Causes of reduced leaf‐level photosynthesis during strong El Niño drought in a Central Amazon forest
Abstract
Abstract Sustained drought and concomitant high temperature may reduce photosynthesis and cause tree mortality. Possible causes of reduced photosynthesis include stomatal closure and biochemical inhibition, but their relative roles are unknown in Amazon trees during strong drought events. We assessed the effects of the recent (2015) strong El Niño drought on leaf‐level photosynthesis of Central Amazon trees via these two mechanisms. Through four seasons of 2015, we measured leaf gas exchange, chlorophyll a fluorescence parameters, chlorophyll concentration, and nutrient content in leaves of 57 upper canopy and understory trees of a lowland terra firme forest on well‐drained infertile oxisol. Photosynthesis decreased 28% in the upper canopy and 17% in understory trees during the extreme dry season of 2015, relative to other 2015 seasons and was also lower than the climatically normal dry season of the following non‐El Niño year. Photosynthesis reduction under extreme drought and high temperature in the 2015 dry season was related only to stomatal closure in both upper canopy and understory trees, and not to chlorophyll a fluorescence parameters, chlorophyll, or leaf nutrient concentration. The distinction is important because stomatal closure is a transient regulatory response that can reverse when water becomes available, whereas the other responsesmore »
- Authors:
-
- Environmental Dynamics Department Brazil′s National Institute for Amazon Research Manaus Brazil
- Department of Forest Sciences Federal University of Amazonas Manaus Brazil
- Center for Distance Education Federal University of Amazonas Manaus Brazil
- Department of Ecology and Evolutionary Biology University of Arizona Tucson Arizona
- Publication Date:
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1439744
- Grant/Contract Number:
- SC0008383
- Resource Type:
- Publisher's Accepted Manuscript
- Journal Name:
- Global Change Biology
- Additional Journal Information:
- Journal Name: Global Change Biology Journal Volume: 24 Journal Issue: 9; Journal ID: ISSN 1354-1013
- Publisher:
- Wiley-Blackwell
- Country of Publication:
- United Kingdom
- Language:
- English
Citation Formats
Santos, Victor Alexandre Hardt Ferreira dos, Ferreira, Marciel José, Rodrigues, João Victor Figueiredo Cardoso, Garcia, Maquelle Neves, Ceron, João Vitor Barbosa, Nelson, Bruce Walker, and Saleska, Scott Reid. Causes of reduced leaf‐level photosynthesis during strong El Niño drought in a Central Amazon forest. United Kingdom: N. p., 2018.
Web. doi:10.1111/gcb.14293.
Santos, Victor Alexandre Hardt Ferreira dos, Ferreira, Marciel José, Rodrigues, João Victor Figueiredo Cardoso, Garcia, Maquelle Neves, Ceron, João Vitor Barbosa, Nelson, Bruce Walker, & Saleska, Scott Reid. Causes of reduced leaf‐level photosynthesis during strong El Niño drought in a Central Amazon forest. United Kingdom. https://doi.org/10.1111/gcb.14293
Santos, Victor Alexandre Hardt Ferreira dos, Ferreira, Marciel José, Rodrigues, João Victor Figueiredo Cardoso, Garcia, Maquelle Neves, Ceron, João Vitor Barbosa, Nelson, Bruce Walker, and Saleska, Scott Reid. Wed .
"Causes of reduced leaf‐level photosynthesis during strong El Niño drought in a Central Amazon forest". United Kingdom. https://doi.org/10.1111/gcb.14293.
@article{osti_1439744,
title = {Causes of reduced leaf‐level photosynthesis during strong El Niño drought in a Central Amazon forest},
author = {Santos, Victor Alexandre Hardt Ferreira dos and Ferreira, Marciel José and Rodrigues, João Victor Figueiredo Cardoso and Garcia, Maquelle Neves and Ceron, João Vitor Barbosa and Nelson, Bruce Walker and Saleska, Scott Reid},
abstractNote = {Abstract Sustained drought and concomitant high temperature may reduce photosynthesis and cause tree mortality. Possible causes of reduced photosynthesis include stomatal closure and biochemical inhibition, but their relative roles are unknown in Amazon trees during strong drought events. We assessed the effects of the recent (2015) strong El Niño drought on leaf‐level photosynthesis of Central Amazon trees via these two mechanisms. Through four seasons of 2015, we measured leaf gas exchange, chlorophyll a fluorescence parameters, chlorophyll concentration, and nutrient content in leaves of 57 upper canopy and understory trees of a lowland terra firme forest on well‐drained infertile oxisol. Photosynthesis decreased 28% in the upper canopy and 17% in understory trees during the extreme dry season of 2015, relative to other 2015 seasons and was also lower than the climatically normal dry season of the following non‐El Niño year. Photosynthesis reduction under extreme drought and high temperature in the 2015 dry season was related only to stomatal closure in both upper canopy and understory trees, and not to chlorophyll a fluorescence parameters, chlorophyll, or leaf nutrient concentration. The distinction is important because stomatal closure is a transient regulatory response that can reverse when water becomes available, whereas the other responses reflect more permanent changes or damage to the photosynthetic apparatus. Photosynthesis decrease due to stomatal closure during the 2015 extreme dry season was followed 2 months later by an increase in photosynthesis as rains returned, indicating a margin of resilience to one‐off extreme climatic events in Amazonian forests.},
doi = {10.1111/gcb.14293},
journal = {Global Change Biology},
number = 9,
volume = 24,
place = {United Kingdom},
year = {Wed May 30 00:00:00 EDT 2018},
month = {Wed May 30 00:00:00 EDT 2018}
}
https://doi.org/10.1111/gcb.14293
Web of Science
Works referenced in this record:
Exploring the likelihood and mechanism of a climate-change-induced dieback of the Amazon rainforest
journal, February 2009
- Malhi, Y.; Aragao, L. E. O. C.; Galbraith, D.
- Proceedings of the National Academy of Sciences, Vol. 106, Issue 49
Drought sensitivity of Amazonian carbon balance revealed by atmospheric measurements
journal, February 2014
- Gatti, L. V.; Gloor, M.; Miller, J. B.
- Nature, Vol. 506, Issue 7486
Differences in the responses of photosystem I and photosystem II of three tree species Cleistanthus sumatranus, Celtis philippensis and Pistacia weinmannifolia exposed to a prolonged drought in a tropical limestone forest
journal, January 2013
- Huang, W.; Fu, P. -L.; Jiang, Y. -J.
- Tree Physiology, Vol. 33, Issue 2
The regional variation of aboveground live biomass in old-growth Amazonian forests
journal, July 2006
- Malhi, Yadvinder; Wood, Daniel; Baker, Timothy R.
- Global Change Biology, Vol. 12, Issue 7
Seasonal variation in the leaf gas exchange of tropical forest trees in the rain forest–savanna transition of the southern Amazon Basin
journal, June 2005
- Miranda, Eduardo Jacusiel; Vourlitis, George L.; Filho, Nicolau Priante
- Journal of Tropical Ecology, Vol. 21, Issue 4
The use of JIP test to evaluate drought-tolerance of transgenic rice overexpressing OsNAC10
journal, January 2011
- Redillas, Mark C. F. R.; Strasser, Reto J.; Jeong, Jin Seo
- Plant Biotechnology Reports, Vol. 5, Issue 2
Tropical rainforest carbon sink declines during El Niño as a result of reduced photosynthesis and increased respiration rates
journal, August 2017
- Cavaleri, Molly A.; Coble, Adam P.; Ryan, Michael G.
- New Phytologist, Vol. 216, Issue 1
Drought impact on forest carbon dynamics and fluxes in Amazonia
journal, March 2015
- Doughty, Christopher E.; Metcalfe, D. B.; Girardin, C. A. J.
- Nature, Vol. 519, Issue 7541
Influence of Seasonal Variations in Soil Water Availability on Gas Exchange of Tropical Canopy Trees
journal, July 2012
- Stahl, Clément; Burban, Benoit; Wagner, Fabien
- Biotropica, Vol. 45, Issue 2
Photoprotection of evergreen and drought-deciduous tree leaves to overcome the dry season in monsoonal tropical dry forests in Thailand
journal, December 2013
- Ishida, A.; Yamazaki, J. -Y.; Harayama, H.
- Tree Physiology, Vol. 34, Issue 1
The crucial role of plant mitochondria in orchestrating drought tolerance
journal, June 2008
- Atkin, Owen K.; Macherel, David
- Annals of Botany, Vol. 103, Issue 4
Amazon Forests Green-Up During 2005 Drought
journal, September 2007
- Saleska, Scott R.; Didan, Kamel; Huete, Alfredo R.
- Science, Vol. 318, Issue 5850
Forest structure and carbon dynamics in Amazonian tropical rain forests
journal, June 2004
- Vieira, Simone; de Camargo, Plinio Barbosa; Selhorst, Diogo
- Oecologia, Vol. 140, Issue 3
Vertical Profiles of Environmental Factors within Tropical Rainforest, Lambir Hills National Park, Sarawak, Malaysia
journal, November 2001
- Kumagai, Tomo'omi; Kuraji, Koichiro; Noguchi, Hironori
- Journal of Forest Research, Vol. 6, Issue 4
POLYPHASIC CHLOROPHYLL a FLUORESCENCE TRANSIENT IN PLANTS AND CYANOBACTERIA
journal, January 1995
- Strasserf, Reto J.; Srivastava, Alaka
- Photochemistry and Photobiology, Vol. 61, Issue 1
The role of deep roots in the hydrological and carbon cycles of Amazonian forests and pastures
journal, December 1994
- Nepstad, Daniel C.; de Carvalho, Claudio R.; Davidson, Eric A.
- Nature, Vol. 372, Issue 6507
Effects of rising temperatures and [CO 2 ] on the physiology of tropical forest trees
journal, February 2008
- Lloyd, Jon; Farquhar, Graham D.
- Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 363, Issue 1498
Comparative measurements of carbon dioxide fluxes from two nearby towers in a central Amazonian rainforest: The Manaus LBA site
journal, January 2002
- Araújo, A. C.
- Journal of Geophysical Research, Vol. 107, Issue D20
Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress
journal, February 2006
- Flexas, Jaume; Bota, Josefina; Galmés, Jeroni
- Physiologia Plantarum, Vol. 127, Issue 3
Photosynthetic Light Environments in a Lowland Tropical Rain Forest in Costa Rica
journal, July 1984
- Chazdon, Robin L.; Fetcher, Ned
- The Journal of Ecology, Vol. 72, Issue 2
Larger trees suffer most during drought in forests worldwide
journal, September 2015
- Bennett, Amy C.; McDowell, Nathan G.; Allen, Craig D.
- Nature Plants, Vol. 1, Issue 10
Fitting photosynthetic carbon dioxide response curves for C 3 leaves
journal, September 2007
- Sharkey, Thomas D.; Bernacchi, Carl J.; Farquhar, Graham D.
- Plant, Cell & Environment, Vol. 30, Issue 9
Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis
journal, June 2010
- Strasser, Reto J.; Tsimilli-Michael, Merope; Qiang, Sheng
- Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1797, Issue 6-7
Oxygen Exchange in Relation to Carbon Assimilation in Water-stressed Leaves During Photosynthesis
journal, June 2002
- Haupt-Herting, S.
- Annals of Botany, Vol. 89, Issue 7
The Impacts of Droughts in Tropical Forests
journal, July 2016
- Corlett, Richard T.
- Trends in Plant Science, Vol. 21, Issue 7
Occurrence of stomatal patchiness and its spatial scale in leaves from various sizes of trees distributed in a South-east Asian tropical rainforest in Peninsular Malaysia
journal, January 2015
- Kamakura, M.; Kosugi, Y.; Takanashi, S.
- Tree Physiology, Vol. 35, Issue 1
Climate drivers of the Amazon forest greening
journal, July 2017
- Wagner, Fabien Hubert; Hérault, Bruno; Rossi, Vivien
- PLOS ONE, Vol. 12, Issue 7
Leaf development and demography explain photosynthetic seasonality in Amazon evergreen forests
journal, February 2016
- Wu, J.; Albert, L. P.; Lopes, A. P.
- Science, Vol. 351, Issue 6276
Variation of carbon and nitrogen cycling processes along a topographic gradient in a central Amazonian forest
journal, May 2004
- Luizao, Regina C. C.; Luizao, Flavio J.; Paiva, Romilda Q.
- Global Change Biology, Vol. 10, Issue 5
Drought-inhibition of Photosynthesis in C3 Plants: Stomatal and Non-stomatal Limitations Revisited
journal, February 2002
- Flexas, J.
- Annals of Botany, Vol. 89, Issue 2
Changes with Leaf Age in Stomatal Function and Water Status of Several Tropical Tree Species
journal, March 1988
- Reich, Peter B.; Borchert, Rolf
- Biotropica, Vol. 20, Issue 1
Decline of photosynthetic capacity with leaf age in relation to leaf longevities for five tropical canopy tree species
journal, May 1997
- Kitajima, Kaoru; Mulkey, Stephen S.; Wright, S. Joseph
- American Journal of Botany, Vol. 84, Issue 5
Stomatal sensitivity to vapour pressure deficit of temperate and tropical evergreen rainforest trees of Australia
journal, February 2004
- Cunningham, ShaunC.
- Trees, Vol. 18, Issue 4
Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents
journal, October 1983
- Lichtenthaler, Hartmut K.; Wellburn, Alan R.
- Biochemical Society Transactions, Vol. 11, Issue 5
Impact of severe dry season on net ecosystem exchange in the Neotropical rainforest of French Guiana
journal, August 2008
- Bonal, Damien; Bosc, Alexandre; Ponton, StÉPhane
- Global Change Biology, Vol. 14, Issue 8
Vegetation dynamics and rainfall sensitivity of the Amazon
journal, October 2014
- Hilker, Thomas; Lyapustin, Alexei I.; Tucker, Compton J.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 45
What drives the seasonality of photosynthesis across the Amazon basin? A cross-site analysis of eddy flux tower measurements from the Brasil flux network
journal, December 2013
- Restrepo-Coupe, Natalia; da Rocha, Humberto R.; Hutyra, Lucy R.
- Agricultural and Forest Meteorology, Vol. 182-183
Techniques and experimental approaches for the measurement of plant water status
journal, February 1981
- Turner, Neil C.
- Plant and Soil, Vol. 58, Issue 1-3
Stomatal and non-stomatal limitations of bell pepper (Capsicum annuum L.) plants under water stress and re-watering: Delayed restoration of photosynthesis during recovery
journal, February 2014
- Campos, Huitziméngari; Trejo, Carlos; Peña-Valdivia, Cecilia B.
- Environmental and Experimental Botany, Vol. 98
Energy dissipation in drought-avoiding and drought-tolerant tree species at midday during the Mediterranean summer
journal, January 2000
- Martinez-Ferri, E.; Balaguer, L.; Valladares, F.
- Tree Physiology, Vol. 20, Issue 2
Sap Pressure in Vascular Plants: Negative hydrostatic pressure can be measured in plants
journal, April 1965
- Scholander, P. F.; Bradstreet, E. D.; Hemmingsen, E. A.
- Science, Vol. 148, Issue 3668
A lumped water balance model to evaluate duration and intensity of drought constraints in forest stands
journal, March 1999
- Granier, A.; Bréda, N.; Biron, P.
- Ecological Modelling, Vol. 116, Issue 2-3
Measuring the strength of ENSO events: How does 1997/98 rank?
journal, September 1998
- Wolter, Klaus; Timlin, Michael S.
- Weather, Vol. 53, Issue 9
Respiration from a Tropical Forest Ecosystem: Partitioning of Sources and low Carbon use Efficiency
journal, August 2004
- Chambers, Jeffrey Q.; Tribuzy, Edgard S.; Toledo, Ligia C.
- Ecological Applications, Vol. 14, Issue sp4
After more than a decade of soil moisture deficit, tropical rainforest trees maintain photosynthetic capacity, despite increased leaf respiration
journal, September 2015
- Rowland, Lucy; Lobo-do-Vale, Raquel L.; Christoffersen, Bradley O.
- Global Change Biology, Vol. 21, Issue 12
Depth of soil water uptake by tropical rainforest trees during dry periods: does tree dimension matter?
journal, July 2013
- Stahl, Clément; Hérault, Bruno; Rossi, Vivien
- Oecologia, Vol. 173, Issue 4
The Amazon basin in transition
journal, January 2012
- Davidson, Eric A.; de Araújo, Alessandro C.; Artaxo, Paulo
- Nature, Vol. 481, Issue 7381
A modified single solution method for the determination of phosphate in natural waters
journal, January 1962
- Murphy, J.; Riley, J. P.
- Analytica Chimica Acta, Vol. 27
The response of tropical rainforests to drought—lessons from recent research and future prospects
journal, March 2016
- Bonal, Damien; Burban, Benoit; Stahl, Clément
- Annals of Forest Science, Vol. 73, Issue 1
Urgent need for warming experiments in tropical forests
journal, March 2015
- Cavaleri, Molly A.; Reed, Sasha C.; Smith, W. Kolby
- Global Change Biology, Vol. 21, Issue 6
Seasonal trends in photosynthesis and electron transport during the Mediterranean summer drought in leaves of deciduous oaks
journal, April 2015
- Osuna, J. L.; Baldocchi, D. D.; Kobayashi, H.
- Tree Physiology, Vol. 35, Issue 5
Environmental change and the carbon balance of Amazonian forests: Environmental change in Amazonia
journal, February 2014
- Aragão, Luiz E. O. C.; Poulter, Benjamin; Barlow, Jos B.
- Biological Reviews, Vol. 89, Issue 4
The 2010 Amazon Drought
journal, February 2011
- Lewis, S. L.; Brando, P. M.; Phillips, O. L.
- Science, Vol. 331, Issue 6017
Chlorophyll fluorescence tracks seasonal variations of photosynthesis from leaf to canopy in a temperate forest
journal, January 2017
- Yang, Hualei; Yang, Xi; Zhang, Yongguang
- Global Change Biology, Vol. 23, Issue 7
Seasonal patterns of leaf-level photosynthetic gas exchange in an eastern Amazonian rain forest
journal, February 2013
- Domingues, Tomas F.; Martinelli, Luiz A.; Ehleringer, James R.
- Plant Ecology & Diversity, Vol. 7, Issue 1-2
Late‐stage canopy tree species with extremely low δ 13 C and high stomatal sensitivity to seasonal soil drought in the tropical rainforest of French Guiana
journal, May 2000
- Bonal, D.; Barigah, T. S.; Granier, A.
- Plant, Cell & Environment, Vol. 23, Issue 5
Climate Change, Deforestation, and the Fate of the Amazon
journal, January 2008
- Malhi, Y.; Roberts, J. T.; Betts, R. A.
- Science, Vol. 319, Issue 5860
Hyperdominance in Amazonian forest carbon cycling
journal, April 2015
- Fauset, Sophie; Johnson, Michelle O.; Gloor, Manuel
- Nature Communications, Vol. 6, Issue 1
Long-term decline of the Amazon carbon sink
journal, March 2015
- Brienen, R. J. W.; Phillips, O. L.; Feldpausch, T. R.
- Nature, Vol. 519, Issue 7543
Water relations and gas exchange of tropical saplings during a prolonged drought in a Bornean heath forest, with reference to root architecture
journal, January 2000
- Cao, Kun-fang
- Journal of Tropical Ecology, Vol. 16, Issue 1
Effects of rainfall exclusion on leaf gas exchange traits and osmotic adjustment in mature canopy trees of Dryobalanops aromatica (Dipterocarpaceae) in a Malaysian tropical rain forest
journal, May 2017
- Inoue, Yuta; Ichie, Tomoaki; Kenzo, Tanaka
- Tree Physiology, Vol. 37, Issue 10
Drought Sensitivity of the Amazon Rainforest
journal, March 2009
- Phillips, O. L.; Aragao, L. E. O. C.; Lewis, S. L.
- Science, Vol. 323, Issue 5919
On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: Basics and applications of the OJIP fluorescence transient
journal, July 2011
- Stirbet, Alexandrina
- Journal of Photochemistry and Photobiology B: Biology, Vol. 104, Issue 1-2
Drought stress effects on photosystem I content and photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance
journal, October 2009
- Oukarroum, Abdallah; Schansker, Gert; Strasser, Reto J.
- Physiologia Plantarum, Vol. 137, Issue 2
Climate seasonality limits leaf carbon assimilation and wood productivity in tropical forests
journal, January 2016
- Wagner, Fabien H.; Hérault, Bruno; Bonal, Damien
- Biogeosciences, Vol. 13, Issue 8
Seasonal patterns of tropical forest leaf area index and CO 2 exchange : TROPICAL FOREST CO
journal, March 2008
- Doughty, Christopher E.; Goulden, Michael L.
- Journal of Geophysical Research: Biogeosciences, Vol. 113, Issue G1
Seasonal variability of foliar photosynthetic and morphological traits and drought impacts in a Mediterranean mixed forest
journal, April 2015
- Sperlich, D.; Chang, C. T.; Penuelas, J.
- Tree Physiology, Vol. 35, Issue 5
Chlorophyll a fluorescence analysis along a vertical gradient of the crown in a poplar (Oxford clone) subjected to ozone and water stress
journal, July 2012
- Desotgiu, R.; Pollastrini, M.; Cascio, C.
- Tree Physiology, Vol. 32, Issue 8
Flooding of tropical forests in central Amazonia: what do the effects on the photosynthetic apparatus of trees tell us about species suitability for reforestation in extreme environments created by hydroelectric dams?
journal, August 2015
- dos Santos Junior, Ulysses Moreira; Gonçalves, José Francisco de Carvalho; Strasser, Reto J.
- Acta Physiologiae Plantarum, Vol. 37, Issue 8
Responses of tree species to heat waves and extreme heat events: Tree response to extreme heat
journal, September 2014
- Teskey, Robert; Wertin, Timothy; Bauweraerts, Ingvar
- Plant, Cell & Environment, Vol. 38, Issue 9
Death from drought in tropical forests is triggered by hydraulics not carbon starvation
journal, November 2015
- Rowland, L.; da Costa, A. C. L.; Galbraith, D. R.
- Nature, Vol. 528, Issue 7580
In situ temperature relationships of biochemical and stomatal controls of photosynthesis in four lowland tropical tree species
journal, October 2017
- Slot, Martijn; Winter, Klaus
- Plant, Cell & Environment, Vol. 40, Issue 12
Growth, leaf nutrient concentration and photosynthetic nutrient use efficiency in tropical tree species planted in degraded areas in central Amazonia
journal, May 2006
- dos Santos, Ulysses Moreira; de Carvalho Gonçalves, José Francisco; Feldpausch, Ted R.
- Forest Ecology and Management, Vol. 226, Issue 1-3
Optimum air temperature for tropical forest photosynthesis: mechanisms involved and implications for climate warming
journal, May 2017
- Tan, Zheng-Hong; Zeng, Jiye; Zhang, Yong-Jiang
- Environmental Research Letters, Vol. 12, Issue 5
Water deficit in field-grown Gossypium hirsutum primarily limits net photosynthesis by decreasing stomatal conductance, increasing photorespiration, and increasing the ratio of dark respiration to gross photosynthesis
journal, November 2014
- Chastain, Daryl R.; Snider, John L.; Collins, Guy D.
- Journal of Plant Physiology, Vol. 171, Issue 17
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species
journal, June 1980
- Farquhar, G. D.; von Caemmerer, S.; Berry, J. A.
- Planta, Vol. 149, Issue 1
Causes of decreased photosynthetic rate and metabolic capacity in water-deficient leaf cells: a critical evaluation of mechanisms and integration of processes
journal, January 2009
- Lawlor, David W.; Tezara, Wilmer
- Annals of Botany, Vol. 103, Issue 4
An In Situ Leaf and Branch Warming Experiment in the Amazon: Warming Experiment in the Amazon
journal, January 2011
- Doughty, Christopher E.
- Biotropica, Vol. 43, Issue 6
Chlorophyll a fluorescence induction: Can just a one-second measurement be used to quantify abiotic stress responses?
journal, January 2018
- Stirbet, A.; Lazár, D.; Kromdijk, J.
- Photosynthetica, Vol. 56, Issue 1
Modeling water availability for trees in tropical forests
journal, September 2011
- Wagner, Fabien; Hérault, Bruno; Stahl, Clément
- Agricultural and Forest Meteorology, Vol. 151, Issue 9
Drought-Induced Reduction in Global Terrestrial Net Primary Production from 2000 Through 2009
journal, August 2010
- Zhao, M.; Running, S. W.
- Science, Vol. 329, Issue 5994