Hostname: page-component-8448b6f56d-c47g7 Total loading time: 0 Render date: 2024-04-25T02:54:28.863Z Has data issue: false hasContentIssue false

Control of Carapa guianensis phenology and seed production at multiple scales: a five-year study exploring the influences of tree attributes, habitat heterogeneity and climate cues

Published online by Cambridge University Press:  08 December 2011

Christie A. Klimas*
Affiliation:
School of Forest Resources and Conservation, University of Florida, Gainesville, FL 32611, USA DePaul University Environmental Science Program, Chicago, IL 60614, USA
Karen A. Kainer
Affiliation:
School of Forest Resources and Conservation, University of Florida, Gainesville, FL 32611, USA Center for Latin American Studies, Tropical Conservation and Development Program, University of Florida, Gainesville, FL 32611, USA
Lúcia H. Wadt
Affiliation:
Embrapa (The Brazilian Agricultural Research Corporation) Acre, BR 364, Km 14, Rio Branco, Acre, 69901-108Brazil
Christina L. Staudhammer
Affiliation:
School of Forest Resources and Conservation, University of Florida, Gainesville, FL 32611, USA
Valéria Rigamonte-Azevedo
Affiliation:
UFAC (Federal University of Acre) Campus Universitário Rodovia BR 364, Km 4 n. 6637 Rio Branco, Acre, 69915-900Brazil
Manoel Freire Correia
Affiliation:
Embrapa (The Brazilian Agricultural Research Corporation) Acre, BR 364, Km 14, Rio Branco, Acre, 69901-108Brazil
Lílian Maria da Silva Lima
Affiliation:
CNPq Fellow, Embrapa Acre, BR 364, Km 14, Rio Branco, Acre, 69901-108Brazil
*
1Corresponding author. Present address: Environmental Science Program, McGowan South 203, 1110 W Belden Ave, Chicago, IL 60614, USA. Email: cklimas@depaul.edu

Abstract:

During 5 y, we monitored reproductive activity and seed production of Carapa guianensis in two forest types to test the hypothesis that seed production is influenced by multiple factors across scales (regional climatic cues, local habitat heterogeneity and individual tree attributes). Variability in seed production was moderate at the population (CVp = 1.25) and individual level (xCVi = 1.24). A mixed model with a Poisson regression revealed that seed production was explained by variables at all scales. Total seed production was significantly higher in occasionally inundated forests. Diameter at breast height, dbh2, crown cross-sectional area, liana load, density, dry-season rainfall and mean maximum temperature were also significant in explaining seed production variation. Seed production increased with dbh until 40–50 cm, then decreased. Liana load demonstrated a negative relationship with seed production, but only in terra firme forests. Climatic cues (rainfall and temperature parameters) were central to setting overall patterns in reproductive activity and seemed to best explain why years with high seed production were consistent across the two forest types (habitats) examined. Dry-season rainfall was positively correlated with seed production.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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

AGREN, J. 1996. Population size, pollinator limitation, and seed set in the self-incompatible herb Lythrum salicaria. Ecology 77:17791790.CrossRefGoogle Scholar
ASHTON, P. S., GIVNISH, T. J. & APPANAH, S. 1988. Staggered flowering in the Dipterocarpaceae: new insights into floral induction and the evolution of mast fruiting in the aseasonal tropics. American Naturalist 132:4466.CrossRefGoogle Scholar
BEVAN, S. L., NORTH, P. R. J., GREY, W. M. F., LOS, O. & PLUMMER, S. E. 2009. Impact of atmospheric aerosol from biomass burning on Amazon dry-season drought. Journal of Geophysical Research 114:D09204. doi:10.1029/2008JD011112.CrossRefGoogle Scholar
BORCHERT, R. 1980. Phenology and ecophysiology of tropical trees: Erythrina poeppigiana O.F. Cook. Ecology 61:10651074.CrossRefGoogle Scholar
BORCHERT, R. 1994. Water storage in soil or tree stems determines phenology and distribution of tropical dry forest trees. Ecology 75:14371449.CrossRefGoogle Scholar
BORCHERT, R., RIVERA, G. & HAGNAUER, W. 2002. Modification of vegetative phenology in a tropical semi-deciduous forest by abnormal drought and rain. Biotropica 34:2739.Google Scholar
BORCHERT, R., MEYER, S. A., FLEGER, R. S. & PORTER-BOLLAND, L. 2004. Environmental control of flowering periodicity in Costa Rican and Mexican tropical dry forests. Global Ecology and Biogeography 13:409425.CrossRefGoogle Scholar
BRUNA, E. M., KRESS, W. J., MARQUES, F. & DA SILVA, O. F. 2004. Heliconia acuminata reproductive success is independent of local floral density. Acta Amazonica 34:467471.CrossRefGoogle Scholar
BURD, M. 1994. Bateman's principle and plant reproduction: the role of pollen limitation in fruit and seed set. Botanical Review 60:83139.CrossRefGoogle Scholar
CHAPMAN, C. A., CHAPMAN, L. J., STRUHSAKER, T. T., ZANNE, A. E., CLARK, C. J. & POULSEN, J. R. 2005. A long-term evaluation of fruiting phenology: importance of climate change. Journal of Tropical Ecology 21:3145.CrossRefGoogle Scholar
CLARK, D. A. & CLARK, D. B. 1990. Distribution and effects on tree growth of lianas and woody hemiepiphytes in a Costa Rican tropical wet forest. Journal of Tropical Ecology 6:321331.CrossRefGoogle Scholar
CLOUTIER, D., KANASHIRO, M., CIAMPI, A. Y. & SCHOEN, D. J. 2007a. Impact of selective logging on inbreeding and gene dispersal in an Amazonian tree population of Carapa guianensis Aubl. Molecular Ecology 16:797809.CrossRefGoogle Scholar
CLOUTIER, D., HARDY, O. J., CARON, H., CIAMPI, A. Y., DEGEN, B., KANASHIRO, M. & SCHOEN, D. J. 2007b. Low inbreeding and high pollen dispersal distances in populations of two Amazonian forest tree species. Biotropica 39:406415.CrossRefGoogle Scholar
COX, P. M., HARRIS, P. P., HUNTINGFORD, C., BETTS, R. A., COLLINS, M., JONES, C. D., JUPP, T. E., MARENGO, J. A. & NOBRE, C. A. 2008. Increasing risk of Amazonian drought due to decreasing aerosol pollution. Nature 453:212215.CrossRefGoogle ScholarPubMed
DÍAZ, M. & GRANADILLO, E. 2005. The significance of episodic rains for reproductive phenology and productivity of trees in semiarid regions of northwestern Venezuela. Trees – Structure and Function 19:336348.CrossRefGoogle Scholar
ELZINGA, J. A., ATLAN, A., BIERE, A., GIGORD, L., WEIS, A. E. & BERNASCONI, G. 2007. Time after time: flowering phenology and biotic interactions. Trends in Ecology and Evolution 22:432439.CrossRefGoogle ScholarPubMed
FEINSINGER, P., TIEBOUT, H. M. & YOUNG, B. E. 1991. Do tropical bird-pollinated plants exhibit density-dependent interactions? Field experiments. Ecology 72:19531963.CrossRefGoogle Scholar
FENNER, M. 1998. The phenology of growth and reproduction in plants. Perspectives in Plant Ecology, Evolution and Systematics 1:7891.CrossRefGoogle Scholar
FERRAZ, I. D. K., CAMARGO, J. L. C. & SAMPAIO, P. T. B. 2002. Sementes e plântulas de andiroba (Carapa guianensis Aubl. e C. procera D.C. – Meliaceae) Aspectos botânicos, ecológicos e tecnológicos. Acta Amazonica 32:661–647.Google Scholar
FORGET, P. M. 1996. Removal of seeds of Carapa procera (Meliaceae) by rodents and their fate in rain forest in French Guiana. Journal of Tropical Ecology 12:751761.CrossRefGoogle Scholar
FOURNIER, L. A. 2003. Species description Carapa guianensis. Pp. 360362 in Vozzo, J. A. (ed.). Tropical tree seed manual. Agricultural Handbook Number 721. USDA Forest Service, Washington DC. 874 pp.Google Scholar
GRAUEL, W. T. & PUTZ, F. E. 2004. Effects of lianas on growth and regeneration of Prioria copaifera in Darien, Panama. Forest Ecology and Management 190:99108.CrossRefGoogle Scholar
GUARIGUATA, M. R., CLAIRE, H. A.-L. & JONES, G. 2002. Tree seed fate in a logged and fragmented forest landscape, Northeastern Costa Rica. Biotropica 34:405415.CrossRefGoogle Scholar
GUEDES, M. C., SOUTO, É. B., CORREA, C. & GOMES, H. S. R. 2008. Produção de sementes e oleo de andiroba (Carapa guianensis Aubl.) em area de várzea do Amapá. Pp. 111119 in Wadt, L. H. O. (ed.). Anais do 1° Seminário do Projeto Kamukaia: Manejo Sustantável de Produtos Florestais Não-madeireiros na Amazônia, Embrapa, Acre, Brazil. 182 pp.Google Scholar
HALL, P., ORRELL, L. C. & BAWA, K. S. 1994. Genetic diversity and mating system in a tropical tree, Carapa guianensis (Meliaceae). American Journal of Botany 81:11041111.CrossRefGoogle Scholar
HARMS, K. E., CONDIT, R., HUBBELL, S. P. & FOSTER, R. B. 2001. Habitat associations of trees and shrubs in a 50-ha neotropical forest plot. Journal of Ecology 89:947959.CrossRefGoogle Scholar
HERRERA, C. M., JORDANO, P., GUITIÁN, J. & TRAVESET, A. 1998. Annual variability in seed production by woody plants and the masting concept: reassessment of principles and relationship to pollination and seed dispersal. American Naturalist 152:576594.CrossRefGoogle ScholarPubMed
HIRAYAMA, D., ITOH, A. & YAMAKURA, T. 2004. Implications from seed traps for reproductive success, allocation and cost in a tall tree species Lindera erythrocarpa. Plant Species Biology 19:185196.CrossRefGoogle Scholar
HUERTE, A. R., DIDAN, K., SHIMABUKURO, Y. E., RATANA, P., SALESKA, S. R., HUTYRA, L. R., YANG, W., Nemani, R. R. & MYNENI, R. 2006. Amazon rainforests green-up with sunlight in dry season. Geophysical Research Letters 33:L06405, doi:10.1029/2005GL025583Google Scholar
IPCC (INTERGOVERNMENTAL PANEL ON CLIMATE CHANGE). 2007. Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the IPCC. Cambridge University Press, Cambridge. 996 pp.Google Scholar
KAINER, K. A., WADT, L. H. O., GOMES-SILVA, D. A. P. & CAPANU, M. 2006. Liana loads and their association with Bertholletia excelsa fruit and nut production, diameter growth and crown attributes. Journal of Tropical Ecology 22:147154.CrossRefGoogle 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
KELLY, D. 1994. The evolutionary ecology of mast seeding. Trends in Ecology and Evolution 9:465470.CrossRefGoogle ScholarPubMed
KELLY, D. & SORK, V. L. 2002. Mast seeding in perennial plants: why, how, where? Annual Reviews of Ecology and Systematics 33:427447.CrossRefGoogle Scholar
KELLY, D., HARRISON, A. L., LEE, W. G., PAYTON, I. J., WILSON, P. R. & SCHAUBER, E. M. 2000. Predator satiation and extreme mast seeding in 11 species of Chionochloa (Poaceae). Oikos 90:477488.CrossRefGoogle Scholar
KILGORE, A., LAMBERS, T. D. & ADLER, G. H. 2010. Lianas influence fruit and seed use by rodents in a tropical forest. Journal of Tropical Ecology 51:143149.Google Scholar
KLIMAS, C. A., KAINER, K. A. & WADT, L. H. O. 2007. Population structure of Carapa guianensis in two forest types in the southwestern Brazilian Amazon. Forest Ecology and Management 250:256265.CrossRefGoogle Scholar
KLIMAS, C. A., KAINER, K. A. & WADT, L. H. O. 2011. The economic value of sustainable seed and timber harvests of multi-use species: an example using Carapa guianensis. Forest Ecology and Management. In press: doi:10.1016/j.foreco.2011.03.006Google Scholar
KÖRNER, C. 2006. Forests, biodiversity and CO2: surprises are certain. Biologist 53:8290.Google Scholar
KOZLOWSKI, T. T. & PALLARDY, S. G. 2002. Acclimation and adaptive responses of woody plants to environmental stresses. Botanical Review 68:270334.CrossRefGoogle Scholar
LEITE, A. M. C. 1997. Ecologia de Carapa guianensis Aublet (Meliaceae) “Andiroba”. PhD dissertation, Instituto Nacional de Pesquisas da Amazônia. Manaus. 181 pp.Google Scholar
LEVIN, S. A. 1992. The problem of pattern and scale in ecology. Ecology 73:19431967.CrossRefGoogle Scholar
LONDRES, M. 2009. Population structure and seed production of Carapa guianensis in three floodplain forest types of the Amazon estuary. M.Sc. thesis, University of Florida, Gainesville 56 pp.Google Scholar
MALHI, Y., ROBERTS, T., BETTS, R. A., KILLEEN, T. J., LI, W. & NOBRE, C. A. 2008. Climate change, deforestation, and the fate of the Amazon. Science 319:169172.CrossRefGoogle ScholarPubMed
MARENGO, J. A., NOBRE, C. A., TOMASELLA, J., OYAMA, M. D., SAMPAIO DE OLIVEIRA, G., DE OLIVEIRA, R., CAMARGO, H., ALVES, L. M. & BROWN, I. F. 2008. The drought of Amazonia in 2005. Journal of Climate 21:495516.CrossRefGoogle Scholar
MAUÉS, M. M. 2006. Estratégias reprodutivas de espécies arbóreas e a sua importância para o manejo e conservação florestal: Floresta Nacional do Tapajós (Belterra-PA). Ph.D. thesis, Universidade de Brasília. Instituto de Ciências Biológicas. Brasília, DF. 206 pp.Google Scholar
MCHARGUE, L. A. & HARTSHORN, G. S. 1983a. Seed and seedling ecology of Carapa guianensis. Turrialba 33:399404.Google Scholar
MCHARGUE, L. A. & HARTSHORN, G. S. 1983b. Carapa guianensis. Pp. 206207 in Janzen, D. H. (ed.). Costa Rican natural history. University of Chicago Press, Chicago.Google Scholar
MORRIS, W. F., PFISTER, C. A., TULJAPURKAR, S., HARIDAS, C. V., BOGGS, C. L., BOYCE, M. S., BRUNA, E. M., CHURCH, D. R., COULSON, T., DOAK, D. F., FORSYTH, S., GAILLARD, J. M., HORVITZ, C. C., KALISZ, S., KENDALL, B. E., KNIGHT, T. M., LEE, C. T. & MENGES, E. S. 2008. Longevity can buffer plant and animal populations against changing climatic variability. Ecology 89:1925.CrossRefGoogle ScholarPubMed
MURRAY, K. G. 1988. Avian seed dispersal of three Neotropical gap-dependent plants. Ecological Monographs 58:271298.CrossRefGoogle Scholar
NABE-NIELSEN, J., KOLLMANN, J. & PEÑA-CLAROS, M. 2009. Effects of liana load, tree diameter and distances between conspecifics on seed production in tropical timber trees. Forest Ecology and Management 257:987993.CrossRefGoogle Scholar
NAITO, Y., KANZAKI, M., NUMATA, S., OBAYASHI, K., KONUMA, A., NISHIMURA, S., OHTA, S., TSUMURA, Y., OKUDA, T., LEE, S. L. & MUHAMMAD, N. 2008. Size-related flowering and fecundity in the tropical canopy tree species, Shorea acuminata (Dipterocarpaceae) during two consecutive flowerings. Journal of Plant Research 121:3342.CrossRefGoogle ScholarPubMed
NEWBERY, D. M., CHUYONG, G. B. & ZIMMERMANN, L. 2006. Mast fruiting of large ectomycorrhizal African rain forest trees: importance of dry season intensity, and the resource-limitation hypothesis. New Phytologist 170:561579.CrossRefGoogle ScholarPubMed
NORGHAUER, J. M., NOCK, C. A. & GROGAN, J. 2011. The importance of tree size and fecundity for wind dispersal of Big-Leaf Mahogany. PLoS One 6:e17488.CrossRefGoogle ScholarPubMed
PENNINGTON, T. D. 2004. Meliaceae. Pp. 243246 in Smith, N., Mori, S. A., Henderson, A., Stevenson, D. W. & Heald, S. V. (ed.). Flowering plants of the Neotropics. Princeton University Press, Princeton.Google Scholar
PHILLIPS, O. L., MARTINEZ, R. V., ARROYO, L., BAKER, T. R., KILLEEN, T., LEWIS, S. L., MALHI, Y., MENDOZA, A. M., NEILL, D., VARGAS, P. N., ALEXIADES, M., CERON, C., DI FIORE, A., ERWIN, T., JARDIM, A., PALACIOS, W., SALDIAS, M. & VINCETI, B. 2002. Increasing dominance of large lianas in Amazonian forests. Nature 418:770774.CrossRefGoogle ScholarPubMed
PHILLIPS, O. L., ARAGAO, L. E. O. C., LEWIS, S. L. & FISHER, J. B., LLOYD, J., LOPEZ-GONZALEZ, G., MALHI, Y., MONTEAGUDO, A., PEACOCK, J., QUESADA, C. A., VAN DER HEIJDEN, G., ALMEIDA, S., AMARAL, I., ARROYO, L., AYMARD, G., BAKER, T. R., BANKI, O., BLANC, L., BONAL, D., BRANDO, P., CHAVE, J., DE OLIVEIRA, A. C. A., CARDOZO, N. D., CZIMCZIK, C. I., FELDPAUSCH, T. R., FREITAS, M. A., GLOOR, E., HIGUCHI, N., JIMENEZ, E., LLOYD, G., MEIR, P., MEDOZA, C., MOREL, A., NEILL, D. A., NEPSTAD, D., PATINO, S., PENUELA, M. C., PRIETO, A., RAMIREZ, F., SCHWARZ, M., SILVA, J., SILVEIRA, M., THOMAS, A. S., TER STEEGE, H., STROPP, J., VASQUEZ, R., ZELAZOWSKI, P., DAVILA, E. A., ANDELMAN, S., ANDRADE, A., CHAO, K. J., ERWIN, T., DI FIORE, A., HONORIO, E., KEELING, H., KILLEEN, T. J., LAURANCE, W. F., CRUZ, A. P., PITMAN, N. C. A., VARGAS, P. N., RAMIREZ-ANGULO, H., RUDAS, A., SALAMAO, R., SILVA, N., TERBORGH, J. & TORRES-LEZAMA, A. 2009. Drought sensitivity of the Amazon Rainforest. Science 323:13441347.CrossRefGoogle ScholarPubMed
PIOVESAN, G. & ADAMS, J. M. 2001. Masting behaviour in beech: linking reproduction and climatic variation. Canadian Journal of Botany 79:10391047.CrossRefGoogle Scholar
PLOWDEN, C. 2004. The ecology and harvest of andiroba seeds for oil production in the Brazilian Amazon. Conservation and Society 2:251272.Google Scholar
RIGAMONTE-AZEVEDO, V. 2010. Dinâmica da regeneração de andiroba (Carapa guianensis) na Reserva Florestal da Embrapa, Acre, Brasil. M.Sc. dissertation, Universidade Federal do Acre, Acre, Brazil.Google Scholar
ROYO, A. A. & CARSON, W. P. 2008. Direct and indirect effects of a dense understory of tree seedling recruitment in temperate forests: habitat-mediated predation versus competition. Canadian Journal of Forest Research 38:16341645.CrossRefGoogle Scholar
SAGARIN, R. & PAUCHARD, A. 2010. Observational approaches in ecology open new ground in a changing world. Frontiers in Ecology and the Environment 8:379386.CrossRefGoogle Scholar
SALESKA, S. R., DIDAN, K., HUERTE, A. R. & DA ROCHA, H. R. 2007. Amazon forests green-up during 2005 drought. Science 318:612.CrossRefGoogle ScholarPubMed
SAMANTHA, A., GANGULY, S., HASHIMOTO, H., DEVADIGA, S., VERMONTE, E., KNYAZIKHIN, Y., NEMANI, R. R. & MYNENI, R. B. 2010. Amazon forests did not green-up during the 2005 drought. Geophysical Research Letters 37: L05401 doi:10.1029/2009GL042154Google Scholar
SCHNITZER, S. A. 2005. A mechanistic explanation for global patterns of liana abundance and distribution. American Naturalist 166: 262276.CrossRefGoogle ScholarPubMed
SCHNITZER, S. A. & CARSON, W. P. 2010. Lianas suppress tree regeneration and diversity in treefall gaps. Ecology Letters 13:849857.CrossRefGoogle ScholarPubMed
SCHNITZER, S. A., KUZEE, M. E. & BONGERS, F. 2005. Disentangling above- and below-ground competition between lianas and trees in tropical forests. Journal of Ecology 93:11151125.CrossRefGoogle Scholar
SCHUPP, E. W., HOWE, H. F., AUGSPURGER, C. K. & LEVEY, D. J. 1989. Arrival and survival in tropical treefall gaps. Ecology 70:562564.CrossRefGoogle Scholar
SHANLEY, P. & MEDINA, G. 2005. Fruitíferas e plantas úteis na vida Amazônica. CIFOR & IMAZON, Belém. 304 pp.Google Scholar
SMITH, D. M., LARSON, B. C., KELTY, M. J. & ASHTON, P. M. S. 1997. The practice of silviculture: applied forest ecology. (Ninth edition). John Wiley & Sons, New York. 560 pp.Google Scholar
SNOOK, L. K., CÁMARA-CABRALES, L. & KELTY, M. J. 2005. Six years of fruit production by mahogany trees (Swietenia macrophylla King): patterns of variation and implications for sustainability. Forest Ecology and Management 206:221235.CrossRefGoogle Scholar
SORK, V. L. & BRAMBLE, J. E. 1993. Prediction of acorn crops in three species of North American oaks: Quercus alba, Q. rubra and Q. velutina. Annales des Sciences Forestieres 50 (Suppl.):128136.CrossRefGoogle Scholar
STEVENS, G. C. 1987. Lianas as structural parasites: the Bursera simaruba example. Ecology 68:7781.CrossRefGoogle Scholar
STEVENSON, P. R., CASTELLANOS, M. C., CORTÉS, A. I. & LINK, A. 2008. Flowering patterns in a seasonal tropical lowland forest in Western Amazonia. Biotropica 40:559567.CrossRefGoogle Scholar
SVENNING, J.-C., KINNER, D. A., STALLARD, R. F., ENGELBRECHT, B. M. J. & WRIGHT, S. J. 2004. Ecological determinism in plant community structure across a tropical forest landscape. Ecology 85:25262538.CrossRefGoogle Scholar
SVENNING, J.-C., ENGELBRECHT, B. M. J., KINNER, D. A., KURSAR, T. A., STALLARD, R. F. & WRIGHT, S. J. 2006. The relative roles of environment, history and local dispersal in controlling the distributions of common tree and shrub species in a tropical forest landscape, Panama. Journal of Tropical Ecology 22:575586.CrossRefGoogle Scholar
TOLEDO-ACEVES, T. & SWAINE, M.D. 2008. Above- and below-ground competition between the liana Acacia kamerunensis and tree seedlings in contrasting light environments. Plant Ecology 196:233244.CrossRefGoogle Scholar
TONINI, H., KAMINSKI, P. E., DA COSTA, P. & SCHWENGBER, L. A. M. 2008. Estrutura populacional e produção de Castanha-do-brasil (Bertholletia excelsa Bonpl.) e Andiroba (Carapa sp.) no sul do Estado de Roraima. Pp. 1624 in Wadt, L. H. O. (ed.). Anais do 1° Seminário do Projeto Kamukaia: Manejo Sustantável de Produtos Florestais Não-madeireiros na Amazônia. Embrapa, Acre. 182 pp.Google Scholar
VAN SCHAIK, C. P., TERBORGH, J. W. & WRIGHT, S. J. 1993. The phenology of tropical forests: adaptive significance and the consequences for primary consumers. Annual Review of Ecology and Systematics 24:353377.CrossRefGoogle Scholar
VANDER WALL, S. B., KUHN, K. M. & BECK, M. J. 2005. Seed removal, seed predation, and secondary dispersal. Ecology 86:801806.CrossRefGoogle Scholar
VIEIRA, S., TRUMBORE, S., CAMARGO, P. B., SELHORST, D., CHAMBERS, J. Q., HIGUCHI, N. & MARTINELLI, L. A. 2005. Slow growth rates of Amazonian trees: consequences for carbon cycling. Proceedings of the National Academy of Sciences USA 102:1850218507.CrossRefGoogle ScholarPubMed
WEBB, C. O. & PEART, D. R. 2000. Habitat associations of trees and seedlings in a Bornean rain forest. Journal of Ecology 88:464478.CrossRefGoogle Scholar
WRIGHT, S. J., CARRASCO, C., CALDERÓN, O. & PATON, S. 1999. The El Niño Southern Oscillation, variable fruit production, and famine in a tropical forest. Ecology 80:16321647.Google Scholar
WRIGHT, S. J., CALDERON, O., HERNANDEZ, A. & PATON, S. 2004. Are lianas increasing in importance in tropical forests? A 17-year record from Barro Colorado Island, Panama. Ecology 85:484489.CrossRefGoogle Scholar
WRIGHT, S. J., JARAMILLO, M. A., PAVON, J., CONDIT, R., HUBBELL, S. & FOSTER, R. 2005. Reproductive size thresholds in tropical trees: variation among individuals, species and forests. Journal of Tropical Ecology 21:307315.CrossRefGoogle Scholar
ZIMMERMAN, J. K., WRIGHT, S. J., CALDERON, O., PAGAN, M. A. & PATON, S. 2007. Flowering and fruiting phenologies of seasonal and aseasonal Neotropical forests: the role of annual changes in irradiance. Journal of Tropical Ecology 23:231251.CrossRefGoogle Scholar
ZUIDEMA, P. A. & BOOT, R. G. A. 2002. Demography of the Brazil nut tree (Bertholletia excelsa) in the Bolivian Amazon: impact of seed extraction on recruitment and population dynamics. Journal of Tropical Ecology 18:131.CrossRefGoogle Scholar