role disseminateur des elephants en foret de Taï, Cote-d'Ivoire. Rev. Ecol. (Terre Vie) 32: 47-72.
2. Andresen, E. (1999). Seed dispersal by monkeys and the fate of dispersed seeds in a Peruvian rain forest. Biotropica 31: 145-158.
3. Andresen, E. (2001). Effects of dung presence, dung amount and secondary dispersal by dung beetles on the fate of Micropholis guyanensis (Sapotaceae) seeds in Central Amazonia. J. Trop. Ecol. 17: 61-78.
4. Andresen, E. (2002). Primary seed dispersal by red howler monkeys and the effect of defecation patterns on the fate of dispersed seeds. Biotropica 34: 261-272.
5. Andrews, P., and Aiello, L. (1984). An evolutionary model for feeding and positional behaviour. In Chivers, D. J., Wood, B. A., and Bilsborough, A. (eds.), Food Acquisition and Processing in Primates. Plenum Press, New York, pp. 429-466.
6. Balasubramanian, P., and Bole, P. V. (1993). Seed dispersal by mammals at Point Calimere Wildlife Sanctuary, Tamil Nadu. J. Bombay Nat. Hist. Soc. 90: 33-44.
7. Beck, H., and Terbrogh, J. (2002). Groves versus isolates: How spatial aggregation of Astrocaryum murumuru palms affects seed removal. J. Trop. Ecol. 18: 275-288.
8. Bodmer, R. E. (1990). Fruit patch size and frugivory in the lowland tapir (Tapirus terrestris). J. Zool. 222: 121-128.
9. Chapman, C. A. (1995). Primate seed dispersal: Coevolution and conservation implications. Evol. Anthropol. 4: 74-82.
10. Chapman, C. A., and Chapman, L. J. (1995). Survival without dispersers: Seedling recruitment under parents. Conserv. Biol. 9: 675-678.
11. Chapman, C. A., and Chapman, L. J. (1996). Frugivory and fate of dispersed and non-dispersed seeds in six African tree species. J. Trop. Ecol. 12: 491-504.
12. Chapman, C. A., and Onderdonk, D. A. (1998). Forests without primates: Primate/plant codependency. Am. J. Primatol. 45: 127-141.
13. Chapman, C. A., Wrangham, R. W., Chapman, L. J., Kennard, D. K., and Zanne, A. E. (1999). Fruit and flower phenology at two sites in Kibale National Park, Uganda. J. Trop. Ecol. 15: 189-211.
14. Chapman, L. J., Chapman, C. A., and Wrangham, R. W. (1992). Balanites wilsoniana: Elephant dependent dispersal? J. Trop. Ecol. 8: 275-283.
15. Cochrane, E. P. (2001). Elephants as Seed Dispersal Agents for Tropical Forest Tree Species in Kibale National Park, Uganda. Ph.D. Dissertation, University of Wisconsin, Madison.
16. Cordeiro, N. J., and Howe, H. F. (2003). Forest fragmentation severs mutualism between seed dispersers and an endemic African tree. Proc. Natl. Acad. Sci. USA 100: 14052-14056.
17. Corlett, R. T. (2002). Frugivory and seed dispersal in degraded tropical East Asian landscapes. In Levey, D. J., Silva, W. R., and Galetti, M. (eds.), Seed Dispersal and Frugivory: Ecology, Evolution and Conservation. CAB International, Wallingford, UK, pp. 451-465.
18. Corlett, R. T., and Lucas, P.W. (1990). Alternative seed-handling strategies in primates: Seed spitting by long-tailed macaques (Macaca fascicularis). Oecologia 82: 166-171.
19. Dinerstein, E, and Wemmer, C. M. (1988). Fruits Rhinoceros eat: Dispersal of Trewia nudiflora (Euphorbiaceae) in lowland Nepal. Ecology 69: 1768-1774.
20. Disotell, T. R., and Raaum R. L. (2002). Molecular timescale and gene tree incongruence in the guenons. In Glenn, M. E., and Cords, M. (eds.). The Guenons: Diversity and Adaptation in African Monkeys, Kluwer Academic / Plenum, New York, pp. 27-36.
21. Dominy, N. J., and Duncan, B.W. (2001). GPS and GIS methods in an African rain forest: Applications to tropical ecology and conservation. Consev. Ecol. 5: 537-549 [online] URL: http://www.consecol.org/vol5/iss2/art6
22. Eriksson, O., Friis, E. M., and Löfgren P. (2000). Seed size, fruit size, and dispersal systems in angiosperms from the early Cretaceous to the late Tertiary. Am. Nat. 156: 47-58.
23. Feer, F. (1995). Seed dispersal in African forest ruminants. J. Trop. Ecol. 11: 683-689.
24. Foster, S. A. (1986). On the adaptive value of large seeds for tropical moist forest trees: A review and synthesis. Bot. Rev. 52: 260-299.
25. Fragoso, J. M. V. (1997). Tapir-generated seed shadows: Scale-dependent patchiness in the Amazon rain forest. J. Ecol. 85: 519-529.
26. Fragoso, J. M. V., Silvius, K. M., and Correa, J. A. (2003). Long-distance dispersal by tapir increases seed survival and aggregates tropical trees. Ecology 84: 1998-2006.
27. Furuichi, T., and Hashimoto, C. (2004). Botanical and topographical factors influencing nesting-site selection by chimpanzees in Kalinzu Forest, Uganda. Int. J. Primatol. 25: 755-765.
28. Garber, P. A. (1986). The ecology of seed dispersal in two species of callitrichid primates (Saguinus mystax and Saguinus fuscicollis). Am. J. Primatol. 10: 155-170.
29. Gautier, J.-P. (1985). Quelques caracteristiques ecologiques du singe des marais: Allenopithecus nigroviridis Lang 1923. Rev. Ecol. (Terre Vie) 40: 331-342.
30. Gautier-Hion, A. (1984). La dissemination des graines par les cercopithecides forestiers Africains. Rev. Ecol. (Terre Vie) 39: 159-165.
31. Gautier-Hion, A., Colyn, M., and Gautier, J.-P. (1999). Histoire Naturelle Des Primates D'Afrique Centrale, ECOFAC, Libreville.
32. Ghiglieri, M. P., Butynski, T. M., Struhsaker, T. T., and Leland, L. (1982). Bush pig (Potamochoerus porcus) polychromatism and ecology in Kibale Forest, Uganda. Afr. J. Ecol. 20: 231-236.
33. Gundling, T., and Hill, A. (2000). Geological context of fossil Cercopithecoidea from eastern Africa. In Whitehead, P. F., and Jolly, C. J. (eds.), Old World Monkeys, Cambridge University Press, Cambridge, UK, pp. 180-213.
34. Hamilton, A. (1991). A Field Guide to Uganda Forest Trees, 2nd edn., Makerere University Printery, Kampala.
35. Harms, K. E., Wright, S. J., Calderón, O., Hernández, A., and Herre, E. A. (2000). Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 404: 493-495.
36. Hawthorne, W. D., and Parren, M. P. E. (2000). How important are forest elephants to the survival of woody plant species in Upper Guinean forests? J. Trop. Ecol. 16: 133-150.
37. Herrera, C. M. (1985). Determinants of plant-animal coevolution: The case of mutualistic dispersal of seeds by vertebrates. Oikos 44: 132-141.
38. Herrera, C. M., Jordano, P., López-Soria, and Amat, J. A. (1994). Recruitment of a mast-fruiting, bird-dispersed tree: Bridging frugivore activity and seedling establishment. Ecol. Monogr. 64: 315-344.
39. Homewood, K. M. (1978). Feeding strategy of the Tana mangabey (Cercocebus galeritus galeritus) (Mammalia: Primates). J. Zool. 186: 375-391.
40. Howe, H. F. (1985). Gompothere fruits: A critique. Am. Nat. 125: 853-865.
41. Howe, H. F. (1989). Scatter- and clump-dispersal and seedling demography: Hypothesis and implications. Oecologia 79: 417-426.
42. Howe, H. F., and Miriti, M. N. (2004). When seed dispersal matters. BioScience 54: 651-660.
43. Jackson, G., and Gartlan, J. S. (1965). The flora and fauna of Lolui Island, Lake Victoria: A study of vegetation, men and monkeys. J. Ecol. 53: 573-597.
44. Jansen, P. A., and Forget, P.-M. (2001). Scatterhoarding rodents and tree regeneration. In Bongers, F., Charles-Dominique, P., Forget, P.-M., and Théry, M. (eds.), Nouragues: Dynamics and Plant-Animal Interactions in a Neotropical Rainforest, Kluwer Academic, Dordrecht, pp. 275-288.
45. Janson, C. H., Stiles, E. W., and White, D. W. (1986). Selection on plant fruiting traits by brown capuchin monkeys: A multivariate approach. In Estrada, A., and Fleming, T. H. (eds.), Frugivores and Seed Dispersal, Dr. W Junk Publishers, Dordrecht, pp. 83-92.
46. Janzen, D. H. (1983). Seed and pollen dispersal by animals: Convergence in the ecology of contamination and sloppy harvest. Biol. J. Linn. Soc. 20: 103-113.
47. Jordano, P., and Herrera, C. M. (1995). Shuffling the offspring: Uncoupling and spatial discordance of multiple stages in vertebrate seed dispersal. Ecoscience 2: 230-237.
48. Julliot, C. (1997). Impact of seed dispersal by red howler monkeys Alouatta seniculus on the seedling population in the understorey of tropical rain forest. J. Ecol. 85: 431-440.
49. Kaplin, B. A., and Lambert, J. E. (2002). Effectiveness of seed dispersal by Cercopithecus monkeys: Implications for seed input into degraded areas. In Levey, D. J., Silva, W. R., and Galetti, M. (eds.), Seed Dispersal and Frugivory: Ecology, Evolution and Conservation, CAB International, Wallingford, UK, pp. 351-364.
50. Kaplin, B. A., and Moermond, T. C. (1998). Variation in seed handling by two species of forest monkeys in Rwanda. Am. J. Primatol. 45: 83-101.
51. Kitamura, S., Yumoto, T., Poonswad, P., Chuailua, P., Plongmai, K., Maruhashi, T., and Noma, N. (2002). Interactions between fleshy fruits and frugivores in tropical seasonal forest in Thailand. Oecologia 133: 559-572.
52. Krebs, C. J. (1999). Ecological Methodology, Second Edition, Benjamin/Cummings, Menlo Park.
53. 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. Am. J. Phys. Anthropol. 109: 365-386.
54. Lambert, J. E. (2001). Red-tailed guenons (Cercopithecus ascanius) and Strychnos mitis: Evidence for plant benefits beyond seed dispersal. Int. J. Primatol. 22: 189-201.
55. Lambert, J. E. (2002). Exploring the link between animal frugivory and plant strategies: The case of primate fruit processing and post-dispersal fate. In Levey, D. J., Silva, W. R., and Galetti, M. (eds.), Seed Dispersal and Frugivory: Ecology, Evolution and Conservation, CAB International, Wallingford, UK, pp. 365-379.
56. Leakey, M. (1988). Fossil evidence for the evolution of the guenons. In Gautier-Hion, A., Bourlière, F., Gautier, J.-P., and Kingdon, J. (eds.), A Primate Radiation: Evolutionary Biology of the African Guenons, Cambridge University Press, Cambridge, UK, pp. 7-12.
57. Lewis, D. M. (1987). Fruiting patterns, seed germination, and distribution of Sclerocarya caffra in an elephant-inhabited woodland. Biotropica 19: 50-56.
58. Lieberman, D., Hall, J. B., Swaine, M. D., and Lieberman, M. (1979). Seed dispersal by baboons in the Shai Hills, Ghana. Ecology 60: 65-75.
59. Lieberman, D., Lieberman, M., and Martin, C. (1987). Notes on seeds in elephant dung from Bia National Park, Ghana. Biotropica 19: 365-369.
60. Lord, J., Egan, J., Clifford, T., Jurado, E., Leishman, M., Williams, D., and Westoby M (1997). Larger seeds in tropical floras: Consistent patterns independent of growth form and dispersal mode. J. Biogeogr. 24: 205-211.
61. Lucas, P. W., Beta, T., Darvell, B. W., Dominy, N. J., Essackjee, H. C., Lee, P. K. D., Osorio, D., Yamashita, N., and Yuen, T. D. B. (2001). Field kit to characterize physical, chemical, and spatial aspects of potential primate foods. Folia Primatol. 72: 11-25.
62. Lucas, P. W., and Corlett, R. T. (1992). Notes on the treatment of palm fruits by long-tailed macaques (Macaca fascicularis Raffles). Principes 36: 45-48
63. Lucas, P. W., and Corlett, R. T. (1998). Seed dispersal by long-tailed macaques. Am. J. Primatol. 45: 29-44.
64. Lwanga, J. S. (2003). Forest succession in Kibale National Park, Uganda: Implications for forest restoration and management. Afr. J. Ecol. 41: 9-22.
65. Mason, A., and Rubens, J. (1992). Kibale Forest tourist project. Swara 15: 31-33.
66. Muller-Landau, H. C., Wright, S. J., Calderon, O., Hubbell, S. P., and Foster, R. B. (2002). Assessing recruitment limitation: Concepts, methods and case-studies from a tropical forest. In Levey, D. J., Silva, W. R., and Galetti, M. (eds.), Seed Dispersal and Frugivory: Ecology, Evolution and Conservation, CAB International, Wallingford, UK, pp. 35-53.
67. Murray, P. (1975). The role of cheek pouches in cercopithecine monkey adaptive strategy. In Tuttle, R. H. (ed.). Primate Functional Morphology and Evolution, Mouton, The Hague, pp. 151-194.
68. Myers, J. H. (1978). Selecting a measure of dispersion. Environ. Entomol. 7: 619-621.
69. Nathan, R., and Muller-Landau, H. C. (2000). Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol. Evol. 15: 278-285.
70. Otani, T., and Shibata, E. (2000). Seed dispersal and predation by Yakushima macaques, Macaca fuscata yakui, in a warm temperate forest of Yakushima Island, southern Japan. Ecol. Res. 15: 133-144.
71. Plotkin, J. B., Chave, J., and Ashton, P. S. (2002). Cluster analysis of spatial patterns in Malaysian tree species. Am. Nat. 160: 629-644.
72. Ridley, H. N. (1930). The Dispersal of Plants Around the World. Reeve, Kent.
73. Rogers, M. E., Voysey, B. C., McDonald, K. E., Parnell, R. J., and Tutin, C. E. G. (1998). Lowland gorillas and seed dispersal: The importance of nest sites. Am. J. Primatol. 45: 45-68.
74. Rowell, T. E., and Mitchell, B. J. (1991). Comparison of seed dispersal by guenons in Kenya and capuchins in Panama. J. Trop. Ecol. 7: 269-274.
75. Schupp, E. W. (1988). Factors affecting post-dispersal seed survival in a tropical forest. Oecologia 76: 525-530.
76. Schupp, E. W. (1990). Annual variation in seedfall, postdispersal predation, and recruitment of a tropical tree. Ecology 71: 504-515.
77. Schupp, E. W. (1993). Quantity, quality, and the effectiveness of seed dispersal by mammals. In Fleming, T. H., and Estrada, A. (eds.), Frugivory and Seed Dispersal: Ecological and Evolutionary aspects. Kluwer, Boston, pp. 15-30.
78. Schupp, E. W. (1995). Seed-seedling conflicts, habitat choice, and patterns of plant recruitment. Am. J. Bot. 82: 399-409.
79. Schupp, E. W., Milleron, T., and Russo, S. E. (2002). Dissemination limitation and the origin and maintenance of species-rich tropical forests. In Levey, D. J., Silva, W. R., and Galetti, M. (eds.), Seed Dispersal and Frugivory: Ecology, Evolution and Conservation, CAB International, Wallingford, UK, pp. 19-33.
80. Shepherd, V. E., and Chapman, C. A. (1998). Dung beetles as secondary seed dispersers: Impact on seed predation and germination. J. Trop. Ecol. 14: 199-215.
81. Stanford, C. B., and Nkurunungi, J. B. (2003). Behavioral ecology of sympatric chimpanzees and gorillas in Bwindi Impenetrable National Park, Uganda: Diet. Int. J. Primatol. 24: 901-918.
82. Struhsaker, T. T. (1997). Ecology of an African rainforest: Logging in Kibale and the conflict between conservation and exploitation. University of Florida Press, Gainesville.
83. Sussman, R. W. (1995). How primates invented the rainforest and vice versa. In Alterman, L., Doyle, G. A., and Izard, M. K. (eds.), Creatures of the Dark: The Nocturnal Prosimians. Plenum Press, New York, pp. 1-10.
84. Sussman, R. W., and Raven, P. H. (1978). Pollination by lemurs and marsupials: An archaic coevolutionary system. Science 200: 731-736.
85. Szalay, F. S., and Delson, E. (1979). Evolutionary History of the Primates. Academic Press, New York.
86. Tiffney, B. H. (1984). Seed size, dispersal syndromes, and the rise of the angiosperms: Evidence and hypothesis. Ann. Missouri Bot. Gard. 71: 551-576.
87. Tosi, A. J., Melnick, D. J., and Disotell, T. R. (2004). Sex chromosome phylogenetics indicate a single transition to terrestriality in the guenons (tribe Cercopithecini). J. Hum. Evol. 46: 223-237.
88. Traveset, A., and Verdú, M. (2002). A meta-analysis of the effect of gut treatment on seed germination. In Levey, D. J., Silva, W. R., and Galetti, M. (eds.). Seed Dispersal and Frugivory: Ecology, Evolution and Conservation, CAB International, Wallingford, UK, pp. 339-350.
89. Tutin, C. E. G., Williamson, E. A., Rogers, M. E., and Fernandez, M. (1991). A case study of a plant-animal relationship: Cola lizae and lowland gorillas in the Lopé Reserve, Gabon. J. Trop. Ecol. 7: 181-199.
90. Upton, G. J. G., and Fingleton, B. (1985). Spatial Data Analysis by Example, Volume 1: Point Pattern and Quantitative Data. Wiley, New York.
91. Voysey, B. C., McDonald, K. E., Rogers, M. E., Tutin, C. E. G., and Parnell, R. J. (1999). Gorillas and seed dispersal in the Lopé Reserve, Gabon. II: Survival and growth of seedlings. J. Trop. Ecol. 15: 39-60.
92. Walsh, P. D., Abernethy, K. A., Bermejo, M., Beyers, R., De Wachter, P., Akou, M. E., Huijbregts, B., Mambounga, D. I., Toham, A. K., Kilbourn, A. M., Lahm, S. A., Latour, S., Maisels, F., Mbina, C., Mihindou, Y., Obiang, S. N., Effa, E. N., Starkey, M. P., Telfer, P., Thibault, M., Tutin, C. E. G., White, L. J. T., and Wilkie, D. S. (2003). Catastrophic ape decline in western equatorial Africa. Nature 422: 611-614.
93. Wang, B. C., and Smith, T. B. (2002). Closing the seed dispersal loop. Trends Ecol. Evol. 17: 379-385.
94. Wehncke, E. V., Hubbell, S. P., Foster, R. B., and Dalling, J. W. (2003). Seed dispersal patterns produced by white-faced monkeys: Implications for the dispersal limitation of neotropical tree species. J. Ecol. 91: 677-685.
95. Wenny, D. G., and Levey, D. J. (1998). Directed seed dispersal by bellbirds in a tropical cloud forest. Proc. Natl. Acad. Sci. USA 95: 6204-6207.
96. Whitten, A. J. (1982). Diet and feeding behaviour of Kloss gibbons on Siberut Island, Indonesia. Folia Primatol. 37: 177-208.
97. Wing, L. D., and Buss, I. O. (1970). Elephants and forests. Wildlife Monogr. 19: 3-92.
98. Wrangham, R. W., Chapman, C. A., and Chapman, L. J. (1994). Seed dispersal by forest chimpanzees. J. Trop. Ecol. 10: 355-368.
99. Wrangham, R. W., Chapman, C. A., Clark-Arcadi, A. P., and Isabirye-Basuta, G. (1996). Social ecology of Kanyawara chimpanzees: Implications for the costs of great ape groups. In McGrew, W. C., Marchant, L. F., and Nishida, T. (eds.), The Great Ape Societies, Cambridge University Press, Cambridge, pp. 45-57.
100. Wrangham, R. W., Conklin-Brittain, N. L., and Hunt, K. D. (1998). Dietary response of chimpanzees and cercopithecines to seasonal variation in fruit abundance: I. Antifeedants. Int. J. Primatol. 19: 949-970.
101. Yasuda, M., Miura, S., and Hussein, N. A. (2000). Evidence for food hoarding behaviour in terrestrial rodents in Pasoh Forest Reserve, a Malaysian lowland rain forest. J. Trop. For. Sci. 12: 164-173.
102. Zhang, S.-Y., and Wang, L.-X. (1995). Fruit consumption and seed dispersal of Ziziphus cinnamomum (Rhamnaceae) by two sympatric primates (Cebus apella and Ateles paniscus) in French Guiana. Biotropica 27: 397-401.