The latrine effect: Impact of howler monkeys on the distribution of small seeds in a tropical rain-forest soil

Journal of Tropical Ecology

Volumn 25, Issue 3, 2009, Pages 239-248

  Pouvelle, Sandrine ^a   Jouard, Sylvie ^a   Feer, Franois ^a   Tully, Thomas ^a   Ponge, Jean François ^a  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

Alouatta seniculus; Forest regeneration; French Guiana; Rain forest; Seed dispersal; Soil seed bank

Indexed keywords

BEETLE; FOREST SOIL; PRIMATE; RAINFOREST; REGENERATION; SEED BANK; SEED DISPERSAL; TROPICAL FOREST;

FRENCH GUIANA; NOURAGUES; SOUTH AMERICA;

ALOUATTA; ALOUATTA SENICULUS; COLEOPTERA;

EID: 69849107391     PISSN: 02664674     EISSN: 14697831     Source Type: Journal    
DOI: 10.1017/S0266467409005987     Document Type: Article

References (64)

1. ANDRESEN, E. 2002a. Dung beetles in a Central Amazonian rainforest and their ecological role as secondary seed dispersers. Ecological Entomology 27:257-270.
2. ANDRESEN, E. 2002b. Primary seed dispersal by red howler monkey and the effect of defecation patterns on the fate of dispersed seeds. Biotropica 34:262-272.
3. ANDRESEN, E. & FEER, F. 2005. The role of dung beetles as secondary seed dispersers and their effects on plant regeneration in tropical rainforests. Pp. 331-349 in Forget, P. M., Lambert, J. E., Hulme, P. E. & Vander Wall, S. B. (eds.). Seed fate: predation, dispersal and seedling establishment. CAB International, Wallingford.
4. ANDRESEN, E. & LEVEY, D. J. 2004. Effects of dung and seed size on secondary dispersal, seed predation, and seedling establishment of rain forest trees. Oecologia 139:45-54.
5. BLOUIN, M., ZUILY-FODIL, Y., PHAM-THI, A. T., LAFFRAY, D., REVERSAT, G., PANDO, A., TONDOH, J. & LAVELLE, P. 2005. Belowground organism activities affect plant aboveground phenotype, inducing plant tolerance to parasites. Ecology Letters 8:202-208.
6. BORZA, J. K., WESTERMAN, P. R. & LIEBMAN, M. 2007. Comparing estimates of seed viability in three foxtail (Setaria) species using the imbibed seed crush test with and without additional tetrazolium testing. Weed Technology 21:518-522.
7. CHARLES-DOMINIQUE, P. 2001. The field station. Pp. 1-7 in Bongers, F., Charles-Dominique, P., Forget, P. M. & Thery, M. (eds.). Nouragues: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer, Dordrecht.
8. CHARLES-DOMINIQUE, P. & COCKLE, A. 2001. Frugivory and seed dispersal by bats. Pp. 207-215 in Bongers, F., Charles-Dominique, P., Forget, P. M. & Thery, M. (eds.). Nouragues: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer, Dordrecht.
9. COLWELL, R. K. & CODDINGTON, J. A. 1994. Estimating terrestrial biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 345:101-118.
10. CONNELL, J. H. 1971. On the role of natural enemies in preventing competitive exclusion in some marine and in rain forest trees. Pp. 298-312 in den Boer, P. J. & Gradwell, G. R. (eds.). Dynamics of populations. PUDOC, Wageningen.
11. DALLING, J. W., SWAINE, M. D. & GARWOOD, N. C. 1998. Dispersal patterns and seed bank dynamics of pioneer trees in moist tropical forest. Ecology 79:564-578.
12. DALLING, J. W., MULLER-LANDAU, H. C., WRIGHT, S. J. & HUBBELL, S. P. 2002. Role of dispersal in the recruitment limitation of neotropical pioneer species. Journal of Ecology 90:714-727.
13. DECAENS, T., MARIANI, L., BETANCOURT, N. & JIMENEZ, J. J. 2003. Seed dispersion by surface casting activities of earthworms in Colombian grasslands. Acta Oecologica 24: 175-185.
14. DIAZ, S., TILMAN, D. & FARGIONE, J. 2005. Biodiversity regulation of ecosystem services. Pp. 297-329 in Hassan, R. M., Scholes, R. & Ash, N. (eds.). Ecosystems and human well-being: current state and trends. Island Press, Washington.
15. ENGEL, T. 2000. Seed dispersal and forest regeneration in a tropical lowland biocoenosis (Shimba Hills, Kenya). Logos, Berlin. 354 pp.
16. FAO 2006. World reference base for soil resources. Food and Agriculture Organization of the United Nations, Rome. 142 pp.
17. FAVRICHON, V. 1994. Classification des especes arborées en groupés fonctionnels en vue de la realisation d'un mód ele de dynamique dés peuplements en foret guyanaisê. Revue d'Ecologie (La Terre et la Vie) 49:379-403.
18. FEELEY, K. 2005. The role of clumped defecation in the spatial distribution of soil nutrients and the availability of nutrients for plant uptake. Journal of Tropical Ecology 21:99-102.
19. FEER, F. 1999. Effects of dung beetles (Scarabaeidae) on seeds dispersed by howler monkeys (Alouatta seniculus) in the French Guianan rain forest. Journal of Tropical Ecology 15:129-142.
20. FEER, F. & HINGRAT, Y. 2005. Effects of forest fragmentation on a dung beetle community in French Guiana. Conservation Biology 19:1103-1112.
21. FEER, F. & PINCEBOURDE, S. 2005. Diel flight activity and ecological segregation within an assemblage of tropical forest dung and carrion beetles. Journal of Tropical Ecology 21:21-30.
22. FORGET, P. M. 1996. Removal of seeds of Carapa procera (Meliaceae) by rodents and their fate in rainforest in French Guiana. Journal of Tropical Ecology 12:751-761.
23. FORGET, P. M. 1997. Effect of microhabitat on seed fate and seedling performance in two rodent-dispersed tree species in rain forest in French Guiana. Journal of Ecology 85:693-703.
24. FORGET, P. M. & JANSEN, P. A. 2007. Hunting increases dispersal limitation in the tree Carapa procera, a nontimber forest product. Conservation Biology 21:106-113.
25. GRIMALDI, M. & RIERA, B. 2001. Geography and climate. Pp. 9-18 in Bongers, F., Charles-Dominique, P., Forget, P. M. & Thery, M. (eds.).Nouragues: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer, Dordrecht.
26. HENRY, M.& JOUARD, S. 2007.Effectofbatexclusiononpatternsofseed rain in tropical rain forest in French Guiana. Biotropica 39:510-518.
27. IHAKA, R. & GENTLEMAN, R. 1996. R: a language for data analysis and graphics. Journal of Computational and Graphical Statistics 5: 299-314.
28. JANKOWSKA-BLASCZUK, M. & GRUBB, P. J. 2006. Changing perspectives on the role of the soil seed bank in northern temperate deciduous forests and in tropical lowland rain forests: parallels and contrasts. Perspectives in Plant Ecology, Evolution and Systematics 8:3-21.
29. JANZEN, D. H. 1970. Herbivores and the number of tree species in tropical forests. The American Naturalist 104:501-528.
30. JULLIOT,C.1992.Utilisation des ressources alimentaires par le singe hurleur roux, Alouatta seniculus (Atelidae, Primates), en Guyane: impact de la dissemination des graines sur la reg en eration forestiere. D.Sc. Thesis, University of Tours, France.
31. JULLIOT, C. 1994. Frugivory and seed dispersal by red howler monkeys: evolutionary aspect. Revue d'Ecologie (La Terre et la Vie) 49:331-341.
32. JULLIOT, C. 1996a. Seed dispersal by red howler monkeys (Alouatta seniculus) in the tropical rain forest of French Guiana. International Journal of Primatology 17:239-258. (Pubitemid 126722484)
33. JULLIOT, C. 1996b. Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest. American Journal of Primatology 40:261-282.
34. JULLIOT, C. 1997. Impact of seed dispersal by red howler monkeys Alouatta seniculus on the seedling population in the understorey of tropical rain forest. Journal of Ecology 85:431-440.
35. JULLIOT, C. & SABATIER, D. 1993. Diet of the howler monkey (Alouatta seniculus) in French Guiana. International Journal of Primatology 14:527-550.
36. JULLIOT, C., SIMMEN, B. & ZHANG, S. 2001. Frugivory and seed dispersalbythreeneotropicalprimates:impactonplantregeneration. Pp. 197-205 in Bongers, F., Charles-Dominique, P., Forget, P. M. & Thery, M. (eds.). Nouragues: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer, Dordrecht.
37. LAMBERT, J. E. & CHAPMAN, C. A. 2005. The fate of primate-dispersed seeds: deposition pattern, dispersal distance and implications for conservation. Pp. 137-150 in Forget, P. M., Lambert, J. E., Hulme, P. E. & Vander Wall, S. B. (eds.). Seed fate: predation, dispersal and seedling establishment. CAB International, Wallingford.
38. LEVEY, D. J. & BYRNE, M. M. 1993. Complex ant-plant interactions: rain forest ants as secondary dispersers and post-dispersal seed predators. Ecology 74:1802-1812.
39. MARTHEWS, T. R., MULLINS, C. E., DALLING, J. W. & BURSLEM, D. F. R. P. 2008. Burial and secondary dispersal of small seeds in a tropical forest. Journal of Tropical Ecology 24:595-605.
40. PEARSON, T. R. H., BURSLEM, D. F. R. P., MULLINS, C. E. & DALLING, J. W. 2003. Functional significance of photoblastic germination in neotropical pioneer trees: a seed's eye view. Functional Ecology 17:394-402.
41. PINHEIRO, J. C. & BATES, D. M. 2000. Mixed-effects models in S and S-Plus. Springer, New York. 528 pp.
42. PIZO, M. A., PASSOS, L. & OLIVEIRA, P. S. 2005. Ants as seed dispersers of fleshy diaspores in Brazilian Atlantic forests. Pp. 315-329 in Forget, P. M., Lambert, J. E., Hulme, P. E. & Vander Wall, S. B. (eds.). Seed fate: predation, dispersal and seedling establishment. CAB International, Wallingford.
43. PONCE-SANTIZO, G., ANDRESEN, E., CANO, E. & CUARON, A. D. 2006. Dispersion primaria de semillas por Primates y dispersión secundaría por escarabajos coprofagós en Tikal, Guatemala. Biotropica 38:390-397.
44. JANKOWSKA-BLASCZUK, M. & GRUBB, P. J. 2006. Changing perspectives on the role of the soil seed bank in northern temperate deciduous forests and in tropical lowland rain forests: parallels and contrasts. Perspectives in Plant Ecology, Evolution and Systematics 8:3-21.
45. JANZEN, D. H. 1970. Herbivores and the number of tree species in tropical forests. The American Naturalist 104:501-528.
46. JULLIOT,C.1992.Utilisation des ressources alimentaires par le singe hurleur roux, Alouatta seniculus (Atelidae, Primates), en Guyane: Impact de la dissemination des graines sur la reg en eration forestiere. D.Sc. Thesis, University of Tours, France.
47. JULLIOT, C. 1994. Frugivory and seed dispersal by red howler monkeys: evolutionary aspect. Revue d'Ecologie (La Terre et la Vie) 49:331-341.
48. JULLIOT, C. 1996a. Seed dispersal by red howler monkeys (Alouatta seniculus) in the tropical rain forest of French Guiana. International Journal of Primatology 17:239-258. (Pubitemid 126722484)
49. JULLIOT, C. 1996b. Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest. American Journal of Primatology 40:261-282.
50. JULLIOT, C. 1997. Impact of seed dispersal by red howler monkeys Alouatta seniculus on the seedling population in the understorey of tropical rain forest. Journal of Ecology 85:431-440.
51. JULLIOT, C. & SABATIER, D. 1993. Diet of the howler monkey (Alouatta seniculus) in French Guiana. International Journal of Primatology 14:527-550.
52. JULLIOT, C., SIMMEN, B. & ZHANG, S. 2001. Frugivory and seed dispersalbythreeneotropicalprimates:impactonplantregeneration. Pp. 197-205 in Bongers, F., Charles-Dominique, P., Forget, P. M. & Thery, M. (eds.). Nouragues: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer, Dordrecht.
53. LAMBERT, J. E. & CHAPMAN, C. A. 2005. The fate of primate-dispersed seeds: deposition pattern, dispersal distance and implications for conservation. Pp. 137-150 in Forget, P. M., Lambert, J. E., Hulme, P. E. & Vander Wall, S. B. (eds.). Seed fate: predation, dispersal and seedling establishment. CAB International, Wallingford.
54. LEVEY, D. J. & BYRNE, M. M. 1993. Complex ant-plant interactions: rain forest ants as secondary dispersers and post-dispersal seed predators. Ecology 74:1802-1812.
55. MARTHEWS, T. R., MULLINS, C. E., DALLING, J. W. & BURSLEM, D. F. R. P. 2008. Burial and secondary dispersal of small seeds in a tropical forest. Journal of Tropical Ecology 24:595-605.
56. PEARSON, T. R. H., BURSLEM, D. F. R. P., MULLINS, C. E. & DALLING, J. W. 2003. Functional significance of photoblastic germination in neotropical pioneer trees: a seed's eye view. Functional Ecology 17:394-402.
57. PINHEIRO, J. C. & BATES, D. M. 2000. Mixed-effects models in S and S-Plus. Springer, New York. 528 pp.
58. PIZO, M. A., PASSOS, L. & OLIVEIRA, P. S. 2005. Ants as seed dispersers of fleshy diaspores in Brazilian Atlantic forests. Pp. 315-329 in Forget, P. M., Lambert, J. E., Hulme, P. E. & Vander Wall, S. B. (eds.). Seed fate: predation, dispersal and seedling establishment. CAB International, Wallingford.
59. PONCE-SANTIZO, G., ANDRESEN, E., CANO, E. & CUARON, A. D. 2006. Dispersion primaria de semillas por Primates y dispérsi on secundaría por escarabajos coprofagós en Tikal, Guatemala. Biotropica 38:390-397.
60. To fruit supplies. Pp. 89-101 in Bongers, F., Charles-Dominique, P., Forget, P. M. & Thery, M. (eds.). Nouragues: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer, Dordrecht.
61. THERY, M. & LARPIN, D. 1993. Seed dispersal and vegetation dynamics at a cock-of-the-rock's lek in the tropical forest of French Guiana. Journal of Tropical Ecology 9:109-116.
62. VANDER WALL, S. B. & LONGLAND, W. 2004. Diplochory: are two dispersers better than one? Trends in Ecology and Evolution 19:155-161.
63. VITOUSEK, P. M. 1984. Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65:285-298.
64. VULINEC, K., LAMBERT, J. E. & MELLOW, D. J. 2006. Primate and dung beetle communities in secondary growth rain forests: implications for conservation of seed dispersal systems. International Journal of Primatology 27:855-879.