Abstract
Severe droughts may alter the reproductive phenology of tropical tree species, but our understanding of these effects has been hampered by confounded variation in drought, light and other factors during natural drought events. We used a large-scale experimental reduction of throughfall in an eastern-central Amazon forest to study the phenological response to drought of an abundant subcanopy tree, Coussarea racemosa. We hypothesized that drought would alter the production and the timing of reproduction, as well as the number of viable fruits. The study system comprised two 1-ha plots in the Tapajos National Forest, Para, Brazil: a dry plot where 50% of incoming precipitation (80% throughfall) was diverted from the soil during the six-month wet season beginning in January 2000, and a wet plot that received natural rainfall inputs. Fruit production of C. racemosa was quantified every 15 days using 100 litter traps (0.5 m2) in each plot. The production of new leaves and flowers was recorded monthly for C. racemosa individuals. Soil water, pre-dawn leaf water potential and solar radiation were measured to help interpret phenological patterns. Over the ∼3.5-year period (April 2000 through December 2003), total fruit production remained similar between plots, declining by 12%. In 2003, production was four times higher in both plots than in previous years. In the dry plot, fruit fall shifted 40 and 60 days later into the dry season in 2002 and 2003, respectively. Total fruit fall dry mass production was variable across the study period. Foliage and flower production coincided with peak irradiance early in the dry season until delays in flowering appeared in the dry plot in 2002 and 2003. Plant water stress, through its influence on leaf developmental processes and, perhaps, inhibition of photosynthesis, appears to have altered both the timing of fruit fall and the quality and number of seeds produced.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Andreae MO, Rosenfeld D, Artaxo P, Costa AA, Frank GP, Longo KM, Silva-Dias MAF (2004) Smoking rain clouds over the Amazon. Science 303:1337–1342
Ashton PS, Givnish TJ, Appanah S (1988) Staggered flowering in the Dipterocarpaceae: New insights into floral induction and the evolution of mast fruiting in the aseasonal tropics. Am Nat 132:44–66
Augspurger CK (1981) Reproductive synchrony of a tropical shrub: experimental studies on effects on pollinators and seed predators on Hybanthus prunifolius (Violaceae). Ecology 62:775–788
Augspurger CK (1984) Seedling survival of tropical tree species: interactions of dispersal distance, light-gaps, and pathogens. Ecology 65:1705–1712
Borchert R (1991) Growth periodicity and dormancy. In: Raghvendra AS (ed) Physiology of trees. Wiley, New York, pp 221–245
Borchert R (1994) Soil and stem water storage determine phenology and distribution of tropical dry forest trees. Ecology 75:1437–1449
Borchert R, Rivera G, Hagnauer W (2002) Modification of vegetative phenology in a tropical semi-deciduous forest by abnormal drought and rain. Biotropica 34:27–39
Borchert R, Meyer SA, Felger RS, Porter-Bolland L (2004) Environmental control of flowering periodicity in Costa Rican and Mexican tropical dry forests. Glob Ecol Biogeogr 13:409–425
Borchert R, Renner SS, Calle Z, Navarrete D, Tye A, Gautier L, Spichiger R, von Hildebrand P (2005) Photoperiodic induction of synchronous flowering near the equator. Nature 433:627–629
Chapin FS III, Schulze E-D, Mooney HA (1990) The ecology and economics of storage in plants. Annu Rev Ecol Syst 21:423–447
Curran LM, Leighton M (2000) Vertebrate responses to spatio-temporal variation in seed production by mast-fruiting Bornean Dipterocarpaceae. Ecol Monogr 70:101–128
Curran LM, Webb CO (2000) Spatio-temporal scale of seed predation in mast-fruiting Dipterocarpaceae: experimental studies of regional seed availability. Ecol Monogr 70:129–148
Curran LM, Caniago I, Paoli GD, Astiani D, Kusneti M, Leighton M, Nirarita C, Haeruman H (1999) Impact of El Niño and logging on canopy tree recruitment in Borneo. Science 286:2184–2188
Frankie GW, Baker HG, Opler PA (1974) Comparative phenological studies of trees in tropical wet and dry forests in the lowlands of Costa Rica. J Ecol 62:881–919
Garwood NC (1983) Seed germination in a seasonal tropical forest in Panama a conmunity study. Ecol Monogr 53:159–181
Graham EA, Mulkey SS, Wright SJ, Kitajima K, Phillips NG (2003) Cloud cover limits productivity in a tropical rain forest tree during La Nina. Proc Nat Acad Sci 100:572–576
Janzen DH (1969) Seed-eaters vs. seed size, number, toxicity, and dispersal. Evolution 23:1–27
Jones HG, Sutherland RA (1991) Stomatal control of xylem embolism. Plant Cell Environ 14:607–612
Larcher W (1995) Physiological plant ecology. 3rd edn. Springer, Berlin Heidelberg New York
Nepstad DC, Carvalho CJR, Davidson EA, Jipp P, Lefebvre PA, Negreiros GH, Silva ED, Stone TA, Trumbore SE, Vieira S (1994) The role of deep roots in the hydrological and carbon cycles of Amazonian forests and pastures. Nature 372:666–669
Nepstad DC, Moutinho PRS, Dias-Filho MB, Davidson EA,Cardinot G, Markewitz D, Figueiredo R, Viana N, Lefebvre PA, Ray DG, Chambers JQ, Barros L, Ishida FY, Belk E, Schwalbe K (2002) The effects of rainfall exclusion on canopy processes and biogeochemistry of an Amazon forest. J Geophys Res 107:1–18
Nepstad DC, Lefebvre P, Da Silva UL, Tomasella J, Schlesinger P, Solorzano L, Moutinho P, Ray D, Benito JG (2004) Amazon drought and its implications for forest flammability and tree growth: a basin-wide analysis. Glob Change Biol 10:704–717
New York Botanical Garden (2006) New York Botanical Garden virtual herbarium: online specimen search. New York Botanical Garden, Bronx, NY (see http://sciweb.nybg.org/Science2/vii2.asp, last accessed 19th July 2006)
Newell EA, Mulkey SS, Wright SH (2002) Seasonal patterns of carbohydrate storage in four neotropical tree species. Oecologia 133:333–342
Oliveira RS, Dawson TE, Burgess SSO, Nepstad D (2005) Hydraulic redistribution in three Amazonian trees. Oecologia 145:354–363
Ozanne CMP, Anhuf D, Boulter SL, Keller M, Kitching RL, Körner C, Meinzer FC, Mitchell AW, Nakashizuka T, Silva Dias PL, Stork NE, Wright SJ, Yoshimura M (2003) Biodiversity meets the atmosphere: a global view of forest canopies. Science 301:183
Parrotta JA, Francis JK, Almeida RR (eds)(1995) Trees of Tapajos: A photographic field guide. General Technical Report IITF-1, United States Department of Agriculture, Forest Service, International Institute of Tropical Forestry, Rio Pedras, Puerto Rico
Penuelas J, Filella I (2001) Responses to a warming world. Science 294:793–795
Reich P, Borchert R (1982) Phenology and ecophysiology of the tropical tree, Tabebuia neochrysantha (Bignoniaceae). Ecology 63:294–299
Rivera G, Borchert R (2000) Induction of flowering in tropical trees by a 30-min reduction in photoperiod: evidence from field observations and herbarium specimens. Tree Physiol 21:201–212
Rivera G, Elliott S, Caldas LS, Nicolossi G, Coradin VTR, Borchert R (2002) Increasing day-length induces spring flushing of tropical dry forest trees in the absence of rain. Trees 16:445–456
Rohter L (2005) A record Amazon drought, and fear of wider ills. New York Times, 11 Dec 2005
Scholander PF, Hammel HT, Bradstreet ED, Hemmingsen EA (1965) Sap pressure in vascular plants. Science 148:339–46
Silva-Dias MS, Rutledge S, Kablat P, Dias PS, Nobre CA, Fish G, Dolman A, Zipser E, Garstang M, Manzi AO, Fuentes JD, Rocha HR, Marengo JÁ, Fattori AP, Sá LDA, Alvalá RCS, Andreae MO, Artaxo P, Gielow R, Gatti L (2002) Cloud and rain processes in a biosphere atmosphere interaction context in the Amazon Region. J Geophys Res 107(D20):8072–8092
Topp GC, Davis JL, Annan AP (1980) Electromagnetic determination of soil water content: measurements in coaxial transmission lines, vol. 16. Water Resources Research, Washington, pp 574–582
Timmermann A, Oberhuber J, Bacher A, Esch M, Latif M, Roeckner E (1999) Increased El Niño frequency in a climate model forced by future greenhouse warming. Nature 398:694–696
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, Berlin Heidelberg New York
Vieira S (2003) Mudanças Globais e Taxa de Crescimento de Espécies Arbóreas da Amazônia. Doctoral Thesis. University of São Paulo, São Paulo, Brazil
Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee T JC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395
Wang GL (2005) Agricultural drought in a future climate: results from 15 global climate models participating in the IPCC 4th Assessment. Climate Dyn 25:739–753
Williams RJ, Myers BA, Muller WJ, Duff A, Eamus D (1997) Leaf phenology of woody species in a North Australian tropical savanna. Ecology 78:2542–2558
Wright SJ (1996) Phenological responses to seasonality in tropical forest plants. In: Mulkey SD, Chazdon RL, Smith AP (eds) Tropical forest ecophysiology. Chapman & Hall, New York, pp 440–460
Wright SJ, Carrasco C, Calderón O, Paton S (1999) The El Niño Southern Oscillation, variable fruit production and famine in a tropical forest. Ecology 80:1632–1647
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle River, NJ, p 931
Acknowledgments
This research was carried out within the experiment “Seca Floresta”, which was funded by the NSF grants DEB 9707556 and DEB 0075602 to the Woods Hole Research Center, by the NASA, LBA-ECO grant NCC5-285 to Woods Hole Research Center, by the Brazilian Ministério do Meio Ambiente, Pilot Program for the Conservation of Brazilian Rain Forests, Directed Research Program to the Instituto de Pesquisa Ambiental da Amazonia, and by a US Agency for International Development Grant to the Woods Hole Research Center. Special thanks to the Instituto Brasileiro de Meio Ambiente e Recursos Renováveis (IBAMA) for infrastructure support within the Tapajos National Forest. We also thank Adilson, Nelson and the “Seca Floresta” crew for support in the lab. Paulo Moutinho and two anonymous reviewers provided constructive comments on this manuscript. The authors declare that the experiment complies with the current laws of Brazil.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Jim Ehleringer.
Rights and permissions
About this article
Cite this article
Brando, P., Ray, D., Nepstad, D. et al. Effects of partial throughfall exclusion on the phenology of Coussarea racemosa (Rubiaceae) in an east-central Amazon rainforest. Oecologia 150, 181–189 (2006). https://doi.org/10.1007/s00442-006-0507-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-006-0507-z