International Journal of Primatology

, Volume 32, Issue 1, pp 177–192 | Cite as

Effectiveness of Spider Monkeys (Ateles geoffroyi vellerosus) as Seed Dispersers in Continuous and Fragmented Rain Forests in Southern Mexico

  • Óscar M. Chaves
  • Kathryn E. Stoner
  • Víctor Arroyo-Rodríguez
  • Alejandro Estrada


Seed dispersal is considered a key process determining spatial structure and dynamics of plant populations, and has crucial implications for forest regeneration. We evaluated the effectiveness of spider monkeys (Ateles geoffroyi) as seed dispersers in continuous and fragmented habitats to test if this interaction is altered in forest fragments. We documented fruit and seed handling, defecation patterns, diversity and composition of seeds in feces, and seed germination of defecated and control seeds in the Lacandona rainforest, Mexico. For most species contributing to 80% of total fruit feeding time, monkeys swallowed and spat seeds, but swallowing was the most frequent seed handling category in continuous and fragmented forests. However, the proportion of feeding records of swallowed seeds was higher in continuous forest (0.59) than in fragments (0.46), whereas the opposite was true for proportion of dropped seeds (0.16 vs. 0.31). This pattern was reflected in the number of fecal samples containing seeds, which was greater in continuous (95.5%) than in fragmented forests (82.5%). Seeds in fecal samples included a total of 71 species from 23 plant families. The numbers of defecated seed species were similar between forest conditions, and in both cases most seeds (>86%) were undamaged. Defecated seeds showed greater germination percentages than control seeds in all of the five species evaluated. Although we identified some differences in seed handling and the percentage of feces with seeds between continuous forest and fragments, our results indicate that, in general terms, spider monkeys are effective seed dispersers in both forest conditions.


Forest regeneration Fragmentation Frugivorous primates Seed dispersal 



This research was supported by grants from the Consejo Nacional de Ciencia y Tecnología, México (CONACyT Grant CB-2005-51043 and CB-2006-56799). This article constitutes a partial fulfillment of the Graduate Program in Biological Sciences of the National Autonomous University of México (UNAM). The organization Idea Wild provided equipment. This study would not have been possible without the collaboration of the local people in Loma Bonita, Chajul, Reforma Agraria, and Zamora Pico de Oro ejidos. V. Sork, D. Scofield, P. Thompson, and M. Quesada provided useful comments and suggestions in advanced drafts of this article. We thank C. Hauglustaine, C. Balderas, S. Martínez, J. Herrera, A. González-Di Pierro, and R. Lombera for field assistance. J. Rodríguez collaborated in the identification of seeds, and J. M. Lobato, G. Sánchez, H. Ferreira, and A. Valencia provided technical support. We also thank J. M. Setchell, E. W. Schupp, and 1 anonymous reviewer for valuable criticisms and suggestions that improved the manuscript.

Supplementary material

10764_2010_9460_MOESM1_ESM.doc (119 kb)
ESM 1 (DOC 119 kb)


  1. Allaby, M. (2006). Tropical forests. New York: Chelsea House Publishers.Google Scholar
  2. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behavior, 49, 227–267.CrossRefGoogle Scholar
  3. 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.Google Scholar
  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.CrossRefPubMedGoogle Scholar
  5. Arroyo-Rodríguez, V., & Mandujano, S. (2006). Forest fragmentation modifies habitat quality for Alouatta palliata. International Journal of Primatology, 27, 1079–1096.CrossRefGoogle Scholar
  6. Arroyo-Rodríguez, V., Mandujano, S., & Benítez-Malvido, J. (2008). Landscape attributes affecting patch occupancy by howler monkeys (Alouatta palliata mexicana) at Los tuxtlas, Mexico. American Journal of Primatology, 70, 69–77.CrossRefPubMedGoogle Scholar
  7. Chapman, C. A. (1987). Flexibility in diets of three species of Costa Rican primates. Folia Primatologica, 49, 90–105.CrossRefGoogle Scholar
  8. Chapman, C. A. (1989). Primate seed dispersal: the fate of dispersed seeds. Biotropica, 21, 148–154.CrossRefGoogle Scholar
  9. Chapman, C. A. (1995). Primate seed dispersal: Coevolution and conservation implications. Evolutionary Anthropology, 4, 74–82.CrossRefGoogle Scholar
  10. Chapman, C. A., Chapman, L. J., Wangham, R., Hunt, K., Gebo, D., & Gardner, L. (1992). Estimators of fruit abundance of tropical trees. Biotropica, 24, 527–531.CrossRefGoogle Scholar
  11. Chaves, O. M., Stoner, K. E., & Arroyo-Rodríguez, V. (in press). Differences in diet between spider monkey groups living in forest fragments and continuous forest in Lacandona, Mexico. Biotropica. Google Scholar
  12. Cheplick, G. P. (1992). Sibling competition in plants. Journal of Ecology, 80, 567–575.CrossRefGoogle Scholar
  13. Cordeiro, N. J., Indangalasi, H. J., McEntee, J. P., & Howe, H. F. (2009). Disperser limitation and recruitment of an endemic African tree in a fragmented landscape. Ecology, 90, 1030–1041.CrossRefPubMedGoogle Scholar
  14. Cosson, J. F., Pons, J. M., & Masson, D. (1999). Effects of forest fragmentation on frugivorous and nectarivorous bats in French Guiana. Journal of Tropical Ecology, 15, 515–534.CrossRefGoogle Scholar
  15. Crawley, M. (1993). GLIM for ecologists. Oxford: Blackwell Scientific Publications.Google Scholar
  16. Cristóbal-Azkarate, J., & Arroyo-Rodríguez, V. (2007). Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: Effects of habitat fragmentation and implications for conservation. American Journal of Primatology, 69, 1013–1029.CrossRefPubMedGoogle Scholar
  17. Dew, J. L. (2008). Spider monkeys as seed dispersers. In C. J. Campbell (Ed.), Spider monkeys: Behavior, ecology and evolution of the genus Ateles (pp. 155–182). Cambridge: Cambridge University Press.Google Scholar
  18. Di Fiore, A., & Campbell, C. J. (2007). The Atelines: variation in ecology, behavior, and social organization. In C. J. Campbell, A. Fuentes, K. C. Mackinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 155–185). Oxford: Oxford University Press.Google Scholar
  19. Di Fiore, A., Link, A., & Dew, J. L. (2008). Diets of wild spider monkeys. In C. J. Campbell (Ed.), Spider monkeys: Behavior, ecology and evolution of the genus Ateles (pp. 81–137). New York: Cambridge University Press.Google Scholar
  20. Dunn, J. C., Cristóbal-Azkarate, J., & Vea, J. J. (2009). Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa. American Journal of Primatology, 71, 654–662.CrossRefPubMedGoogle Scholar
  21. Estrada, A., Van Belle, S., & García del Valle, Y. (2004). Survey of black howler (Alouatta pigra) and spider (Ateles geoffroyi) monkeys along the Río Lacantún, Chiapas, Mexico. Neotropical Primates, 12, 70–75.Google Scholar
  22. Figueroa-Esquivel, E., Puebla-Olivares, F., Goudínez-Álvarez, H., & Núñez-Farfán, J. (2009). Seed dispersal effectiveness by understory birds on Dendropanax arboreus in a fragmented landscape. Biodiversity and Conservation, 18, 3357–3365.CrossRefGoogle Scholar
  23. Forget, M., & Cuijpers, L. (2008). Survival and scatterhoarding of frugivores-dispersed seeds as a function of forest disturbance. Biotropica, 40, 380–385.CrossRefGoogle Scholar
  24. Gentry, A. H. (1982). Neotropical floristic diversity: Phytogeographical connections between Central and South America, pleistocene climatic fluctuations, or an accident of the Andean orogeny? Annals of Missouri Botanical Garden, 69, 557–593.CrossRefGoogle Scholar
  25. González-Di Pierro, A., Benítez-Malvido, J., Mendez, M., Zermeño, I., Arroyo-Rodríguez, V., Stoner, K. E., & Estrada, A. (in press). Effects of the physical environment and primate gut passage on the early establishment of Ampelocera hottlei Standley in tropical rainforest fragments. Biotropica Google Scholar
  26. González-Zamora, A., Arroyo-Rodríguez, V., Chaves, O. M., Sánchez-López, S., Stoner, K. E., & Riba-Hernández, P. (2009). Diet of spider monkeys (Ateles geoffroyi) in Mesoamerica: Current knowledge and future directions. American Journal of Primatology, 71, 8–20.CrossRefPubMedGoogle Scholar
  27. Gotelli, N. J., & Entsminger, G. L. (2001). EcoSim: Null models software for ecology. Version 7.0. Acquired Intelligence Inc. & Kesey Bear. (
  28. Herrera, C. (1985). Determinants of plant-animal coevolution: The case mutualistic vertebrate seed disperser systems. Oikos, 44, 132–41.CrossRefGoogle Scholar
  29. Howe, H. F. (1989). Scatter and clump–dispersal and seedling demography: hypothesis and implications. Oecologia, 79, 417–426.CrossRefGoogle Scholar
  30. Janzen, D. H. (1970). Herbivores and the number of tree species in the tropical forest. American Naturalist, 104, 501–528.CrossRefGoogle Scholar
  31. Jordano, P. (1995). Angiosperm fleshy fruits and seed dispersers: A comparative analysis of adaptation and constraints in plant–animal interactions. American Naturalist, 145, 163–191.CrossRefGoogle Scholar
  32. Jordano, P., & Schupp, E. W. (2000). Seed disperser effectiveness: The quantity component and patterns of seed rain for Prunus mahaleb. Ecological Monographs, 70, 591–615.Google Scholar
  33. Julliot, C. (1996). Seed dispersal by red howling monkeys (Alouatta seniculus) in the tropical rain forest of French Guiana. International Journal of Primatology, 17, 239–258.CrossRefGoogle Scholar
  34. Link, A., & Di Fiore, A. (2006). Seed dispersal by spider monkeys and its importance in the maintenance of Neotropical rain-forest diversity. Journal of Tropical Ecology, 22, 235–246.CrossRefGoogle Scholar
  35. Martensen, C. A., Pimentel, R. G., & Metzger, J. P. (2008). Relative effects of fragment size and connectivity on bird community in the Atlantic Rain Forest: Implications for conservation. Biological Conservation, 141, 2184–2192.CrossRefGoogle Scholar
  36. Melo, F. P. L., Martínez-Salas, E., Benítez-Malvido, J., & Ceballos, G. (2010). Forest fragmentation reduces recruitment of large-seeded tree species in a semi-deciduous tropical forest of southern Mexico. Journal of Tropical Ecology, 26, 35–43.CrossRefGoogle Scholar
  37. Moran, C., Catterrall, C. P., & Kanowski, J. (2009). Reduced dispersal of native plant species as a consequence of the reduced abundance of frugivore species in fragmented rainforest. Biological Conservation, 142, 541–552.CrossRefGoogle Scholar
  38. Muller-Landau, H. C., & Hardesty, B. D. (2005). Seed dispersal of woody plants in tropical forests: Concepts, examples and future directions. In B. F. R. P. Burslem, M. A. Pinard, & S. E. Hartley (Eds.), Biotic interactions in the tropics: Their role in the maintenance of species diversity (pp. 267–309). Cambridge: Cambridge University Press.Google Scholar
  39. Nathan, R., & Casagrandi, R. (2004). A simple mechanistic model of seed dispersal, predation and plant establishment: Janzen-Connell and beyond. Journal of Ecology, 92, 733–746.CrossRefGoogle Scholar
  40. Norconk, M. A., Grafton, B. W., & Conklin-Brittain, N. L. (1998). Seed dispersal by neotropical seed predators. American Journal of Primatology, 45, 103–126.CrossRefPubMedGoogle Scholar
  41. Onderdonk, D. A., & Chapman, C. A. (2000). Coping with forest fragmentation: the primates of Kibale National Park, Uganda. International Journal of Primatology, 21, 587–611.CrossRefGoogle Scholar
  42. Orihuela-López, G., Terborgh, J., & Ceballos, N. (2005). Food selection by a hyperdense population of red howler monkeys (Alouatta seniculus). Journal of Tropical Ecology, 21, 445–450.CrossRefGoogle Scholar
  43. Queenborough, S. A., Burslem, D. F. R. P., Garwood, N. C., & Valencia, R. (2007). Neighborhood and community interactions determine the spatial pattern of tropical tree seedling survival. Ecology, 88, 2248–2258.CrossRefPubMedGoogle Scholar
  44. Russo, S. E. (2005). Linking seed fate to natural dispersal patterns: Factors affecting predation and scatter-hoarding of Virola calophylla seeds in Peru. Journal of Tropical Ecology, 21, 243–253.CrossRefGoogle Scholar
  45. Russo, S. E., & Augspurger, C. K. (2004). Aggregated seed dispersal by spider monkeys limits recruitment to clumped patterns in Virola calophylla. Ecolological Letters, 7, 1058–1067.CrossRefGoogle Scholar
  46. Russo, S. E., Campbell, C. J., Dew, J. L., Stevenson, P. R., & Suarez, S. A. (2005). A multi-forest comparison of dietary preferences and seed dispersal by Ateles spp. International Journal of Primatology, 26, 1017–1037.CrossRefGoogle Scholar
  47. Schupp, E. W. (1993). Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio, 107(108), 15–29.Google Scholar
  48. Schupp, E. W., & Fuentes, M. (1995). Spatial patterns of seed dispersal and the unification of plant-population ecology. Ecoscience, 2, 267–275.Google Scholar
  49. Stevenson, P. R. (2000). Seed dispersal by woolly monkeys (Lagothrix lagotricha) at Tinigua National Park, Colombia: Dispersal distance, germination rates, and dispersal quantity. American Journal of Primatology, 50, 275–289.CrossRefPubMedGoogle Scholar
  50. Stevenson, P. R. (2004). Fruit choice by woolly monkeys in Tinigua National Park, Colombia. International Journal of Primatology, 25, 367–381.CrossRefGoogle Scholar
  51. 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, & D. W. Westcott (Eds.), Seed dispersal: Theory and its application in a changing world (pp. 340–362). Wallingford, UK: CAB International.Google Scholar
  52. Stevenson, P. R., & Aldana, A. M. (2008). Potential effects of Ateline extinction and forest fragmentation on plant diversity and composition in the western Orinoco Basin, Colombia. International Journal of Primatology, 29, 365–377.CrossRefGoogle Scholar
  53. Stevenson, P. R., Castellanos, M. C., Pizarro, J. C., & Garavito, M. (2002). Effects of seed dispersal by three ateline monkey species on seed germination at Tinigua National Park, Colombia. International Journal of Primatology, 23, 1187–1204.CrossRefGoogle Scholar
  54. Stevenson, P. R., Pineda, M., & Samper, T. (2005). Influence of seed size on dispersal patterns of woolly monkeys (Lagothrix lagotricha) at Tinigua Park, Colombia. Oikos, 110, 435–440.CrossRefGoogle Scholar
  55. Stoner, K. E., Riba-Hernández, P., Vulinec, K., & Lambert, J. E. (2007). The role of mammals in creating and modifying seedshadows in tropical forests and some possible consequences of their elimination. Biotropica, 39, 316–327.CrossRefGoogle Scholar
  56. Uribe Mú, C. A. (2006). Interacción entre el insecto barrenador Oncideres albomarginata Chamela y su planta hospedera Spondias purpurea. Ph.D. Thesis, Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México UNAM, Morelia, Michoacán, México.Google Scholar
  57. Valenta, K., & Fedigan, L. (2009). Effects of gut passage, feces, and seed handling on latency and rate of germination in seeds consumed by capuchins (Cebus capucinus). American Journal of Physical Anthropology, 138, 486–492.CrossRefPubMedGoogle Scholar
  58. Waterman, P. G. (1984). Food acquisition and processing as a function of plant chemistry. In D. J. Chivers, B. A. Wood, & A. Bilsborough (Eds.), Food acquisition and processing in primates (pp. 177–211). New York: Plenum Press.Google Scholar
  59. Wehncke, E. V., Valdez, C. N., & Domínguez, C. A. (2004). Seed dispersal and defecation patterns of Cebus capucinus and Alouatta palliata: Consequences for seed dispersal effectiveness. Journal of Tropical Ecology, 20, 535–543.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Óscar M. Chaves
    • 1
  • Kathryn E. Stoner
    • 1
  • Víctor Arroyo-Rodríguez
    • 1
  • Alejandro Estrada
    • 2
  1. 1.Centro de Investigaciones en EcosistemasUniversidad Nacional Autónoma de México (UNAM)MoreliaMexico
  2. 2.Laboratorio de Primates, Instituto de BiologíaUniversidad Nacional Autónoma de MéxicoSan Andrés TuxtlaMexico

Personalised recommendations