Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-22T15:37:16.609Z Has data issue: false hasContentIssue false

Seed dispersal of the Brazil nut tree (Bertholletia excelsa) by scatter-hoarding rodents in a central Amazonian forest

Published online by Cambridge University Press:  30 March 2010

Joanne M. Tuck Haugaasen
Affiliation:
Laboratório de Genética e Biologia Reprodutiva de Plantas, Coordenação de Pesquisas em Botânica, Instituto Nacional de Pesquisas da Amazonia, Caixa Postal 478, Manaus, Amazonas State, Brazil
Torbjørn Haugaasen*
Affiliation:
Norwegian University of Life Sciences, Department of Ecology and Natural Resource Management, P.O. Box 5003, 1432 Ås, Norway Centre for Ecology, Evolution and Conservation, School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, UK
Carlos A. Peres
Affiliation:
Centre for Ecology, Evolution and Conservation, School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, UK
Rogerio Gribel
Affiliation:
Laboratório de Genética e Biologia Reprodutiva de Plantas, Coordenação de Pesquisas em Botânica, Instituto Nacional de Pesquisas da Amazonia, Caixa Postal 478, Manaus, Amazonas State, Brazil
Per Wegge
Affiliation:
Norwegian University of Life Sciences, Department of Ecology and Natural Resource Management, P.O. Box 5003, 1432 Ås, Norway
*
1Corresponding author. Emails: [email protected]; [email protected]

Abstract:

We know surprisingly little about the fate of seeds of the Brazil nut tree (Bertholletia excelsa) under natural conditions. Here we investigate seed removal, predation and caching of Brazil nuts by scatter-hoarding rodents in the wet and dry seasons, based on an experimental approach using 900 thread-marked seeds. We tracked the fate of seeds handled by these animals to examine how seasonal food availability may influence caching rates, dispersal distances and cache longevity. Most seeds exposed to dispersal trials were removed by scatter-hoarders during the first week in both seasons and seeds were generally buried intact in single-seeded caches within 10 m of seed stations. Seeds were removed significantly faster and buried at greater distances during the dry season. The proportion of seeds buried intact was considerably higher in the wet season (74.4%) than in the dry season (38.2%). Most (99.4%) of the 881 primary caches monitored were recovered, but these had a significantly shorter lifetime in the dry season. Our results show that rodents are highly skilled at retrieving buried Brazil nuts and that caching behaviour appears to be affected by seasonal resource abundance. Reduced seed availability due to intensive harvest could potentially create a dry-season scenario where most seeds succumb to pre-dispersal predation, thereby adversely affecting the natural regeneration of Brazil nut trees.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2010

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

ASQUITH, N. M., TERBORGH, J., ARNOLD, A. E. & MAILÉN RIVEROS, C. 1999. The fruits the agouti ate: Hymenaea courbaril seed fate when its disperser is absent. Journal of Tropical Ecology 15:229235.CrossRefGoogle Scholar
BAIDER, C. 2000. Demografia e ecologia de dispersão de frutos de Bertholletia excelsa Humb. & Bonpl. (Lecythidaceae) em castanhais silvestres da Amazônia oriental. PhD thesis, University of São Paulo.Google Scholar
BOUWMAN, M. & VAN DIJK, S. 1999. Removal and fate of Brazil nut seeds (Bertholletia excelsa) exposed in two contrasting seed densities in a Bolivian moist forest. M.Sc. thesis, Utrecht University.Google Scholar
CHAPMAN, C. A., WRANGHAM, R. W., CHAPMAN, L. J., KENNARD, D. K. & ZANNE, A. E. 1999. Fruit and flower phenology at two sites in Kibale National Park, Uganda. Journal of Tropical Ecology 15:189211.CrossRefGoogle Scholar
CHAUVET, S., FEER, F. & FORGET, P.-M. 2004. Seed fates of two Sapotaceae species in a Guianan rain forest in the context of escape and satiation hypothesis. Journal of Tropical Ecology 20:19.CrossRefGoogle Scholar
DAUSMANN, K. H., GLOS, J., GANZHORN, J. U. & HELDMAIER, G. 2005. Hibernation in the tropics: lessons from a primate. Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology 175:147155.CrossRefGoogle ScholarPubMed
DINIZ, T. D. A. S. & BASTOS, T. X. 1974. Contribuição ao conhecimento do clima típico da castanha do Brasil. Boletin Técnico IPEAN 64:5971.Google Scholar
DUBOST, G. 1988. Ecology and social life of the red acouchi, Myoprocta exilis: a comparison with the orange-rumped agouti, Dasyprocta leporina. Journal of Zoology 214:107123.CrossRefGoogle Scholar
DUBOST, G. & HENRY, O. 2006. Comparison of diets of the acouchy, agouti and paca, the three largest terrestrial rodents of French Guianan forests. Journal of Tropical Ecology 22:641651.CrossRefGoogle Scholar
FORGET, P.-M. 1990. Seed dispersal of Vouacapoua americana (Caesalpiniaceae) by caviomorph rodents in French Guiana. Journal of Tropical Ecology 6:459468.CrossRefGoogle Scholar
FORGET, P.-M. 1991. Scatterhoarding of Astrocaryum paramaca by Proechimys in French Guiana: comparison with Myoprocta exilis. Tropical Ecology 32:155167.Google Scholar
FORGET, P.-M. 1992. Seed removal and seed fate in Gustavia superba (Lecythidaceae). Biotropica 24:408414.CrossRefGoogle Scholar
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 12:751761.CrossRefGoogle Scholar
FORGET, P.-M. & JANSEN, P. A. 2007. Hunting increases dispersal limitation in the tree Carapa procera, a nontimber forest product. Conservation Biology 21:106113.CrossRefGoogle ScholarPubMed
FORGET, P.-M. & MILLERON, T. 1991. Evidence for secondary seed dispersal by rodents in Panama. Oecologia 87:596599.CrossRefGoogle ScholarPubMed
FORGET, P.-M. & WENNY, D. G. 2005. How to elucidate seed fate? A review of methods used to study seed removal and secondary dispersal. Pp. 379393 in Forget, P.-M., Lambert, J., Hulme, P. E. & Vander Wall, S. B. (eds.). Seed fate: seed predation, seed dispersal and seedling establishment. CABI Publishing, Wallingford.Google Scholar
FORGET, P.-M., MILLERON, T. & FEER, F. 1998. Patterns in post-dispersal seed removal by neotropical rodents and seed fate in relation to seed size. Pp. 2547 in Newbery, D. M., Brown, N. & Prins, H. H. T. (eds.). Dynamics of tropical communities. Blackwell Science, Oxford.Google Scholar
FORGET, P.-M., HAMMOND, D., MILLERON, T. & THOMAS, R. 2002. Seasonality of fruiting and food hoarding by rodents in Neotropical forests: consequences for seed dispersal and seedling recruitment. Pp. 241253 in Levey, D. J., Silva, W. R. & Galetti, M. (eds.). Seed dispersal and frugivory: ecology, evolution and conservation. CABI Publishing, Wallingford.Google Scholar
FOSTER, R. B. 1982. The seasonal rhythm of fruit fall on Barro Colorado Island. Pp. 151172 in Leigh, E. G., Rand, A. S. & Windsor, D. M. (eds.). The ecology of a tropical forest: seasonal rhythms and long-term changes. Smithsonian Institutional Press, Washington D.C.Google Scholar
FRANKIE, G. W., BAKER, H. G. & OPLER, P. A. 1974. Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. Journal of Ecology 62:881919.CrossRefGoogle Scholar
GANZHORN, J. U., KLAUS, S., ORTMANN, S. & SCHMID, J. 2003. Adaptations to seasonality: some primate and non-primate examples. Pp. 132148 in Kappeler, P. M. & Pereira, M. E. (eds.). Primate life histories and socioecology. University of Chicago Press, Chicago.Google Scholar
HALLWACHS, W. 1986. Agoutis (Dasyprocta punctata): the inheritors of guapinol (Hymenaea courbaril: Leguminosae). Pp. 285304 in Estrada, A. & Fleming, T. H. (eds.). Frugivores and seed dispersal. Dr W. Junk Publishers, Dordrecht.CrossRefGoogle Scholar
HAMMOND, D. S. & BROWN, V. K. 1998. Disturbance, phenology and life-history characteristics: factors influencing frequency-dependent attack on tropical seed and seedlings. Pp. 5178 in Newbery, D. M., Brown, N. & Prins, H. H. T. (eds.). Dynamics of tropical communities. Blackwell Science, Oxford.Google Scholar
HAUGAASEN, T. & PERES, C. A. 2005. Tree phenology in adjacent Amazonian flooded and unflooded forests. Biotropica 37:620630.CrossRefGoogle Scholar
HAUGAASEN, T. & PERES, C. A. 2006. Floristic, edaphic and structural characteristics of flooded and unflooded forests in the lower Purús region of central Amazônia, Brazil. Acta Amazonica 36:2536.CrossRefGoogle Scholar
HAUGAASEN, T. & PERES, C. A. 2007. Vertebrate responses to plant phenology in Amazonian flooded and unflooded forest. Biodiversity and Conservation 16:41654190.CrossRefGoogle Scholar
HENRY, O. 1999. Frugivory and the importance of seeds in the diet of orange-rumped agouti (Dasyprocta leporina) in French Guiana. Journal of Tropical Ecology 15:291300.CrossRefGoogle Scholar
JANSEN, P. A. & FORGET, P.-M. 2001. Scatterhoarding rodents and tree regeneration. Pp. 275288 in Bongers, F., Charles-Dominique, P., Forget, P.-M. & Théry, M. (eds.). Noruages: dynamics and plant-animal interactions in a neotropical rainforest. Kluwer Academic Publishers, Dordrecht.Google Scholar
JANSEN, P. A., BARTHOLOMEUS, M., BONGERS, F., ELZINGA, J. A., DEN OUDEN, J. & VAN WIEREN, S. E. 2002. The role of seeds size in dispersal by a scatter-hoarding rodent. Pp. 209225 in Levey, D. J., Silva, W. R. & Galetti, M. (eds.). Seed dispersal and frugivory: ecology, evolution and conservation. CABI Publishing, Wallingford.Google Scholar
JANSEN, P. A., BONGERS, F. & HEMERIK, L. 2004. Seed mass and mast seeding enhance dispersal by a neotropical scatter-hoarding rodent. Ecological Monographs 74:569589.CrossRefGoogle Scholar
JANSEN, P. A., BONGERS, F. & PRINS, H. H. T. 2006. Tropical rodents change rapidly germinating seeds into long-term food supplies. Oikos 113:449458.CrossRefGoogle Scholar
JANSEN, P. A., BONGERS, F. & Van Der MEER, P. J. 2008. Is farther seed dispersal better? Spatial patterns of offspring mortality in three rainforest tree species with different dispersal abilities. Ecography 31:4352.CrossRefGoogle Scholar
JANZEN, D. H. 1971. Seed predation by animals. Annual Review of Ecology and Systematics 2:465492.CrossRefGoogle Scholar
JORGE, M. L. & 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 37:317321.CrossRefGoogle Scholar
KAINER, K. A., MATOS MALAVASI, M., DURYEA, M. L. & DA SILVA, A. R. 1999. Brazil nut (Bertholletia excelsa) seed characteristics, preimbibition and germination. Seed Science and Technology 27:731745.Google Scholar
KAINER, K. A., WADT, L. H. O. & STAUDHAMMER, C. L. 2007. Explaining variation in Brazil nut fruit production. Forest Ecology and Management 250:244255.CrossRefGoogle Scholar
KILTIE, R. A. 1981. Distribution of palm fruits on a rain forest floor: why white-lipped peccaries forage near objects. Biotropica 13:141145.CrossRefGoogle Scholar
LEVEY, D. J. 1988. Spatial and temporal variation in Costa Rican fruit and fruit-eating bird abundance. Ecological Monographs 58:251269.CrossRefGoogle Scholar
LOISELLE, B. A., & BLAKE, J. G. 1991. Temporal variation in birds and fruits along an elevational gradient in Costa Rica. Ecology 72:180193.CrossRefGoogle Scholar
MILLER, C. J. 1990. Natural history, economic botany, and germplasm conservation of the Brazil nut tree (Bertholletia excelsa Humb and Bonpl.). M.Sc. thesis, University of Florida, Gainesville.Google Scholar
MORI, S. A. & PRANCE, G. T. 1990. Taxonomy, ecology and economic botany of the Brazil nut (Bertholletia excelsa Humb. and Bonpl.: Lecythidaceae). Advances in Economic Botany 8:130150.Google Scholar
MÜLLER, C. H. 1981. Castanha-do-Brasil: estudos agronomicos. Documentos 1:125.Google Scholar
MÜLLER, C. H., RODRIGUES, I. A., MÜLLER, A. A. & MÜLLER, N. R. M. 1980. Castanha do Brasil: resultados de pesquisas. Miscelânia 2:125.Google Scholar
PERES, C. A. 1991. Seed predation of Cariniana micrantha (Lecythidaceae) by brown capuchin monkeys in central Amazonia. Biotropica 23:262270.CrossRefGoogle Scholar
PERES, C. A. 2000. Identifying keystone plant resources in tropical forests: the case of gums from Parkia pods. Journal of Tropical Ecology 16:287317.CrossRefGoogle Scholar
PERES, C. A. & BAIDER, C. 1997. Seed dispersal, spatial distribution and population structure of Brazil nut trees (Bertholletia excelsa) in southeastern Amazonia. Journal of Tropical Ecology 13:595616.CrossRefGoogle Scholar
PERES, C. A., SCHIESARI, L.C. & DIAS-LEME, C.L. 1997. Vertebrate predation of Brazil-nuts (Bertholletia excelsa, Lecythidaceae), an agouti-dispersed Amazonian seed crop: a test of the escape hypothesis. Journal of Tropical Ecology 13:6979.CrossRefGoogle Scholar
PERES, C. A., BAIDER, C., ZUIDEMA, P. A., WADT, L. H. O., KAINER, K. A., GOMES-SILVA, D. A. P., SALOMAO, R. P., SIMOES, L. L., FRANCIOSI, E. R. N., VALVERDE, F. C., GRIBEL, R., SHEPARD, G. H., KANASHIRO, M., COVENTRY, P., YU, D. W., WATKINSON, A. R. & FRECKLETON, R. P. 2003. Demographic threats to the sustainability of Brazil nut exploitation. Science 302:21122114.CrossRefGoogle Scholar
SMYTHE, N. 1970. Relationships between fruiting seasons and seed dispersal methods in a neotropical forest. American Naturalist 104:2535.CrossRefGoogle Scholar
SMYTHE, N. 1978. The natural history of the Central American agouti (Dasyprocta punctata). Smithsonian Contributions to Zoology 257:152.CrossRefGoogle Scholar
STAPANIAN, M. A. & SMITH, C. C. 1978. A model for seed scatterhoarding: coevolution of fox squirrels and black walnuts. Ecology 59:884896.CrossRefGoogle Scholar
VANDER WALL, S. B. 1990. Food hoarding in animals. University of Chicago Press, Chicago. 445 pp.Google Scholar
VANDER WALL, S. B. 1991. Mechanisms of cache recovery in yellow chipmunks. Animal Behavior 41:851863.CrossRefGoogle Scholar
VANDER WALL, S. B. 2002. Secondary dispersal of Jeffrey Pine seeds by rodent scatter-hoarders: the role of pilfering, reaching and a variable environment. Pp. 193208 in Levey, D. J., Silva, W. R. & Galetti, M. (eds.). Seed dispersal and frugivory: ecology, evolution and conservation. CABI Publishing, Wallingford.Google Scholar
VANDER WALL, S. B. 2003. Effects of seed size of wind-dispersed pines (Pinus) on secondary seed dispersal and the caching behaviour of rodents. Oikos 100:2534.CrossRefGoogle Scholar
WADT, L. H. O., KAINER, K. A. & GOMES-SILVA, D. A. P. 2005. Population structure and nut yield of a Bertholletia excelsa stand in Southwestern Amazonia. Forest Ecology and Management 211:371384.CrossRefGoogle Scholar
WATSON, W. 1901. Germination of seeds of Bertholletia excelsa. Annals of Botany 15:99102.CrossRefGoogle Scholar
WHITE, L. J. T. 1994. Patterns of fruit-fall phenology in the Lope Reserve, Gabon. Journal of Tropical Ecology 10:289312.CrossRefGoogle Scholar
WILLSON, M. F. 1992. The ecology of seed dispersal. Pp. 6185 in Fenner, M. (ed.). The ecology of regeneration in plant communities. CABI Publishing, Wallingford.Google Scholar
XIAO, Z., JANSEN, P. A. & ZHANG, Z. 2006. Using seed-tagging methods for assessing post-dispersal seed fate in rodent-dispersed trees. Forest Ecology and Management 223:1823.CrossRefGoogle Scholar
ZUIDEMA, P. A. 2003. Demography and management of the Brazil nut tree (Bertholletia excelsa). PROMAB Scientific series 6. Utrecht University, the Netherlands. 112 pp.Google Scholar