Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-08T19:28:28.747Z Has data issue: false hasContentIssue false
  • English
  • Français

Primary seed dispersal by three Neotropical seed-predating primates (Cacajao melanocephalus ouakary, Chiropotes chiropotes and Chiropotes albinasus)

Published online by Cambridge University Press:  22 November 2012

Adrian A. Barnett ,
Sarah A. Boyle ,
Liliam P. Pinto ,
Waldete C. Lourenço ,
Thais Almeida ,
Welma Sousa Silva ,
Beatriz Ronchi-Teles ,
Bruna M. Bezerra ,
Caroline Ross  and
Ann MacLarnon
...Show all authors
Adrian A. Barnett*
Affiliation:
Centre for Research in Evolutionary and Environmental Anthropology, Roehampton University, London SW15 4JD, UK Coordenação de Bioiversidade, Caixa Postal 478, Instituto Nacional de Pesquisas da Amazônia, Manaus 69060-001, Amazonas, Brazil
Sarah A. Boyle
Affiliation:
Department of Biology, Rhodes College, Memphis 38112-1690, Tennessee, USA Biological Dynamics of Forest Fragments Project, Instituto Nacional de Pesquisas da Amazônia and Smithsonian Tropical Research Institute, Manaus 69011-970, Amazonas, Brazil
Liliam P. Pinto
Affiliation:
Centro Nacional de Pesquisa e Conservação da Biodiversidade Amazônica, Instituto Chico Mendes de Conservação da Biodiversidade – I, Manaus, 69041-10, Amazonas, Brazil, and Curso de Pós-Graduação em Ecologia, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, São Paulo 13083-970, Brazil
Waldete C. Lourenço
Affiliation:
Biological Dynamics of Forest Fragments Project, Instituto Nacional de Pesquisas da Amazônia and Smithsonian Tropical Research Institute, Manaus 69011-970, Amazonas, Brazil
Thais Almeida
Affiliation:
Laboratório de Herpetologia, Universidade Federal do Mato Grosso, Av. Fernando Correa da Costa, 2367, Boa Esperança 78060-900, Mato Grosso, Brazil
Welma Sousa Silva
Affiliation:
Instituto de Ciências Exatas e Tecnologia, Universidade Federal do Amazonas, Rua N. Sra. Rosário, 3868, Itacoatiara 69100-000, Amazonas, Brazil
Beatriz Ronchi-Teles
Affiliation:
Coordenação de Pesquisas em Entomologia, Instituto Nacional de Pesquisas da Amazônia, Manaus 69060-000, Amazonas, Brazil
Bruna M. Bezerra
Affiliation:
Departamento de Zoologia, Universidade Federal de Pernambuco. Av. Prof. Moraes Rego, 1235 - Cidade Universitária, Recife - PE - CEP: 50670-901, Brazil
Caroline Ross
Affiliation:
Centre for Research in Evolutionary and Environmental Anthropology, Roehampton University, London SW15 4JD, UK
Ann MacLarnon
Affiliation:
Centre for Research in Evolutionary and Environmental Anthropology, Roehampton University, London SW15 4JD, UK
Wilson R. Spironello
Affiliation:
Coordenação de Bioiversidade, Caixa Postal 478, Instituto Nacional de Pesquisas da Amazônia, Manaus 69060-001, Amazonas, Brazil
*
1Corresponding author. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract:

The Neotropics house two guilds of large arboreal vertebrate seed predators: parrots and the pitheciin primates. Both have diets dominated by immature fruits. The possibility of members of the Pitheciinae (genera Cacajao, Chiropotes and Pithecia) acting as occasional seed dispersers has been mooted, but not experimentally shown. We combined primate behavioural data and seed germination data from three separate field studies in the Brazilian states of Amazonas and Pará to analyse patterns of post-consumption seed survivorship for seeds discarded by three pitheciin species (Cacajao melanocephalus ouakary, Chiropotes chiropotes and Chiropotes albinasus). We then calculated the frequency of dispersal events for four species eaten by C. m. ouakary. All three primate species dropped intact seeds while feeding, and 30.7% of 674 dropped seeds germinated ex situ. Undamaged seeds from unripe and ripe samples germinated (29.3% and 42.7%, respectively), and all three primate species carried some fruits up to 20 m from the parent tree before consuming them. Potential seed-dispersal events varied from 1 (Macrolobium acaciifolium) per fruiting cycle to more than 6500 (Duroia velutina), suggesting that there are differences in dispersal potential. In summary, although they are highly specialized seed predators, these primates may also act as important dispersers for some plant species, and effective dispersal is not restricted to ripe fruits, as immature fruits removed from a tree may continue to mature and the seeds later germinate, a much-neglected aspect of dispersal ecology. The possibility that similar events occur in parrots should be experimentally investigated.

Keywords

Amazonasfrugivoreprimatesseed dispersalseed predator
Type
Research Article
Information
Journal of Tropical Ecology , Volume 28 , Issue 6 , November 2012 , pp. 543 - 555
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ADLER, G. H. 1995. Fruit and seed exploitation by Central American spiny rats, Proechimys semispinosus. Studies in Neotropical Fauna and Environment 30:237–244.CrossRefGoogle Scholar
ALTMANN, J. 1974. Observational study of behavior: sampling methods. Behaviour 48:227–265.CrossRefGoogle Scholar
ARAÚJO-LIMA, C. & GOULDING, M. 1998. Os frutos do tambaqui: ecologia, conservação e cultivo na Amazônia. Sociedade Civil Mamirauá/CNPq, Brasília. 186 pp.Google Scholar
AYRES, J. M. 1989. Comparative feeding ecology of the uakari and bearded saki, Cacajao and Chiropotes. Journal of Human Evolution 18:697–716.CrossRefGoogle Scholar
BARNETT, A. A. 2010. Diet, habitat use and conservation ecology of the golden-backed uacari, Cacajao melanocephalus ouakary, in Jaú National Park, Amazonian Brazil. PhD dissertation, Centre for Research in Evolutionary Anthropology, Roehampton University, London, UK.Google Scholar
BARNETT, A. A. & BRANDON-JONES, D. 1997. The ecology, biogeography and conservation of the uacaris, Cacajao (Pitheciinae). Folia Primatologica 68:223–235.CrossRefGoogle Scholar
BARNETT, A. A., DE CASTILHO, C. V., SHAPLEY, R. L. & ANICÁCIO, A. 2005. Diet, habitat selection and natural history of Cacajao melanocephalus ouakary in Jaú National Park, Brazil. International Journal of Primatology 26:949–969.CrossRefGoogle Scholar
BARNETT, A. A., BOYLE, S. A., NORCONK, M. A., PALMINTERI, S., SANTOS, R. R., VEIGA, L. M., ALVIM, T. H. G., BOWLER, M., CHISM, J., DI FIORE, A., FERNANDEZ-DUQUE, E., GUIMARÃES, A. C. P., HARRISON-LEVINE, A., HAUGAASEN, T., LEHMAN, S., MACKINNON, K., DE MELO, F. R., MOREIRA, L. S., MOURAV., S. V., S., PHILLIPS, C. R., PINTO, L. P., PORT-CARVALHO, M., SETZ, E. Z. F., SHAFFER, C., DA SILVA, L. R., DA SILVA, S. S. B., SOARES, R. F., THOMPSON, C. L., VIEIRA, T. M., VREEDZAAM, A., WALKER-PACHECO, S. E., SPIRONELLO, W. R., MACLARNON, A. & FERRARI, S. F. 2012 a. Terrestrial activity in Pitheciins (Cacajao, Chiropotes, and Pithecia). American Journal of Primatology DOI 10.1002/ajp.22068:1–22.Google ScholarPubMed
BARNETT, A. A., SHAW, P., SPIRONELLO, W. R., MACLARNON, A. & ROSS, C. 2012 b. Sleeping site selection by golden-backed uacaris, Cacajao melanocephalus ouakary (Pitheciidae), in Amazonian flooded forests. Primates 53:273–285.CrossRefGoogle ScholarPubMed
BARNETT, A. A., PINTO, L. P., BICCA-MARQUES, J. C., FERRARI, S. F., GORDO, M., GUEDES, P. G., LOPES, M. A., OPAZO, J. C., PORT-CARVALHO, M., DOS SANTOS, R. R., SOARES, R. F., SPIRONELLO, W. R., VEIGA, L. M., VIEIRA, T. M. & BOYLE, S. A. In press. A proposal for the common names for species of Chiropotes (Pitheciinae: Primates). Zootaxa.Google Scholar
BERG, K. S., SOCOLA, J. & ANGEL, R. R. 2007. Green macaws and the annual cycle of their food plants in Ecuador. Journal of Field Ornithology 78:1–10.CrossRefGoogle Scholar
BONVICINO, C. R., BOUBLI, J. P., OTAZÚ, I. B., ALMEIDA, F. C., NASCIMENTO, F. F., COURA, J. R. & SEUÁNEZ, H. N. 2003. Morphologic, karyotypic, and molecular evidence of a new form of Chiropotes (Primates, Pitheciinae). American Journal of Primatology 61:123–133.CrossRefGoogle ScholarPubMed
BOUBLI, J. P. 1999. Feeding ecology of black-headed uacaris (Cacajao melanocephalus melanocephalus) in the Pico de Neblina National Park, Brazil. International Journal of Primatology 20:719–749.CrossRefGoogle Scholar
BOUBLI, J. P., DA SILVA, M. N. F., AMADO, M. V., HRBEK, T., PONTUAL, F. B. & FARIAS, I. P. 2008. A taxonomic reassessment of Cacajao melanocephalus Humboldt (1811), with the description of two new species. International Journal of Primatology 29:723–741.CrossRefGoogle Scholar
BOYLE, S. A. & SMITH, A. T. 2010. Behavioral modifications in northern bearded saki monkeys (Chiropotes satanas chiropotes) in forest fragments of central Amazonia. Primates 51:43–51.CrossRefGoogle ScholarPubMed
BOYLE, S. A., LOURENÇO, W. C., DA SILVA, L. R. & SMITH, A. T. 2009. Travel and spatial patterns change when northern bearded saki monkeys (Chiropotes satanas chiropotes) live in forest fragments. International Journal of Primatology 30:515–531.CrossRefGoogle Scholar
BOYLE, S. A., ZARTMAN, C. E., SPIRONELLO, W. R. & SMITH, A. T. 2012. Implications of habitat fragmentation on the diet of bearded saki monkeys in central Amazonian forest. Journal of Mammalogy 93:1–18.CrossRefGoogle Scholar
BUSTAMENTE, R. O., SIMONETTI, J. A. & MELLA, J. E. 1992. Are foxes legitimate and efficient seed dispersers? A field test. Acta Oecologia 13:203–208.Google Scholar
BUTLER, L. H., HAY, R. F., ELLIS, R. H. & SMITH, R. D. 2009. Post-abscission, pre-dispersal seeds of Digitalis purpurea remain in a developmental state that is not terminated by desiccation ex planta. Annals of Botany 103:785–794.CrossRefGoogle Scholar
CHAMBERS, J. C. & MACMAHON, J. A. 1994. A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Annual Review of Ecology and Systematics 25:263–292.CrossRefGoogle Scholar
CHAVES, O. M., STONER, K. E., ARROYO-RODRÍGUEZ, V. & ESTRADA, A. 2010. Effectiveness of spider monkeys (Ateles geoffroyi vellerosus) as seed dispersers in continuous and fragmented rain forests in Southern Mexico. International Journal of Primatology 32:177–192.CrossRefGoogle Scholar
CORREA, S. B., WINEMILLER, K. O., LÓPEZ-HÉRNANDEZ, H. & GALETTI, M. 2007. Evolutionary perspectives on seed consumption and dispersal by fishes. Bioscience 57:748–756.CrossRefGoogle Scholar
DE FIGUEIREDO, R. A. 1993. Ingestion of Fícus enormis seeds by howler monkeys (Alouatta fusca) in Brazil: effects on seed germination. Journal of Tropical Zoology 9:541–543.Google Scholar
DE STEVEN, D. & PUTZ, F. E. 1984. Impact of mammals on early recruitment of a tropical tree canopy tree, Dipteryx panamenensis, in Panama. Oikos 43:207–216.CrossRefGoogle Scholar
FENNER, M. & THOMPSON, K. 2004. The ecology of seeds. Cambridge University Press, Cambridge. 263 pp.Google Scholar
GALETTI, M. 1997. Seasonal abundance and foraging of parrots and parakeets in a lowland Atlantic forest of Brazil. Ararajuba 5:169–174.Google Scholar
GALETTI, M., KEUROGHLIAN, A., HANADA, L. & MORATO, M. I. 2001. Frugivory and dispersal by the lowland tapir (Tapirus terrestris) in southeast Brazil. Biotropica 33:723–726.CrossRefGoogle Scholar
GENTRY, A. H. 1993. A field guide to the families and genera of woody plants of Northwest South America (Colombia, Ecuador, Peru) with supplementary notes. University of Chicago Press, Chicago. 895 pp.Google Scholar
GOULDING, M., LEAL CARVALHO, M. & FERREIRA, E. G. 1988. Rio Negro, rich life in poor water: Amazonian diversity and foodchain ecology as seen through fish communities. SBP Academic Publishing, The Hague. 200 pp.Google Scholar
GRAFTON, B. W., NORCONK, M. N. & RAGHANTI, M. A. 2002. Seed dispersal by the white-faced saki (Pithecia pithecia), a neotropical seed predator. American Journal of Primatology 57 (Suppl 1):42.Google Scholar
HEANEY, L. R. 1978. Ecology of Neotropical red-tailed squirrels, Sciurus granatensis, in the Panama Canal Zone. Journal of Mammalogy 59:846–851.CrossRefGoogle Scholar
HERSHKOVITZ, P. 1985. A preliminary taxonomic review of the South American bearded saki monkeys genus Chiropotes (Cebidae, Platyrrhini), with the description of a new subspecies. Fieldiana (Zool.) 27:1–46.Google Scholar
HERSHKOVITZ, P. 1987. Uacaris. New World monkeys of the genus Cacajao (Cebidae, Platyrrhini): a preliminary taxonomic review with a description of a new sub-species. American Journal of Primatology 12:1–53.CrossRefGoogle Scholar
HOWE, H. F. 1989. Scatter- and clump-dispersal by birds and mammals and seedling demography: hypothesis and implications. Oecologia 79:417–426.CrossRefGoogle Scholar
JANZEN, D. H. 1971. Seed predation by animals. Annual Review of Ecology and Systematics 2:465–492.CrossRefGoogle Scholar
JORGE, M. S. P. & PERES, C. A. 2005. Population density and home range size of red-rumped agoutis (Dasyprocta leporina) within and outside a natural Brazil nut stand in southeastern Amazonia. Biotropica 37:317–321.CrossRefGoogle Scholar
JULLIOT, C. 1997. Impacts of seed dispersal by red howler monkeys Alouatta seniculus on the seedling population in the understory of tropical rain forest. Journal of Ecology 85:431–440.CrossRefGoogle Scholar
KINZEY, W. G. 1992. Dietary and dental adaptations in the Pitheciinae. American Journal of Physical Anthropology 88:499–514.CrossRefGoogle ScholarPubMed
KINZEY, W. G. & NORCONK, M. A. 1990. Hardness as a basis of fruit choice in two sympatric primates. American Journal of Physical Anthropology 81:5–15.CrossRefGoogle ScholarPubMed
KONÉ, I., LAMBERT, J. E., REFISCH, J. & BAKAYOKO, A. 2008. Primate seed dispersal and its potential role in maintaining useful tree species in the Taï region, Côte-d'Ivoire: implications for the conservation of forest fragments. Tropical Conservation Science 1:293–306.CrossRefGoogle Scholar
KUBITZKI, K. & ZIBURSKI, A. 1994. Seed dispersal in flood plain forests of Amazonia. Biotropica 26:30–43.CrossRefGoogle Scholar
LAMBERT, J. E. & GARBER, P. A. 1998. Evolutionary and ecological implications of primate seed dispersal. American Journal of Primatology 45:9–28.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
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
MOSES, K. & SEMPLE, S. 2011. Primary seed dispersal by the black-and-white ruffed lemur (Varecia variegata) in the Manombo forest, south-east Madagascar. Journal of Tropical Ecology 27:1–10.CrossRefGoogle Scholar
NORCONK, M. A. 2011. Sakis, uakaris, and titi monkeys: behavioral diversity in a radiation of primate seed predators. Pp. 122–139 in Campbell, C. J., Fuentes, A., MacKinnon, K. C., Bearder, S. K. & Stumpf, R. M. (eds.). Primates in perspective. Second edition. Oxford University Press, New York.Google Scholar
NORCONK, M. A., GRAFTON, B. W. & CONKLIN-BRITTAIN, N. L. 1998. Seed dispersal by Neotropical seed predators. American Journal of Primatology 45:103–126.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
PAROLIN, P. 2000. Submergence tolerance vs. escape from submergence: two strategies of seedling establishment in Amazonian floodplains. Environmental and Experimental Botany 48:177–186.CrossRefGoogle Scholar
PAROLIN, P. 2001. Seed germination and early establishment in 12 tree species from nutrient-rich and nutrient-poor Central Amazonian floodplains. Aquatic Botany 70:89–103.CrossRefGoogle Scholar
PAROLIN, P., DE SIMONE, O., HAAS, K., WALDHOFF, D., ROTTENBERGER, S., KUHN, U., KESSELMEIER, J., KLEISS, B., SCHMIDT, W., PIEDADE, M. T. F. & JUNK, W. J. 2004. Central Amazonian floodplain forests: tree adaptations in a pulsing system. Botanical Review 70:357–380.CrossRefGoogle Scholar
PARROTA, J. A., FRANCIS, J. K. & ALMEIDA, R. R. 1995. The trees of the Tapajós: a photographic guide. General technical report IITF-1. Department of Agriculture, Forestry Service. International Institute of Tropical Forestry, Rio Piedras. 370 pp.Google Scholar
PASCHOAL, M. 1995. Seasonal food use by the neotropical squirrel Sciurus ingrami in southeastern Brazil. Biotropica 27:268–273.CrossRefGoogle Scholar
PÉREZ-EMÁN, J. L. & PAOLILLO, A. 1997. Diet of the pelomedusid turtle Peltocephalus dumerilianus in the Venezuelan Amazon. Journal of Herpetology 31:173–179.CrossRefGoogle Scholar
PINTO, L. P. 2008. Ecologia alimentar do cuxiú-de-nariz-vermelho Chiropotes albinasus (Primates: Pitheciidae) na Floresta Nacional do Tapajós, Pará. PhD dissertation, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, Brazil.Google Scholar
POULSEN, J. R., CLARK, C. J. & SMITH, T. B. 2001. Seed dispersal by a diurnal primate community in the Dja Reserve, Cameroon. Journal of Tropical Ecology 17:787–808.CrossRefGoogle Scholar
PRANCE, G. T. 1979. Notes on the vegetation types of Amazonia III – the terminology of Amazonian forest types subject to inundation. Brittonia 31:26–38.CrossRefGoogle Scholar
RENTON, K. 2006. Diet of adult and nestling scarlet macaws in southwest Belize, Central America. Biotropica 38:280–283.CrossRefGoogle Scholar
RIBEIRO, S. J. E. L., HOPKINS, M. J. G., VICENTINI, A., SOTHERS, C. A., DA COSTA, S. M. A., DE BRITO, J. M., DE SOUZA, M. A. D., MARTINS, L. H. P., LOHMANN, L. G., ASSUNÇÃO, P. A. C. L., DA PEREIRA, C. E., DA SILVA, C. F., MESQUITA, M. R. & PROCÓPIO, L. C. 1999. Flora da Reserva Ducke: guia de identificação das plantas vasculares de uma floresta de terra firme na Amazonia Central. DFID-Instituto Nacional de Pesquisas da Amazônia, Manaus. 799 pp.Google Scholar
RIOS, R. S. & PACHECO, L. F. 2006. The effect of dung and dispersal on post-dispersal seed predation of Attalea phalerata (Arecaceae) by bruchid beetles. Biotropica 38:778–781.CrossRefGoogle Scholar
ROSENBERGER, A. L. 1992. Evolution of feeding niches in New World monkeys. American Journal of Physical Anthropology 88:525–562.CrossRefGoogle ScholarPubMed
SALM, R. 2006. Invertebrate and vertebrate seed predation in the Amazonian palm Attalea maripa. Biotropica 38:558–560.CrossRefGoogle Scholar
SCHUPP, E. W. 1993. Quantity, quality, and the effectiveness of seed dispersal by animals. Vegetatio 107/108:15–29.CrossRefGoogle Scholar
SCHUPP, E., JORDANO, P. & MARIA GOMEZ, J. 2010. Seed dispersal effectiveness revisited: a conceptual review. New Phytologist 188:333–353.CrossRefGoogle ScholarPubMed
SIMÃO, I., DOS SANTOS, F. A. M. & PIZO, M. A. 1997. Vertical stratification and diet of psitticids in a lowland tropical forest of Brazil. Ararajuba 5:169–174.Google Scholar
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
VALLEJO-MARÍN, M., DOMÍNGUEZ, C. A. & DIRZO, R. 2006. Simulated seed predation reveals a variety of germination responses of neotropical rain forest species. American Journal of Botany 93:369–376.CrossRefGoogle ScholarPubMed
VAN ROOSMALEN, M. G. M. 1985. Fruits of the Guyana flora. University of Utrecht Press, Utrecht. 483 pp.Google Scholar
VÁZQUEZ-YANES, C. & OROZCO-SEGOVIA, A. 1993. Patterns of seed longevity and germination in the tropical rainforest. Annual Review of Ecology and Systematics 24:69–87.CrossRefGoogle Scholar
VEIGA, L. M. 2006. Ecologia e comportamento do cuxiú-preto (Chiropotes satanas) na paisagem fragmentada da Amazônia Oriental. PhD dissertation, Department of Experimental Psychology, Universidade Federal do Pará, Belém, Brazil.Google Scholar
ZHANG, S. Y. 1995. Fruit consumption and seed dispersal of Ziziphus cinamomum (Rhamnaceae) by two sympatric primates (Cebus apella and Ateles paniscus) in French Guiana. Biotropica 27:397–401.CrossRefGoogle Scholar