Frugivory and Seed Dispersal by Brown Lemurs in a Malagasy Tropical Dry Forest

Biotropica

Volumn 44, Issue 4, 2012, Pages 479-488

  Sato, Hiroki ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Fecal analysis; Fruit consumption; Germination; Keystone disperser; Lemurs; Mutualism; Seed size

Indexed keywords

DRY FOREST; FECES; FEEDING BEHAVIOR; FRUGIVORY; GERMINATION; KEYSTONE SPECIES; MUTUALISM; PRIMATE; REGENERATION; SEED DISPERSAL; SEED SIZE; SPECIES DIVERSITY; TROPICAL FOREST;

MADAGASCAR;

ANIMALIA; EULEMUR FULVUS; EULEMUR FULVUS FULVUS; GREWIA; LEMURIDAE; PRIMATES; VITEX;

EID: 84863429229     PISSN: 00063606     EISSN: 17447429     Source Type: Journal    
DOI: 10.1111/j.1744-7429.2011.00838.x     Document Type: Article

References (74)

1. Agetsuma, N. 1995. Foraging strategies of Yakushima macaques (Macaca fuscata yakui). Int. J. Primatol. 16: 595-609.
2. Altmann, J. 1974. Observational study of behavior: Sampling methods. Behaviour 49: 227-267.
3. Ankarafantsika National Park. 2006. Liste des Plantes Répertoiées dans Région d'Ankarafantsika. ANGAP Ankarafantsika, Andranofasika.
4. Birkinshaw, C. R. 2001. Fruit characteristics of species dispersed by black lemur (Eulemur macaco) in the Lokobe Forest, Madagascar. Biotropica 33: 478-486.
5. Bollen, A., and L. Van Elsacker 2002. Feeding ecology of Pteropus rufus (Pteropodidae) in the littoral forest of Sainte Luce (south-east Madagascar). Acta Chiropterol. 4: 33-47.
6. Bollen, A., L. Van Elsacker, and J. U. Ganzhorn 2004. Relations between fruits and disperser assemblages in a Malagasy littoral forest: A community-level approach. J. Trop. Ecol. 20: 599-612.
7. Bunker, D. E., F. DeClerck, J. C. Bradford, R. K. Colwell, I. Perfecto, O. L. Phillips, M. Sankaran, and S. Naeem 2005. Species loss and aboveground carbon storage in a tropical forest. Science 310: 1029-1031.
8. Burney, D. A., L. P. Burney, L. R. Godfrey, W. L. Jungers, S. M. Goodman, H. T. Wright, and A. J. T. Jull 2004. A chronology for late prehistoric Madagascar. J. Hum. Evol. 47: 25-63.
9. Campbell, J. L., J. H. Eisemann, C. V. Williams, and M. G. Kelly 2000. Description of gastrointestinal tract of five lemur species: Propithecus tattersalli, Propithecus verreauxi coquereli, Varecia variegata, Hapalemur griseus, and Lemur catta. Am. J. Primatol. 52: 133-142.
10. Campbell, J. L., C. V. Williams, and J. H. Eisemann 2004. Characterizing gastrointestinal transit time in four lemur species using barium-impregnated polyethylene spheres (BIPS). Am. J. Primatol. 64: 309-321.
11. Chapman, C. A. 1995. Primate seed dispersal: Coevolution and conservation implications. Evol. Anthropol. 4: 74-82.
12. Chapman, L. J., C. A. Chapman, and R. W. Wrangham 1992. Balanites wilsoniana: Elephant dependent dispersal? J. Trop. Ecol. 8: 275-283.
13. Chapman, C. A., and D. A. Onderdonk 1998. Forests without primates: Primate/plant codependency. Am. J. Primatol. 45: 127-141.
14. Charalambidou, I., L. Santamaría, C. Jansen, and B. A. Nolet 2005. Digestive plasticity in Mallard ducks modulates dispersal probabilities of aquatic plants and crustaceans. Funct. Ecol. 19: 513-519.
15. Cipollini, M. L., and D. J. Levey 1997. Secondary metabolites of fleshy vertebrate-dispersed fruits: Adaptive hypotheses and implications for seed dispersal. Am. Nat. 150: 346-372.
16. Cochrane, E. P. 2003. The need to be eaten: Balanites wilsoniana with and without elephant seed dispersal. J. Trop. Ecol. 19: 579-589.
17. Cordeiro, N. J., and H. F. Howe 2003. Forest fragmentation severs mutualism between seed dispersers and an endemic African tree. Proc. Natl. Acad. Sci. USA. 100: 14052-14056.
18. Corlett, R. T. 2002. Frugivory and seed dispersal in degraded tropical East Asian landscapes. In D. J. Levey, W. R. Silva, and M. Galetti (Eds.). Seed Dispersal and Frugivory: Ecology, Evolution and Conservation, pp. 451-465. CAB International, Wallingford.
19. Corlett, R. T. 2007. Pollination or seed dispersal: which should we worry about most? In A. J. Dennis, E. W. Schupp, R. J. Green, and D. A. Westcott (Eds.). Seed Dispersal: Theory and its Applications in a Changing World, pp. 523-544. CAB International, Wallingford.
20. Davis, A., and D. Bridson 2003. Rubiaceae. In S. M. Goodman, and J. P. Benstead (Eds.). The Natural History of Madagascar, pp. 431-434. The University of Chicago Press, Chicago.
21. De Wit, M. J. 2003. Madagascar: Heads it's a continent, tails it's an island. Annu. Rev. Earth Planet Sci. 31: 213-248.
22. Dew, J. L., and P. Wright 1998. Frugivory and seed dispersal by four species of primates in Madagascar's eastern rain forest. Biotropica 30: 425-437.
23. Fleming, T. H. 1991. Fruiting plant-frugivore mutualism: the evolutionary theater and the ecological play. In P. W. Price, T. M. Lewinsohn, G. W. Fernandes, and W. W. Benson (Eds.). Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions, pp. 199-244. J. Wiley & Sons, New York.
24. Fleming, T. H., R. Breitwish, and G. H. Whitesides 1987. Patterns of tropical vertebrate frugivore diversity. Annu. Rev. Ecol. Syst. 18: 91-109.
25. Foster, S. A., and C. H. Janson 1985. The relationship between seed size and establishment conditions in tropical woody plants. Ecology 66: 773-780.
26. Ganzhorn, J. U., S. Arrigo-Nelson, S. Boinski, A. Bollen, V. Carrai, A. Derby, G. Donati, A. Koenig, M. Kowalewski, P. Lahann, I. Norscia, S. Polowinsky, C. Schwitzer, P. R. Stevenson, M. G. Talebi, C. Tan, E. R. Vogel, and P. C. Wright 2009. Possible fruit protein effects of primate communities in Madagascar and the Neotropics. PLoS ONE 4: e8253.
27. Ganzhorn, J. U., J. Fietz, E. Rakotovao, D. Schwab, and D. Zinner 1999a. Lemurs and the regeneration of dry deciduous forest in Madagascar. Conserv. Biol. 13: 794-804.
28. Ganzhorn, J. U., P. C. Wright, and J. Ratsimbazafy 1999b. Primate communities: Madagascar. In J. G. Fleagle, C. Janson, and K. E. Reed (Eds.). Primate Communities, pp. 75-89. Cambridge University Press, Cambridge.
29. Garbutt, N. 2007. Mammals of Madagascar: a Complete Guide. Yale University Press, New Haven and London.
30. Gautier, L. 2003. Sapotaceae. In S. M. Goodman, and J. P. Benstead (Eds.). The Natural History of Madagascar, pp. 342-346. The University of Chicago Press, Chicago.
31. Godfrey, L. R., G. M. Semprebon, W. L. Jungers, M. R. Sutherland, E. L. Simons, and N. Solounias 2004. Dental use wear in extinct lemurs: Evidence of diet and niche differentiation. J. Hum. Evol. 47: 145-169.
32. Goodman, S. M., and J. U. Ganzhorn 1997. Rarity of figs (Ficus) on Madagascar and its relationship to a depauperate frugivore community. Rev. Ecol. 52: 321-329.
33. Harrison, M. J. S. 1985. Time budget of the green monkey, Ceropithecus sabaeus: Some optimal strategies. Int. J. Primatol. 6: 351-376.
34. Hemingway, C. A. 1998. Selectivity and variability in the diet of Milne-Edwards' sifakas (Propithecus diadema edwardsi): Implications for folivory and seed-eating. Int. J. Primatol. 19: 355-377.
35. Hyatt, L. A., and A. S. Evans 1998. Is decreased germination fraction associated with risk of sibling competition? Oikos 83: 29-35.
36. Johnson, S. E. 2006. Evolutionary divergence in the brown lemur species complex. In L. Gould, and M. L. Sauther (Eds.). Lemurs: Ecology and Adaptation, pp. 187-210. Springer, New York.
37. Jones, R. H., and R. R. Sharitz 1989. Potential advantages and disadvantages of germinating early for trees in floodplain forests. Oecologia 81: 443-449.
38. Julliot, C. 1996. Seed dispersal by red howling monkeys (Alouatta seniculus) in the tropical rain forest of French Guiana. Int. J. Primatol. 17: 239-258.
39. Kitamura, S., T. Yumoto, P. Poonswad, P. Chuailua, K. Plongmai, T. Maruhashi, and N. Noma 2002. Interactions between fleshy fruits and frugivores in a tropical seasonal forest in Thailand. Oecologia 133: 559-572.
40. Labat, J. N., and J. Moat 2003. Legumonosae (Fabaceae). In S. M. Goodman, and J. P. Benstead (Eds.). The Natural History of Madagascar, pp. 346-373. The University of Chicago Press, Chicago.
41. Lahann, P. 2007. Feeding ecology and seed dispersal of sympatric cheirogaleid lemurs (Microcebus murinus, Cheirogaleus medius, Cheirogaleus major) in the littoral rainforest of south-east Madagascar. J. Zool. 271: 88-98.
42. Lambert, J. E. 1998. Primate digestion: Interactions among anatomy, physiology, and feeding ecology. Evol. Anthropol. 7: 8-20.
43. Lambert, J. E., and C. A. Chapman 2005. The fate of primate-dispersed seeds: deposition pattern, dispersal distance and implications for conservation. In P. M. Forget, J. E. Lambert, P. E. Hulme, and S. B. Vander Wall (Eds.). Seed fate: Predation, Dispersal and Seedling Establishment, pp. 137-150. CAB International, Wallingford.
44. Leroy, J. F. 1978. Composition, origin, and affinities of the Madagascan vascular flora. Ann. Mo. Bot. Gard. 65: 535-589.
45. Levey, D. J., and A. Grajal 1991. Evolutionary implications of fruit-processing limitations in cedar waxwings. Am. Nat. 138: 171-189.
46. Lewis, D. M. 1987. Fruiting patterns, seed germination, and distribution of Sclerocarya caffra in an elephant-inhabited woodland. Biotropica 19: 50-56.
47. Loiselle, B. A. 1990. Seeds in droppings of tropical fruit-eating birds: Importance of considering seed composition. Oecologia 82: 494-500.
48. Mack, A. L., and D. D. Wright 2005. The frugivore community and the fruiting plant flora in a New Guinea rainforest: Identifying keystone frugivores. In J. L. Dew, and J. P. Boubli (Eds.). Tropical Fruits and Frugivores: The Search for Strong Interactors, pp. 185-203. Springer, Dordrecht.
49. McConkey, K. R., F. Aldy, A. Ario, and D. J. Chivers 2002. Selection of fruit by gibbons (Hylobates muelleri X agilis) in the rain forests of Central Borneo. Int. J. Primatol. 23: 123-145.
50. Mittermeier, R. A., E. E. Louis Jr, M. Richardson, C. Schwitzer, O. Langrand, A. B. Rylands, F. Hawkins, S. Rajaobelina, J. Ratsimbazafy, R. Rasoloarison, C. Roos, P. M. Kappeler, and J. Mackinnon 2010. Lemurs of Madagascar(3rd Ed.), Conservation International, Washington, D. C.
51. Morris, P., and F. Hawkins 1998. Birds of Madagascar: A Photographic Guide. Yale University Press, New Haven and London.
52. Murray, K. G., S. Russell, C. M. Picone, K. Winnett-Murray, W. Sherwood, and M. L. Kuhlmann 1994. Fruit laxatives and seed passage rates in frugivores: Consequences for plant reproductive success. Ecology 75: 989-994.
53. Noma, N., and T. Yumoto 1997. Fruiting phenology of animal-dispersed plants in response to winter migration of frugivores in a warm temperate forest on Yakushima Island, Japan. Ecol. Res. 12: 119-129.
54. Overdorff, D. J., and S. G. Strait 1998. Seed handling by three prosimian primates in southeastern Madagascar: Implications for seed dispersal. Am. J. Primatol. 45: 69-82.
55. Pearson, T. R. H., D. F. R. P. Burslem, C. E. Mullins, and J. W. Dalling 2002. Germination ecology of neotropical pioneers: Interacting effects of environmental conditions and seed size. Ecology 83: 2798-2807.
56. Peres, C. A., and E. Palacios 2007. Basin-wide effects of game harvest on vertebrate population densities in Amazonian forests: Implications for animal-mediated seed dispersal. Biotropica 39: 304-315.
57. Poulsen, J. R., C. J. Clark, and T. B. Smith 2001. Seed dispersal by diurnal primate community in the Dja Reserve, Cameroon. J. Trop. Ecol. 17: 787-808.
58. Randrianasolo, A. 2003. Anacardiaceae. In S. M. Goodman, and J. P. Benstead (Eds.). The Natural History of Madagascar, pp. 398-402. The University of Chicago Press, Chicago.
59. Rasmussen, M. A. 1999. Ecological Influences on Activity Cycle in Two Cathemeral Primates, the Mongoose Lemur (Eulemur mongoz) and the Common Brown Lemur (Eulemur fulvus fulvus). PhD Dissertation. Duke University, Raleigh.
60. Robertson, A. W., A. Trass, J. J. Ladley, and D. Kelly 2006. Assessing the benefits of frugivory for seed germination: The importance of the deinhibition effect. Funct. Ecol. 20: 58-66.
61. Samuels, I. A., and D. J. Levey 2005. Effects of gut passage on seed germination: Do experiments answer the questions they ask? Funct. Ecol. 19: 365-368.
62. Sato, H. 2009. Gut passage time and size of swallowed seeds in the common brown lemur and the mongoose lemur. Primate Res. 25: 45-54.
63. Sato, H. 2011. The Foraging Strategy of Common Brown Lemurs and the Importance as Seed Dispersers in a Dry Deciduous Forest in Northwestern Madagascar. PhD Dissertation. Kyoto University, Kyoto.
64. Schatz, G. E. 2001. Generic Tree Flora of Madagascar. The Cromwell Press, Royal Botanic Gardens, Kew and Missouri Botanical Garden, St Louis.
65. Schupp, E. W. 1993. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetation 107/108: 15-29.
66. Stevenson, P. R. 2007. Estimates of the number of seeds dispersed by a population of primates in a lowland forest in western Amazonia. In A. J. Dennis, E. W. Schupp, R. J. Green, and D. A. Westcott (Eds.). Seed Dispersal: Theory and its Applications in a Changing World, pp. 340-362. CAB International, Wallingford.
67. Tattersall, I., and R. W. Sussman 1998. 'Little brown lemurs' of northern Madagascar: Phylogeny and ecological role in resource partitioning. Folia Primatol. 69: 379-388.
68. Traveset, A., and M. Verdú 2002. A meta-analysis of the effect of gut treatment on seed germination. In D. J. Levey, W. R. Silva, and M. Galetti (Eds.). Seed Dispersal and Frugivory: Ecology, Evolution and Conservation, pp. 339-350. CAB International, Wallingford.
69. Tutin, C. E. G., E. A. Williamson, M. E. Rogers, and M. Fernandez 1991. A case study of a plant-animal relationship: Cola lizae and lowland gorillas in the Lope Reserve, Gabon. J. Trop. Ecol. 7: 181-199.
70. Willson, M. F., A. K. Irvine, and N. G. Walsh 1989. Vertebrate dispersal syndromes in some Australian and New Zealand plant communities, with geographic comparisons. Biotropica 21: 133-147.
71. Wrangham, R. W., C. A. Chapman, and L. J. Chapman 1994. Seed dispersal by forest chimpanzees in Uganda. J. Trop. Ecol. 10: 355-368.
72. Wright, P. C. 1999. Lemur traits and Madagascar ecology: Coping with an island environment. Yrbk. Phys. Anthropol. 42: 31-72.
73. Wright, P. C., V. R. Razafindratsita, S. T. Pochron, and J. Jernavall 2005. The key to Madagascar forugivores. In J. L. Dew, and J. P. Boubli (Eds.). Tropical Fruits and Frugivores: The Search for Strong Interactions, pp. 121-138. Springer, Dordrecht.
74. Wright, P. C., S. R. Tecot, E. M. Erhart, A. L. Baden, S. J. King, and C. Grassi 2011. Frugivory in four sympatric lemurs: Implications for the future of Madagascar's forests. Am. J. Primatol. 73: 585-602.