Abstract
Episodic multi-year droughts fundamentally alter the dynamics, functioning, and structure of Amazonian forests. However, the capacity of individual plant species to withstand intense drought regimes remains unclear. Here, we evaluated ecophysiological responses from a forest community where we sampled 83 woody plant species during 5 years of experimental drought (throughfall exclusion) in an eastern Amazonian terra firme forest. Overall, the experimental drought resulted in shifts of some, but not all, leaf traits related to photosynthetic carbon uptake and intrinsic water-use efficiency. Leaf δ13C values increased by 2–3‰ within the canopy, consistent with increased diffusional constraints on photosynthesis. Decreased leaf C:N ratios were also observed, consistent with lower investments in leaf structure. However, no statistically significant treatment effects on leaf nitrogen content were observed, consistent with a lack of acclimation in photosynthetic capacity or increased production of nitrogen-based secondary metabolites. The results of our study provide evidence of robust acclimation potential to drought intensification in the diverse flora of an Amazonian forest community. The results reveals considerable ability of several species to respond to intense drought and challenge commonly held perspectives that this flora has attained limited adaptive plasticity because of a long evolutionary history in a favorable and stable climate.
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References
Anderegg WRL, Flint A, Huang CY et al (2015) Tree mortality predicted from drought-induced vascular damage. Nat Geosci 8(5):367–371. https://doi.org/10.1038/ngeo2400
Andreae MO, Rosenfeld D, Artaxo P et al (2004) Smoking rain clouds over the Amazon. Science 303(5662):1337–1342. https://doi.org/10.1126/science.1092779
Blumenthal SA, Rothman JM, Chritz KL et al (2016) Stable isotopic variation in tropical forest plants for applications in primatology. Am J Primatol 78:1041–1054. https://doi.org/10.1002/ajp.22488
Boisier JP, Ciais P, Ducharne A et al (2015) Projected strengthening of Amazonian dry season by constrained climate model simulations. Nat Clim Chang 5(7):656–660. https://doi.org/10.1038/nclimate2658
Brando PM, Nepstad DC, Davidson EA et al (2008) Drought effects on litterfall, wood production and belowground carbon cycling in an Amazon forest: results of a throughfall reduction experiment. Philos Trans R Soc B 363:1839–1848. https://doi.org/10.1098/rstb.2007.0031
Carswell FE, Meir P, Wandelli EV et al (2000) Photosynthetic capacity in a central Amazonian rain forest. Tree Physiol 20:179–186. https://doi.org/10.1093/treephys/20.3.179
Cernusak LA, Winter K, Turner BL (2009) Physiological and isotopic (δ13C and δ18O) responses of three tropical tree species to water and nutrient availability. Plant Cell Environ 32:1441–1455. https://doi.org/10.1111/j.1365-3040.2009.02010.x
Cox P, Betts R, Collins M et al (2004) Amazonian forest dieback under climate-carbon cycle projections for the 21st century. Theor Appl Climatol 78:137–156. https://doi.org/10.1007/s00704-004-0049-4
Cox PM, Pearson D, Booth BB et al (2013) Sensitivity of tropical carbon to climate change constrained by carbon dioxide variability. Nature 494(7437):341–344. https://doi.org/10.1038/nature11882
Domingues TF, Martinelli LA, Ehleringer JR (2007) Ecophysiological traits of plant functional groups in forest and pasture ecosystems from eastern Amazônia, Brazil. Plant Ecol 193:101–112. https://doi.org/10.1007/s11258-006-9251-z
Domingues TF, Martinelli LA, Ehleringer JR (2013) Seasonal patterns of leaf-level photosynthetic gas exchange in an eastern Amazonian rain forest. Plant Ecol Divers 7:189–203. https://doi.org/10.1080/17550874.2012.748849
Duffy PB, Brando P, Asner GP, Field CB (2015) Projections of future meteorological drought and wet periods in the Amazon. Proc Natl Acad Sci 112(43):13172–13177. https://doi.org/10.1073/pnas.1421010112
Farquhar GD, Werselaar R, Firth PM (1979) Ammonia volatilization from senescing leaves of maize. Science 203(4386):1257–1258. https://doi.org/10.1126/science.203.4386.1257
Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Phys Plant Mol Biol 40:503–537. https://doi.org/10.1146/annurev.pp.40.060189.002443
Feldpausch TR, Phillips OL, Brienen RJW et al (2017) Amazon forest response to repeated droughts. Glob Biogeochem Cycles 30(7):964–982. https://doi.org/10.1002/2015GB005133
Flexas J, Ribas-Carbó M, Diaz-Espejo A et al (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant Cell Environ 31:602–621. https://doi.org/10.1111/J.1365-3040.2007.01757.X
Fyllas NM, Patiño S, Baker TR et al (2009) Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate. Biogeosciences 6:2677–2708. https://doi.org/10.5194/bg-6-2677-2009
Högberg P, Johnnisson C, Högberg M et al (1995) Measurements of abundances of 15N and 13C as tools in retrospective studies of N balances and water stress in forests: a discussion of preliminary results. Plant Soil 168:125–133. https://doi.org/10.1007/BF00029321
Huntingford C, Zelazowski P, Galbraith D et al (2013) Simulated resilience of tropical rainforests to CO2-induced climate change. Nat Geosci 6(4):268–273. https://doi.org/10.1038/ngeo1741
Marengo JA, Ambrizzi T, da Rocha H et al (2010) Future change of climate in South America in the late twenty-first century: intercomparison of scenarios from three regional climate models. Clim Dyn 35(6):1073–1097. https://doi.org/10.1007/s00382-009-0721-6
McDowell N, Pockman WT, Allen CD et al (2008) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178:719–739. https://doi.org/10.1111/j.1469-8137.2008.02436.x
Nardoto GB, Quesada CA, Patiño S et al (2014) Basin-wide variations in Amazon forest nitrogen-cycling characteristics as inferred from plant and soil 15N:14N measurements. Plant Ecol Divers 7:173–187. https://doi.org/10.1080/17550874.2013.807524
Nepstad DC, de Carvalho CR, Davidson EA et al (1994) The role of deep roots in the hydrological and carbon cycles of Amazonian forests and pastures. Nature 372(6507):666–669. https://doi.org/10.1038/372666a0
Nepstad DC, Moutinho P, Dias-Filho MB et al (2002) The effects of partial throughfall exclusion on canopy processes, aboveground production, and biogeochemistry of an Amazon forest. J Geophys Res 107(D20):8085. https://doi.org/10.1029/2001JD000360
Nepstad DC, Tohver IM, Ray D et al (2007) Mortality of large trees and lianas following experimental drought in an Amazon forest. Ecology 88:2259–2269. https://doi.org/10.1890/06-1046.1
Norby RJ, De Kauwe MG, Domingues TF et al (2016) Model-data synthesis for the next generation of forest free-air CO2 enrichment (FACE) experiments. New Phytol 209:17–28. https://doi.org/10.1111/nph.13593
Oliveira RS, Dawson TE, Burgess SSO et al (2005) Hydraulic redistribution in three Amazonian trees. Oecologia 145:354–363. https://doi.org/10.1007/s00442-005-0108-2
Ometto JPHB, Ehleringer JR, Domingues TF et al (2006) The stable carbon and nitrogen isotopic composition of vegetation in tropical forests of the Amazon Basin, Brazil. Biogeochemistry 79:251–274. https://doi.org/10.1007/s10533-006-9008-8
Quesada CA, Lloyd J, Schwarz M et al (2010) Variations in chemical and physical properties of Amazon forest soils in relation to their genesis. Biogeosciences 7:1515–1541. https://doi.org/10.5194/bg-7-1515-2010
Roberts P, Blumenthal SA, Dittus W et al (2017) Stable carbon, oxygen, and nitrogen, isotope analysis of plants from a South Asian tropical forest: implications for primatology. Am J Primatol. https://doi.org/10.1002/ajp.22656
Rowland L, da Costa ACL, Galbraith DR et al (2015) Death from drought in tropical forests is triggered by hydraulics not carbon starvation. Nature 528(7580):119–122. https://doi.org/10.1038/nature15539
Silva-Dias MAF, Rutledge S, Kabat P et al (2002) Cloud and rain processes in a biosphere–atmosphere interaction context in the Amazon Region. J Geophys Res 107(D20):8072. https://doi.org/10.1029/2001JD000335
Sperry JS (2000) Hydraulic constraints on plant gas exchange. Agric For Meteorol 104(1):13–23. https://doi.org/10.1016/S0168-1923(00)00144-1
Acknowledgements
We thank P. Camargo, M. Moreira, F. Ishida, E. Mazzi, and our colleagues at the LBA-ECO and IPAM-Santarém offices. Financial support for this work was provided partially by a research grant from NASA LBA-Ecology to JRE, LBF, JAB and L.A.M.
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JRE, LAM and DCN designed the study and provided institutional support, TFD and JPHBO collected and processed samples. LAM, JPHBP and TFD analysed the data and wrote the manuscript with contributions from all authors, DCN and PMB provided support to field activities, shared auxiliary data and scientific insights.
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Communicated by Russell K. Monson.
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Domingues, T.F., Ometto, J.P.H.B., Nepstad, D.C. et al. Ecophysiological plasticity of Amazonian trees to long-term drought. Oecologia 187, 933–940 (2018). https://doi.org/10.1007/s00442-018-4195-2
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DOI: https://doi.org/10.1007/s00442-018-4195-2