Differential seed handling by two African primates affects seed fate and establishment of large-seeded trees

Acta Oecologica

Volumn 37, Issue 6, 2011, Pages 578-586

  Gross Camp, Nicole D ^a,b   Kaplin, Beth A ^b  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b ANTIOCH UNIVERSITY NEW ENGLAND   (United States)

Author keywords

Cercopithecus lhoesti; Microhabitat; Pan troglodytes; Rwanda; Syzygium; Wadge

Indexed keywords

DISPERSAL; EXPERIMENTAL STUDY; FOREST ECOSYSTEM; GERMINATION; MICROHABITAT; NUMERICAL MODEL; OBSERVATIONAL METHOD; PRIMATE; SEED DISPERSAL; SEEDLING ESTABLISHMENT; TERRESTRIAL ENVIRONMENT;

AFRICA;

CERCOPITHECUS; CERCOPITHECUS LHOESTI; HAPLORHINI; PAN; PAN TROGLODYTES; PRIMATES; SYZYGIUM;

EID: 80955166133     PISSN: 1146609X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.actao.2011.04.003     Document Type: Article

References (86)

1. Andresen E., Feer F. The role of dung beetles as secondary dispersers and their effect on plant regeneration in tropical rainforests. Seed Fate 2005, 331-350. CABI Publishing, Cambridge, MA. P.M. Forget, J. Lambert, P.E. Hulme, S.B. Vander Wall (Eds.).
2. Andresen E., Levey D.J. Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees. Oecologia 2004, 139:45-54.
3. Balcomb S.R., Chapman C.A. Bridging the gap: influence of seed deposition on seedling recruitment in a primate-tree interaction. Ecological Monographs 2003, 73:625-642.
4. Benitez-Malvido J. Effect of low vegetation on the recruitment of plants in successional habitat types. Biotropica 2006, 38:171-182.
5. Brodie J.F., Helmy O.E., Brockelman W.Y., Maron J.L. Bushmeat poaching reduces the seed dispersal and population growth rate of a mammal-dispersed tree. Ecological Applications 2009, 19:854-863.
6. Chapman C.A., Chapman L.J. Frugivory and the fate of dispersed and non-dispersed seeds of six African tree species. Journal of Tropical Ecology 1996, 12:491-504.
7. Clark C., Poulsen J.R., Conner E.F., Parker V.T. Fruiting trees as dispersal foci in a semi-deciduous tropical forest. Oecologia 2004, 139:66-75.
8. Connell J.H. On the Role of Natural Enemies in Preventing Competitive Exclusion in Some Marine Animals and in Rain Forest Trees. Dynamics of Populations: Proceedings of the Advanced Study Institute on Dynamics of Numbers in Populations 1971, Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands.
9. Corlett R.T., Lucas P.W. Alternative seed-handling strategies in primates: seed-spitting by long-tailed macaques (Macaca fascicularis). Oecologia 1990, 82:166-171.
10. Cramer J.M., Mesquita R.C.G., Williamson G.B. Forest fragmentation differentially affects seed dispersal of large and small-seeded tropical trees. Biological Conservation 2007, 137:415-423.
11. Duncan R.S., Chapman C.A. Seed dispersal and potential forest succession in abandoned agriculture in tropical Africa. Ecological Applications 1999, 9:998-1008.
12. Eisenberg J.F., Thorington R.W. A preliminary analysis of a neotropical mammal fauna. Biotropica 1973, 5:150-161.
13. Forget P.-M. Effect of microhabitat on seed fate and seedling performance in two rodent-dispersed tree species in rain forest in french Guiana. Journal of Ecology 1997, 85:693-703.
14. Forget P.-M., Milleron T., Feer F. Patterns in post-dispersal seed removal by neotropical rodents and seed fate in relation to seed size. Dynamics of Tropical Communities 1998, 25-49. Blackwell Science, Oxford, UK, Symposium No. 37 of the British Ecological Society. D.M. Newberry, H.H.T. Prins, N.D. Brown (Eds.).
15. Frankie G.W., Baker H.G., Opler P.A. Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. Journal of Ecology 1974, 62:881-919.
16. Gautier-Hion A. Seasonal variations of diets related to species and sex in a community of Cercopithecus monkeys. Journal of Animal Ecology 1980, 49:237-269.
17. Gautier-Hion A., Duplantier J.-M., Quris R., Feer F., Sourd C., Decoux J.-P., Dubost G., Emmons L., Erard C., Hecketsweiler P., Roussilhon C., Thiollay J.-M. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 1985, 65:324-337.
18. Goodall J. The Chimpanzees of Gombe 1986, Belknap Press, Cambridge.
19. Gross-Camp N., Kaplin B.A. Chimpanzee (Pan troglodytes) seed dispersal in an afromontane forest: microhabitat influences on the post-dispersal fate of large seeds. Biotropica 2005, 37:641-649.
20. Gross-Camp N.D., Masozera M., Kaplin B.A. Chimpanzee seed dispersal quantity in a tropical montane forest of Rwanda. American Journal of Primatology 2009, 71:901-911.
21. Gross-Camp N.D., Mulindahabi F., Kaplin B.A. Comparing the dispersal of large-seeded tree species by frugivore assemblages in tropical montane forest in Africa. Biotropica 2009, 41:442-451.
22. Hair J.F., Anderson R.E., Tatham R.L. Multivariate Data Analysis 1987, Macmillan, New York. second ed.
23. Harms K.E., Powers J.S., Montgomery R.A. Variation in small sapling density, understory cover, and resource availability in four Neotropical forests. Biotropica 2004, 38:40-51.
24. Harms K.E., Wright S.J., Calderon O., Hernandez A., Herre E.A. Pervasive density-dependent recruitment enhances seedling diversity in a tropical forest. Nature 2000, 404:493-495.
25. Herrera C.M., Jordano P., Lopez-Soria L., Amat J.A. Recruitment of a mast-fruiting, bird-dispersed tree: bridging frugivore activity and seedling establishment. Ecological Monographs 1994, 64:315-344.
26. Herrera J.M., Garcia D. The role of remnant trees in seed dispersal through the matrix: being alone is not always so sad. Biological Conservation 2009, 142:149-158.
27. Hines D.A., Eckman K. Indigenous Multipurpose Trees of Tanzania: Uses and Economic Benefits for People 1993, Cultural Survival Canada and Development Services Foundation of Tanzania, Ottawa, Ontario, Canada.
28. Holl K.D. Do bird perching structures elevate seed rain and seedling establishment in abandoned tropical pasture?. Restoration Ecology 1998, 6:253-261.
29. Holl K.D. Factors limiting tropical rain forest regeneration in abandoned pasture: seed rain, seed germination, microclimate, and soil. Biotropica 1999, 31:229-242.
30. Howe H.F. Gomphothere fruits: a critique. The American Naturalist 1985, 125:853-865.
31. Howe H.F. Seed dispersal by fruit-eating birds and mammals. Seed Dispersal 1986, 123-189. Academic Press, New York. D.R. Murray (Ed.).
32. Howe H.F., Miriti M.N. No question: seed dispersal matters. Trends in Ecology & Evolution 2000, 15:434-436.
33. Howe H.F., Smallwood J. Ecology of seed dispersal. Annual Review of Ecology and Systematics 1982, 13:201-228.
34. Hubbell S.P. The Unified Neutral Theory of Biodiversity and Biogeography 2001, Princeton University Press, Princeton, New Jersey.
35. Hulme P.E. Post-dispersal seed predation by small mammals. Symposium of the Zoological Society of London 1993, 65:269-287.
36. Hyatt L.A., Rosenberg M.S., Howard T.G., Bole G., Fang W., Anastasia J., Brown K., Grella R., Hinman K., Kurdziel J.P., Gurevich J. The distance dependence prediction of the Janzen-Connell hypothesis: a meta-analysis. Oikos 2003, 103:590-602.
37. Janson C.H. Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science 1983, 219:187-189.
38. Janzen D.H. Herbivores and the number of tree species in tropical forests. American Naturalist 1970, 104:501-528.
39. Janzen D.H., Ataroff M., Farinas M., Reyes S., Rincon N., Soler A., Soriano P., Vera M. Changes in the arthropod community along an elevational transect in the Venezualen Andes. Biotropica 1976, 8:193-203.
40. Jordano P., Godoy J.A. Frugivore-generated seed shadows: a landscape view of demographic and genetic effects. Seed Dispersal and Frugivory: Ecology, Evolution and Conservation 2002, CABI Publishing, Oxon, UK. D.J. Levey, W.R. Silva, M. Galetti (Eds.).
41. Jordano P., Schupp E.W. Determinants of seed dispersal effectiveness: the quantity component in the Prunus mahaleb - frugivorous bird interaction. Ecological Monographs 2000, 70:591-615.
42. Julliot C. Seed dispersal by red howling monkeys (Alouatta seniculus) in the tropical rain forest of French Guiana. International Journal of Primatology 1996, 17:239-258.
43. Kankam B.O., Oduro W. Frugivores and fruit removal of Antiaris toxicaria (Moraceae) at Bia Biosphere Reserve, Ghana. Journal of Tropical Ecology 2009, 25:201-204.
44. Kaplin B.A., Lambert J.E. Effectiveness of seed dispersal by Cercopithecus monkeys: implications for seed input into degraded areas. Seed Dispersal and Frugivory 2002, 351-364. CABI Publishing, Oxon, UK. D.J. Levey, W.R. Silva, M. Galetti (Eds.).
45. Kaplin B.A., Moermond T.C. Variation in seed handling by two species of forest monkeys in Rwanda. American Journal of Primatology 1998, 45:83-101.
46. Kaplin B.A., Moermond T.C. Foraging ecology of the mountain monkey (Cercopithecus lhoesti): implications for its evolutionary history and use of disturbed forest. American Journal of Primatology 2000, 50:227-246.
47. Kiltie R.A. Distribution of palm fruits on a rainforest floor: why white-lipped peccaries forage near objects?. Biotropica 1981, 13:141-145.
48. Kitchings J.T., Levey D.J. Habitat patterns in a small mammal community. Journal of Mammology 1981, 62:814-820.
49. Lambert J.E. Red-tailed guenons (Cercopithecus ascanius) and Strychnos mitis: evidence for plant benefits beyond seed dispersal. International Journal of Primatology 2001, 22:189-201.
50. Lambert J.E. Exploring the link between animal frugivory and plant strategies: the case of primate fruit processing and post-dispersal seed fate. Seed Dispersal and Frugivory: Ecology, Evolution, and Conservation 2002, 365-379. CABI Publishing, Wallingford, Oxfordshire, UK. D.J. Levey, W.R. Silva, M. Galetti (Eds.).
51. Lambert J.E. Primate seed dispersers as umbrella species: a case study from Kibale National Park, Uganda, with implications for Afrotropical forest conservation. American Journal of Primatology 2011, 73:9-24.
52. Lambert J.E., Chapman C. The fate of primate-dispersed seeds: deposition patterns, dispersal distance and implications for conservation. Seed Fate 2005, 137-150. CABI Publishing, Cambridge, MA. P.M. Forget, J. Lambert, P.E. Hulme, S.B. Vander Wall (Eds.).
53. Lambert J.E., Garber P.A. Evolutionary and ecological implications of primate seed dispersal. American Journal of Primatology 1998, 45:9-28.
54. Lemmon P.E. A new instrument for measuring forest overstory density. Journal of Forestry 1957, 55:667-668.
55. Levine J.M., Murrell D.J. The community-level consequences of seed dispersal patterns. Annual Review of Ecology, Evolution and Systematics 2003, 34:549-574.
56. McClanahan T.R., Wolfe R.W. Accelerating forest succession in a fragmented landscape: the role of birds and perches. Conservation Biology 1993, 7:279-288.
57. Newton-Fisher N.E. The home range of the Sonso community of chimpanzees from the Budongo Forest, Uganda. African Journal of Ecology 2003, 41:151-156.
58. Nunez-Iturri G., Howe H.F. Bushmeat and the fate of trees with seeds dispersed by large primates in a lowland rain forest in Western Amazonia. Biotropica 2007, 39:348-354.
59. Nunez-Iturri G., Olsson O., Howe H.F. Hunting reduces recruitment on primate-dispersed trees in Amazonian Peru. Biological Conservation 2008, 141:1536-1546.
60. Peres C., Van Roosmalen M. Primate frugivory in two species-rich Neotropical forests: implications for the demography of large-seeded plants in overhunted areas. Seed Dispersal and Frugivory 2002, 407-421. CABI Publishing, Wallingford, Oxfordshire, UK. D.J. Levey, W.R. Silva, M. Galetti (Eds.).
61. Peres C.A., Palacios E. Basin-wide effects of game harvest on vertebrate population densitites in Amazonian forests: implications for animal-mediated seed dispersal. Biotropica 2007, 39:304-315.
62. Plumptre A.J., Masozera M., Fashing P.J., McNeilage A., Ewango C., Kaplin B.A., Liengola I. Biodiversity Surveys of the Nyungwe Forest of Southwest Rwanda: Final Report 2002, Wildlife Conservation Society, Bronx, NY.
63. Poulsen J.R., Clark C.J., Connor E.F., Smith T.B. Differential resource use by primates and hornbills: implications for seed dispersal. Ecology 2002, 83:228-240.
64. Quinn G.P., Keough M.J. Experimental Design and Data Analysis for Biologists 2002, Cambridge University Press, Cambridge, U.K.
65. Rey P.J., Alcantra J.M. Recruitment dynamics of a fleshy-fruited plant (Olea europaea): connecting patterns of seed dispersal to seedling establishment. Journal of Ecology 2000, 88:622-633.
66. Rogers M.E., Maisels F., Williamson E.A., Fernandez M., Tutin C.E.G. Gorilla diet in the Lope Reserve, Gabon: a nutritional analysis. Oecologia 1990, 84:326-339.
67. Rowell T.E., Mitchell B.J. Comparison of seed dispersal by guenons in Kenya and capuchins in Panama. Journal of Tropical Ecology 1991, 7:269-274.
68. Russo S.E. Linking seed fate to natural dispersal patterns: factors affecting predation and scatter-hoarding of Virola calophylla seeds in Peru. Journal of Tropical Ecology 2005, 21:243-253.
69. Russo S.E., Portnoy S., Augspurger C.K. Incorporating animal behavior into seed dispersal models: implications for seed shadows. Ecology 2006, 87:3160-3174.
70. Schupp E.W. Factors affecting post-dispersal seed survival in a tropical forest. Oecologia 1988.
71. Schupp E.W. Seed and early seedling predation in the forest understory and in treefall gaps. Oikos 1988, 51:71-78.
72. Schupp E.W. Quantity, quality, and the effectiveness of seed dispersal by animals. Plant Ecology 1993, 107-108:15-29.
73. Schupp E.W., Howe H.F., Augspurger C.K., Levey D.J. Arrival and survival in tropical treefall gaps. Ecology 1989, 70:562-564.
74. Stevenson P.R. Seed dispersal by woolly monkeys (Lagothrix lagothricha) at Tinigua National Park, Columbia: dispersal distance, germination rates, and dispersal quantity. American Journal of Primatology 2000, 50:275-289.
75. Stiles E.W., White D.W. Seed deposition patterns: influence of season, nutrients, and vegetation structure. Frugivores and Seed Dispersal 1986, Junk Publishers, Dordrecht, Dr. W. A. Estrada, T.H. Fleming (Eds.).
76. Stoner K.E., Riba-Hernandez P., Vulinec K., Lambert J.E. The role of mammals in creating and modifying seedshadows in tropical forests and some possible consequences of their elimination. Biotropica 2007, 39:316-327.
77. Sun C., Kaplin B.A., Kristensen K.A., Munyaligoga V., Mvukiyumwami J., Kajonda K., Moermond T.C. Tree phenology in a tropical montane forest of Rwanda. Biotropica 1996, 28:668-681.
78. Terborgh J. Community aspects of frugivory in tropical forests. Frugivores and Seed Dispersal 1986, 371-384. Dr. W. Junk, Dordrecht. A. Estrada, T.H. Fleming (Eds.).
79. Vanthomme H., Belle B., Forget P.M. Bushmeat hunting alters recruitment of large-seeded plant species in Central Africa. Biotropica 2010, 42:672-679.
80. Wang B.C., Smith T.B. Closing the seed dispersal loop. Trends in Ecology & Evolution 2002, 17:379-385.
81. Wang B.C., Sork V.L., Leong M.T., Smith T.B. Hunting of mammals reduces seed removal and dispersal of the Afrotropical tree, Antocaryon klaineanum (Anacardiaceae). Biotropica 2007, 39:340-347.
82. Wenny D.G. Seed dispersal, seed predation, and seedling recruitment of a neotropical montane tree. Ecological Monographs 2000, 70:331-351.
83. Wheelwright N.T. Fruit size, gape width, and the diets of fruit-eating birds. Ecology 1985, 66:808-818.
84. Wrangham R.W., Chapman C., Chapman L.J. Seed dispersal by forest chimpanzees in Uganda. Journal of Tropical Ecology 1994, 10:355-368.
85. Wright S.J., Stoner K.E., Beckman N.B., Cortlett R.T., Dirzo R., Muller-Landau H.C., Nunez-Iturri G., Peres C.A., Wang B.C. The plight of large animals in tropical forests and the consequences for plant regeneration. Biotropica 2007, 39:289-291.
86. Zhang S., Wang L. Fruit consumption and seed dispersal of Ziziphus cinnamomum (Rhamnaceae) by two sympatric primates (Cebus apella and Ateles paniscus) in French Guiana. Biotropica 1995, 27:397-401.