Plant hydraulics, stomatal control, and the response of a tropical forest to water stress over multiple temporal scales.
El Niño
carbon cycles
evapotranspiration
gross primary productivity
plant hydraulics
stomata control
tropical forest
water stress
Journal
Global change biology
ISSN: 1365-2486
Titre abrégé: Glob Chang Biol
Pays: England
ID NLM: 9888746
Informations de publication
Date de publication:
07 2022
07 2022
Historique:
received:
14
10
2021
accepted:
21
03
2022
pubmed:
5
4
2022
medline:
18
6
2022
entrez:
4
4
2022
Statut:
ppublish
Résumé
Many tropical regions are experiencing an intensification of drought, with increasing severity and frequency. The ecosystem response to these changes is still highly uncertain. On short time scales (from diurnal to seasonal), tropical forests respond to water stress by physiological controls, such as stomatal regulation and phenological adjustment, to cope with increasing atmospheric water demand and reduced water supply. However, the interactions among biological processes and co-varying environmental factors that determine the ecosystem-level fluxes are still unclear. Furthermore, climate variability at longer time scales, such as that generated by ENSO, produces less predictable effects because it depends on a highly stochastic combination of factors that might vary among forests and even between events in the same forest. This study will present some emerging patterns of response to water stress from 5 years of water, carbon, and energy fluxes observed on a seasonal tropical forest in central Panama, including an increase in productivity during the 2015 El Niño. These responses depend on the combination of environmental factors experienced by the forest throughout the seasonal cycle, in particular, increase in solar radiation, stimulating productivity, and increasing vapor pressure deficit (VPD) and decreasing soil moisture, limiting stomata opening. These results suggest a critical role of plant hydraulics in mediating the response to water stress over a broad range of temporal scales (diurnal, intraseasonal, seasonal, and interannual), by acclimating canopy conductance to light and VPD during different soil moisture regimes. A multilayer photosynthesis model coupled with a plant hydraulics scheme can reproduce these complex responses. However, results depend critically on parameters regulating water transport efficiency and the cost of water stress. As these costs have not been properly identified and quantified yet, more empirical research is needed to elucidate physiological mechanisms of hydraulic failure and recover, for example embolism repair and xylem regrowth.
Substances chimiques
Soil
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
4359-4376Informations de copyright
© 2022 John Wiley & Sons Ltd.
Références
Aguilos, M., Hérault, B., Burban, B., Wagner, F., & Bonal, D. (2018). What drives long-term variations in carbon flux and balance in a tropical rainforest in French Guiana? Agricultural & Forest Meteorology, 253-254, 114-123.
Atkin, O. K., Bloomfield, K. J., Reich, P. B., Tjoelker, M. G., Asner, G. P., Bonal, D., Bönisch, G., Bradford, M. G., Cernusak, L. A., Cosio, E. G., Creek, D., Crous, K. Y., Domingues, T. F., Dukes, J. S., Egerton, J. J. G., Evans, J. R., Farquhar, G. D., Fyllas, N. M., Gauthier, P. P. G., … Zaragoza-Castells, J. (2015). Global variability in leaf respiration in relation to climate, plant functional types and leaf traits. New Phytologist, 206, 614-636. https://doi.org/10.1111/nph.13253
Barkhordarian, A., Saatchi, S. S., Behrangi, A., Loikith, P. C., & Mechoso, C. R. (2019). A recent systematic increase in vapor pressure deficit over tropical South America. Scientific Reports, 9, 1-12. https://doi.org/10.1038/s41598-019-51857-8
Barros, F. D. V., Bittencourt, P. R. L., Brum, M., Restrepo-Coupe, N., Pereira, L., Teodoro, G. S., Saleska, S. R., Borma, L. S., Christoffersen, B. O., Penha, D., Alves, L. F., Lima, A. J. N., Carneiro, V. M. C., Gentine, P., Lee, J.-E., Aragão, L. E. O. C., Ivanov, V., Leal, L. S. M., Araujo, A. C., & Oliveira, R. S. (2019). Hydraulic traits explain differential responses of Amazonian forests to the 2015 El Niño-induced drought. New Phytologist, 223, 1253-1266. https://doi.org/10.1111/nph.15909
Bartlett, M. K., Detto, M., & Pacala, S. W. (2019). Predicting shifts in the functional composition of tropical forests under increased drought and CO2 from trade-offs among plant hydraulic traits. Ecology Letters, 22, 67-77.
Bartlett, M. K., Klein, T., Jansen, S., Choat, B., & Sack, L. (2016). The correlations and sequence of plant stomatal, hydraulic, and wilting responses to drought. Proceedings of the National Academy of Sciences of the United States of America, 113, 13098-13103. https://doi.org/10.1073/pnas.1604088113
Beer, C., Reichstein, M., Tomelleri, E., Ciais, P., Jung, M., Carvalhais, N., Rödenbeck, C., Arain, M. A., Baldocchi, D., Bonan, G. B., Bondeau, A., Cescatti, A., Lasslop, G., Lindroth, A., Lomas, M., Luyssaert, S., Margolis, H., Oleson, K. W., Roupsard, O., … Papale, D. (2010). Terrestrial gross carbon dioxide uptake: Global distribution and covariation with climate. Science, 329, 834-838. https://doi.org/10.1126/science.1184984
Bernacchi, C. J., Pimentel, C., & Long, S. P. (2003). In vivo temperature response functions of parameters required to model RuBP-limited photosynthesis. Plant, Cell and Environment, 26, 1419-1430.
Bonal, D., Bosc, A., Ponton, S., Goret, J.-Y., Burban, B., Gross, P., Bonnefond, J.-M., Elbers, J., Longdoz, B., Epron, D., Guehl, J.-M., & Granier, A. (2008). Impact of severe dry season on net ecosystem exchange in the Neotropical rainforest of French Guiana. Global Change Biology, 14, 1917-1933. https://doi.org/10.1111/j.1365-2486.2008.01610.x
Bonal, D., Burban, B., Stahl, C., Wagner, F., & Hérault, B. (2016). The response of tropical rainforests to drought-Lessons from recent research and future prospects. Annals of Forest Science, 73, 27-44. https://doi.org/10.1007/s13595-015-0522-5
Brodersen, C. R., Knipfer, T., & McElrone, A. J. (2018). In vivo visualization of the final stages of xylem vessel refilling in grapevine (Vitis vinifera) stems. New Phytologist, 217, 117-126.
Brodribb, T. J., Powers, J., Cochard, H., & Choat, B. (2020). Hanging by a thread? Forests and drought. Science, 266, 261-266. https://doi.org/10.1126/science.aat7631
Brutsaert, W., & Sugita, M. (1991). A bulk similarity approach in the atmospheric boundary layer using radiometric skin temperature to determine regional surface fluxes. Boundary-Layer Meteorology, 55, 1-23. https://doi.org/10.1007/BF00119324
Cai, W., Borlace, S., Lengaigne, M., van Rensch, P., Collins, M., Vecchi, G., Timmermann, A., Santoso, A., McPhaden, M. J., Wu, L., England, M. H., Wang, G., Guilyardi, E., & Jin, F.-F. (2014). Increasing frequency of extreme El Niño events due to greenhouse warming. Nature Climate Change, 4, 111-116. https://doi.org/10.1038/nclimate2100
Carswell, F. E., Costa, A. L., Palheta, M., Malhi, Y., Meir, P., Costa, J. D. P. R., Ruivo, M. D. L., Leal, L. D. S., Costa, J. M. N., Clement, R. J. & Grace, J. (2002). Seasonality in CO2 and H2O flux at an eastern Amazonian rain forest. Journal of Geophysical Research-Atmospheres, 107, LBA 43-1-LBA 43-16.
Castro, S. M., Sanchez-Azofeifa, G. A., & Sato, H. (2018). Effect of drought on productivity in a Costa Rican tropical dry forest. Environmental Research Letters, 13, 045001.
Cavaleri, M. A., Coble, A. P., Ryan, M. G., Bauerle, W. L., Loescher, H. W., & Oberbauer, S. F. (2017). Tropical rainforest carbon sink declines during El Niño as a result of reduced photosynthesis and increased respiration rates. New Phytologist, 216(1), 136-149. https://doi.org/10.1111/nph.14724
Cavelier, J. (1992). Fine-root biomass and soil properties in a semideciduous and a lower montane rain forest in Panama. Plant and Soil, 142, 187-201. https://doi.org/10.1007/BF00010965
Cheng, Y., Leung, L. R., Huang, M., Koven, C., Detto, M., Knox, R., Bisht, G., Bretfeld, M., & Fisher, R. A. (2021). Modeling the joint effects of vegetation characteristics and soil properties on ecosystem dynamics in a Panama tropical forest. Journal of Advances in Modeling Earth Systems, 14, e2021MS002603.
Christoffersen, B. O., Gloor, M., Fauset, S., Fyllas, N. M., Galbraith, D. R., Baker, T. R., Kruijt, B., Rowland, L., Rosie, F., Binks, O., Sevanto, S., Chonggang, X., Jansen, S., Choat, B., Mencuccini, M., McDowell, N., & Meir, P. (2016). Linking hydraulic traits to tropical forest function in a size-structured and trait-driven model (TFS vol 1-Hydro). Geoscientific Model Development, 9, 4227-4255.
Christoffersen, B. O., Restrepo-Coupe, N., Arain, M. A., Baker, I. T., Cestaro, B. P., Ciais, P., Fisher, J. B., Galbraith, D., Guan, X., Gulden, L., van den Hurk, B., Ichii, K., Imbuzeiro, H., Jain, A., Levine, N., Miguez-Macho, G., Poulter, B., Roberti, D. R., Sakaguchi, K., … Saleska, S. R. (2014). Mechanisms of water supply and vegetation demand govern the seasonality and magnitude of evapotranspiration in Amazonia and Cerrado. Agricultural & Forest Meteorology, 191, 33-50. https://doi.org/10.1016/j.agrformet.2014.02.008
Condit, R., Watts, K., Bohlman, S. A., Pérez, R., Foster, R. B., & Hubbell, S. P. (2000). Quantifying the deciduousness of tropical forest canopies under varying climates. Journal of Vegetation Science, 11, 649-658. https://doi.org/10.2307/3236572
Corlett, R. T. (2016). The impacts of droughts in tropical forests. Trends in Plant Science, 21, 584-593. https://doi.org/10.1016/j.tplants.2016.02.003
Cowan, I. R., & Farquhar, G. D. (1977). Stomatal function in relation to leaf metabolism and environment. Symposia of the Society for Experimental Biology, 31, 471-505.
Crago, R. D., & Qualls, R. J. (2014). Use of land surface temperature to estimate surface energy fluxes: Contributions of Wilfried Brutsaert and collaborators. Water Resources Research, 50, 3396-3408. https://doi.org/10.1002/2013WR015223
Croat, T. B. (1978). Flora of Barro Colorado Island. Bulletin of the Torrey Botanical Club. Stanford University Press, 956 pp.
Cusack, D. F., & Turner, B. L. (2020). Fine root and soil organic carbon depth distributions are inversely related across fertility and rainfall gradients in lowland tropical forests. Ecosystems, 24(5), 1075-1092. https://doi.org/10.1007/s10021-020-00569-6
De Deurwaerder, H. P. T., Visser, M. D., Detto, M., Boeckx, P., Meunier, F., Kuehnhammer, K., Magh, R.-K., Marshall, J. D., Wang, L., Zhao, L., & Verbeeck, H. (2020). Causes and consequences of pronounced variation in the isotope composition of plant xylem water. Biogeosciences, 17(19), 1-47. https://doi.org/10.5194/bg-17-4853-2020
De Pury, D. G. G., & Farquhar, G. D. (1997). Simple scaling of photosynthesis from leaves to canopies without the errors of big-leaf models. Plant, Cell and Environment, 20, 537-557. https://doi.org/10.1111/j.1365-3040.1997.00094.x
Detto, M., Asner, G. P., Muller-landau, H. C., & Sonnentag, O. (2015). Spatial variability in tropical forest leaf area density from multireturn lidar and modeling. Journal of Geophysical Research, 120, 294-309. https://doi.org/10.1002/2014JG002774
Detto, M., Baldocchi, D., & Katul, G. G. G. (2010). Scaling properties of biologically active scalar concentration fluctuations in the atmospheric surface layer over a managed peatland. Boundary-Layer Meteorol, 136, 407-430. https://doi.org/10.1007/s10546-010-9514-z
Detto, M., Wright, S. J., Calderón, O., & Muller-landau, H. C. (2018). Resource acquisition and reproductive strategies of tropical forest in response to the El Niño-Southern Oscillation. Nature Communications, 9, 1-8. https://doi.org/10.1038/s41467-018-03306-9
Eller, C. B., Rowland, L., Oliveira, R. S., Bittencourt, P. R. L., Barros, F. V., da Costa, A. C. L., Meir, P., Friend, A. D., Mencuccini, M., Sitch, S., & Cox, P. (2018). Modelling tropical forest responses to drought and El Niño with a stomatal optimization model based on xylem hydraulics. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1760), 20170315.
Fang, Y., Leung, L. R., Wolfe, B. T., Detto, M., Knox, R. G., McDowell, N. G., Grossiord, C., Xu, C., Christoffersen, B. O., Gentine, P., Koven, C. D., & Chambers, J. Q. (2021). Disentangling the effects of vapor pressure deficit and soil water availability on canopy conductance in a seasonal tropical forest during the 2015 El Niño drought. Journal of Geophysical Research - Atmospheres, 126, 1-20. https://doi.org/10.1029/2021JD035004
Farquhar, G. D., Von Caemmerer, S., & Berry, J. A. (1980). A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta, 149, 78-90. https://doi.org/10.1007/BF00386231
Feng, X., Porporato, A., & Rodriguez-iturbe, I. (2013). Changes in rainfall seasonality in the tropics. Nature Climate Change, 3, 811-815. https://doi.org/10.1038/nclimate1907
Fu, Z., Gerken, T., Bromley, G., Araújo, A., Bonal, D., Burban, B., Ficklin, D., Fuentes, J. D., Goulden, M., Hirano, T., Kosugi, Y., Liddell, M., Nicolini, G., Niu, S., Roupsard, O., Stefani, P., Mi, C., Tofte, Z., Xiao, J., … Stoy, P. C. (2018). The surface-atmosphere exchange of carbon dioxide in tropical rainforests: Sensitivity to environmental drivers and flux measurement methodology. Agricultural & Forest Meteorology, 263, 292-307. https://doi.org/10.1016/j.agrformet.2018.09.001
Garwood, N. C. (2009). Seedlings of Barro Colorado Island and the Neotropics. Cornell university Press.
Goulden, M. L., Miller, S. D., Da Rocha, H. R., Menton, M. C., De Freitas, H. C., Silva Figueira, A. M., & Dias de Sousa, C. A. (2004). Diel and seasonal patterns of tropical forest CO2 exchange. Ecological Applications, 14, 42-54.
Green, J. K., Berry, J., Ciais, P., Zhang, Y., & Gentine, P. (2020). Amazon rainforest photosynthesis increases in response to atmospheric dryness. Science Advances, 6(47), 1-10.
Grossiord, C., Christoffersen, B., Alonso-Rodríguez, A. M., Anderson-Teixeira, K., Asbjornsen, H., Aparecido, L. M. T., Carter Berry, Z., Baraloto, C., Bonal, D., Borrego, I., Burban, B., Chambers, J. Q., Christianson, D. S., Detto, M., Faybishenko, B., Fontes, C. G., Fortunel, C., Gimenez, B. O., Jardine, K. J., … McDowell, N. G. (2019). Precipitation mediates sap flux sensitivity to evaporative demand in the neotropics. Oecologia, 191, 519-530. https://doi.org/10.1007/s00442-019-04513-x
Hagan, M. T., & Menhaj, M. (1994). Training feedforward networks with the Marquardt algorithm. IEEE Transactions on Neural Networks, 5, 989-993. https://doi.org/10.1109/72.329697
Hayek, M. N., Wehr, R., Longo, M., Hutyra, L. R., Wiedemann, K., Munger, J. W., Bonal, D., Saleska, S. R., Fitzjarrald, D. R., & Wofsy, S. C. (2018). A novel correction for biases in forest eddy covariance carbon balance. Agricultural & Forest Meteorology, 250-251, 90-101. https://doi.org/10.1016/j.agrformet.2017.12.186
Houghton, R. A. (2005). Aboveground forest biomass and the global carbon balance. Global Change Biology, 11, 945-958. https://doi.org/10.1111/j.1365-2486.2005.00955.x
Huang, C., Domec, J.-C., Ward, E. J., Duman, T., Manoli, G., Parolari, A. J., & Katul, G. G. (2016). The role of plant water storage on water fluxes within the coupled soil-plant system. New Phytologist, 213, 1-32.
Huang, M., Xu, Y. I., Longo, M., Keller, M., Knox, R. G., Koven, C. D., & Fisher, R. A. (2020). Assessing impacts of selective logging on water, energy, and carbon budgets and ecosystem dynamics in Amazon forests using the functionally assembled terrestrial ecosystem simulator. Biogeosciences, 17, 4999-5023. https://doi.org/10.5194/bg-17-4999-2020
Jackson, R. B., Canadell, J., Ehleringer, J. R., Mooney, H. A., Sala, O. E., & Schulze, E. D. (1996). A global analysis of root distributions for terrestrial biomes. Oecologia, 108, 389-411. https://doi.org/10.1007/BF00333714
Jarvis, P. G. (1976). The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philosophical Transactions of the Royal Society London B: Biological Science, 273, 593-610.
Kaewthongrach, R., Chidthaisong, A., Charuchittipan, D., Vitasse, Y., Sanwangsri, M., Varnakovida, P., Diloksumpun, S., Panuthai, S., Pakoktom, T., Suepai, T., & LeClerc, M. Y. (2020). Impacts of a strong El Niño event on leaf phenology and carbon dioxide exchange in a secondary dry dipterocarp forest. Agricultural and Forest Metrology, 287, 107945.
Katul, G., Manzoni, S., Palmroth, S., & Oren, R. (2010). A stomatal optimization theory to describe the effects of atmospheric CO2 on leaf photosynthesis and transpiration. Annals of Botany, 105, 431-442. https://doi.org/10.1093/aob/mcp292
Keller, M., Alencar, A., Asner, G. P., Braswell, B., Bustamante, M., Davidson, E., Feldpausch, T., Fernandes, E., Goulden, M., Kabat, P., Kruijt, B., Luizão, F., Miller, S., Markewitz, D., Nobre, A. D., Nobre, C. A., Priante Filho, N., da Rocha, H., Silva Dias, P., … Vourlitis, G. L. (2004). Ecological research in the large-scale biosphere-atmosphere experiment in Amazonia: Early results. Ecological Applications, 14, 3-16. https://doi.org/10.1890/03-6003
Klein, T., Zeppel, M. J. B., Anderegg, W. R. L., Bloemen, J., De Kauwe, M. G., Hudson, P., Ruehr, N. K., Powell, T. L., von Arx, G., & Nardini, A. (2018). Xylem embolism refilling and resilience against drought-induced mortality in woody plants: Processes and trade-offs. Ecological Research, 33, 839-855. https://doi.org/10.1007/s11284-018-1588-y
Koehler, B., Corre, M. D., Steger, K., Well, R., Zehe, E., Sueta, J. P., & Veldkamp, E. (2012). An in-depth look into a tropical lowland forest soil: Nitrogen-addition effects on the contents of N2O, CO2 and CH4 and N2O isotopic signatures down to 2-m depth. Biogeochemistry, 111, 695-713. https://doi.org/10.1007/s10533-012-9711-6
Koven, C., Knox, R., Fisher, R., Chambers, J., Christoffersen, B., Davies, S., Detto, M., Dietze, M. C., Faybishenko, B., Holm, J., Huang, M., Kovenock, M., Kueppers, L. M., Lemieux, G., Massoud, E., McDowell, N. G., Muller-Landau, H. C., Needham, J. F., Norby, R. J., … Xu, C. (2019). Benchmarking and parameter sensitivity of physiological and vegetation dynamics using the functionally assembled terrestrial ecosystem simulator (FATES) at Barro Colorado Island, Panama. Biogeosciences Discuss, 17, 1-46.
Kupers, S. J., Wirth, C., Engelbrecht, B. M. J., & Rüger, N. (2019). Dry season soil water potential maps of a 50 hectare tropical forest plot on Barro Colorado Island, Panama. Scientific Data, 6, 1-9. https://doi.org/10.1038/s41597-019-0072-z
Larsen, M. C., Stallard, R. F., & Paton, S. (2021). Lutz Creek watershed, Barro Colorado Island, Republic of Panama. Hydrological Processes, 35, 1-6. https://doi.org/10.1002/hyp.14157
Lasslop, G., Reichstein, M., Detto, M., Richardson, A. D., & Baldocchi, D. D. (2010). Comment on Vickers et al: Self-correlation between assimilation and respiration resulting from flux partitioning of eddy-covariance CO2 fluxes. Agricultural & Forest Meteorology, 150, 312-314. https://doi.org/10.1016/j.agrformet.2009.11.003
Lin, Y.-S., Medlyn, B. E., Duursma, R. A., Prentice, I. C., Wang, H., Baig, S., Eamus, D., de Dios, V. R., Mitchell, P., Ellsworth, D. S., de Beeck, M. O., Wallin, G., Uddling, J., Tarvainen, L., Linderson, M.-L., Cernusak, L. A., Nippert, J. B., Ocheltree, T. W., Tissue, D. T., … Wingate, L. (2015). Optimal stomatal behaviour around the world. Nature Climate Change, 5, 459-464. https://doi.org/10.1038/nclimate2550
Loescher, H. W., Law, B. E., Mahrt, L., Hollinger, D. Y., Campbell, J., & Wofsy, S. C. (2006). Uncertainties in, and interpretation of, carbon flux estimates using the eddy covariance technique. Journal of Geophysical Research - Atmospheres, 111, 1-19. https://doi.org/10.1029/2005JD006932
Malhi, Y., Doughty, C., & Galbraith, D. (2011). The allocation of ecosystem net primary productivity in tropical forests. Philosophical Transactions of the Royal Society B: Biological Sciences, 366, 3225-3245. https://doi.org/10.1098/rstb.2011.0062
Marengo, J. A., Jones, R., Alves, L. M., & Valverde, M. C. (2009). Future change of temperature and precipitation extremes in South America as derived from the precis regional climate modeling system. International Journal of Climatology, 29, 2241-2255. https://doi.org/10.1002/joc.1863
Martínez Cano, I., Shevliakova, E., Malyshev, S., Wright, S. J., Detto, M., Pacala, S. W., & Muller-Landau, H. C. (2020). Allometric constraints and competition enable the simulation of size structure and carbon fluxes in a dynamic vegetation model of tropical forests (LM3PPA-TV). Global Change Biology, 26, 1-17. https://doi.org/10.1111/gcb.15188
Massmann, A., Gentine, P., & Lin, C. (2019). When does vapor pressure deficit drive or reduce evapotranspiration? Journal of Advances in Modeling Earth Systems, 11, 3305-3320. https://doi.org/10.1029/2019MS001790
Mauder, M., Cuntz, M., Drüe, C., Graf, A., Rebmann, C., Schmid, H. P., Schmidt, M., & Steinbrecher, R. (2013). A strategy for quality and uncertainty assessment of long-term eddy-covariance measurements. Agricultural & Forest Meteorology, 169, 122-135. https://doi.org/10.1016/j.agrformet.2012.09.006
Meador, W. E., & Weaver, W. R. (1980). Two-stream approximation to radiative transfer in planetary atmospheres: A unified description of existing methods and a new improvement. Journal of Atmospheric Science, 37, 630-643.
Medlyn, B. E., Dreyer, E., Ellsworth, D., Forstreuter, M., Harley, P. C., Kirschbaum, M. U. F., Le Roux, X., Montpied, P., Strassemeyer, J., Walcroft, A., Wang, K., & Loustau, D. (2002). Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant, Cell and Environment, 25, 1167-1179. https://doi.org/10.1046/j.1365-3040.2002.00891.x
Medlyn, B. E., Duursma, R. A., Eamus, D., Ellsworth, D. S., Prentice, I. C., Barton, C. V. M., Crous, K. Y., De angelis, P., Freeman, M., & Wingate, L. (2011). Reconciling the optimal and empirical approaches to modelling stomatal conductance. Global Change Biology, 17, 2134-2144. https://doi.org/10.1111/j.1365-2486.2010.02375.x
Meinzer, F. C., James, S. A., Goldstein, G., & Woodruff, D. (2003). Whole-tree water transport scales with sapwood capacitance in tropical forest canopy trees. Plant, Cell and Environment, 26, 1147-1155. https://doi.org/10.1046/j.1365-3040.2003.01039.x
Meir, P., Mencuccini, M., & Dewar, R. C. (2015). Drought-related tree mortality: Addressing the gaps in understanding and prediction. New Phytologist, 207, 28-33. https://doi.org/10.1111/nph.13382
Mendes, K. R., Campos, S., da Silva, L. L., Mutti, P. R., Ferreira, R. R., Medeiros, S. S., Perez-Marin, A. M., Marques, T. V., Ramos, T. M., de Lima Vieira, M. M., Oliveira, C. P., Gonçalves, W. A., Costa, G. B., Antonino, A. C. D., Menezes, R. S. C., Bezerra, B. G., & Santos e Silva, C. M. (2020). Seasonal variation in net ecosystem CO2 exchange of a Brazilian seasonally dry tropical forest. Scientific Reports, 10, 1-16. https://doi.org/10.1038/s41598-020-66415-w
Mercado, L. M., Bellouin, N., Sitch, S., Boucher, O., Huntingford, C., Wild, M., & Cox, P. M. (2009). Impact of changes in diffuse radiation on the global land carbon sink. Nature, 458, 1014-1017. https://doi.org/10.1038/nature07949
Moffat, A. M., Papale, D., Reichstein, M., Hollinger, D. Y., Richardson, A. D., Barr, A. G., Beckstein, C., Braswell, B. H., Churkina, G., Desai, A. R., Falge, E., Gove, J. H., Heimann, M., Hui, D., Jarvis, A. J., Kattge, J., Noormets, A., & Stauch, V. J. (2007). Comprehensive comparison of gap-filling techniques for eddy covariance net carbon fluxes. Agricultural & Forest Meteorology, 147, 209-232. https://doi.org/10.1016/j.agrformet.2007.08.011
Monteith, J. I. (1965). Evaporation and environment. Symposia of the Society for Experimental Biology, 19, 205-234.
Norman, J. M. (1980). Interfacing leaf and canopy light interception models. In Predicting photosynthesis for ecosystem models (pp. 49-68). CRC Press.
Novick, K. A., Ficklin, D. L., Stoy, P. C., Williams, C. A., Bohrer, G., Oishi, A. C., Papuga, S. A., Blanken, P. D., Noormets, A., Sulman, B. N., Scott, R. L., Wang, L., & Phillips, R. P. (2016). The increasing importance of atmospheric demand for ecosystem water and carbon fluxes. Nature Climate Change, 6, 1023-1027. https://doi.org/10.1038/nclimate3114
Olchev, A., Ibrom, A., Panferov, O., Gushchina, D., Kreilein, H., Popov, V., Propastin, P., June, T., Rauf, A., & Gravenhorst, G. (2015). Response of CO2 and H2O fluxes in a mountainous tropical rainforest in equatorial Indonesia to El Niño events. Biogeosciences, 12, 6655-6667.
Pan, Y., Birdsey, R. A., Fang, J., Houghton, R., Kauppi, P. E., Kurz, W. A., Phillips, O. L., Shvidenko, A., Lewis, S. L., Canadell, J. G., Ciais, P., Jackson, R. B., Pacala, S. W., McGuire, A. D., Piao, S., Rautiainen, A., Sitch, S., & Hayes, D. (2011). A large and persistent carbon sink in the world’s forests. Science, 333, 988-993. https://doi.org/10.1126/science.1201609
Papale, D., & Valentini, R. (2003). A new assessment of European forests carbon exchanges by eddy fluxes and artificial neural network spatialization. Global Change Biology, 9, 525-535. https://doi.org/10.1046/j.1365-2486.2003.00609.x
Park, J. Y., Muller-Landau, H. C., Lichstein, J. W., Rifai, S. W., Dandois, J. P., & Bohlman, S. A. (2019). Quantifying leaf phenology of individual trees and species in a tropical forest using unmanned aerial vehicle (UAV) images. Remote Sensing, 11, 1534. https://doi.org/10.3390/rs11131534
Pinty, B., Lavergne, T., Dickinson, R. E., Widlowski, J. L., Gobron, N., & Verstraete, M. M. (2006). Simplifying the interaction of land surfaces with radiation for relating remote sensing products to climate models. Journal of Geophysical Research - Atmospheres, 111, 1-20. https://doi.org/10.1029/2005JD005952
Poorter, L., McDonald, I., Alarcón, A., Fichtler, E., Licona, J.-C., Peña-Claros, M., Sterck, F., Villegas, Z., & Sass-Klaassen, U. (2010). The importance of wood traits and hydraulic conductance for the performance and life history strategies of 42 rainforest tree species. New Phytologist, 185, 481-492. https://doi.org/10.1111/j.1469-8137.2009.03092.x
Powell, T. L., Koven, C. D., Johnson, D. J., Faybishenko, B., Fisher, R. A., Knox, R. G., McDowell, N. G., Condit, R., Hubbell, S. P., Wright, S. J., Chambers, J. Q., & Kueppers, L. M. (2018). Variation in hydroclimate sustains tropical forest biomass and promotes functional diversity. New Phytologist, 219, 932-946. https://doi.org/10.1111/nph.15271
Powers, J. S., Vargas G., G., Brodribb, T. J., Schwartz, N. B., Pérez-Aviles, D., Smith-Martin, C. M., Becknell, J. M., Aureli, F., Blanco, R., Calderón-Morales, E., Calvo-Alvarado, J. C., Calvo-Obando, A. J., Chavarría, M. M., Carvajal-Vanegas, D., Jiménez-Rodríguez, C. D., Murillo Chacon, E., Schaffner, C. M., Werden, L. K., Xu, X., & Medvigy, D. (2020). A catastrophic tropical drought kills hydraulically vulnerable tree species. Global Change Biology, 26, 3122-3133. https://doi.org/10.1111/gcb.15037
Qian, X., Qiu, B., & Zhang, Y. (2019). Widespread decline in vegetation photosynthesis in Southeast Asia due to the prolonged drought during the 2015/2016 El Niño. Remote Sensing, 11, 910. https://doi.org/10.3390/rs11080910
Reda, I., & Andreas, A. (2003). Solar position algorithm for solar radiation applications. NREL Report No. TP-560-34302, Revised January 2008, 55 pp.
Restrepo-Coupe, N., Levine, N. M., Christoffersen, B. O., Albert, L. P., Wu, J., Costa, M. H., Galbraith, D., Imbuzeiro, H., Martins, G., da Araujo, A. C., Malhi, Y. S., Zeng, X., Moorcroft, P., & Saleska, S. R. (2017). Do dynamic global vegetation models capture the seasonality of carbon fluxes in the Amazon basin? A data-model intercomparison. Global Change Biology, 23, 191-208. https://doi.org/10.1111/gcb.13442
Roderick, M., Farquhar, G., Berry, S., & Noble, I. (2001). On the direct effect of clouds and atmospheric particles on the productivity and structure of vegetation. Oecologia, 129, 21-30. https://doi.org/10.1007/s004420100760
Rowland, L., Costa, A. C. L., Oliveira, R. S., Bittencourt, P. R. L., Giles, A. L., Coughlin, I., Britto Costa, P., Bartholomew, D., Domingues, T. F., Miatto, R. C., Ferreira, L. V., Vasconcelos, S. S., Junior, J. A. S., Oliveira, A. A. R., Mencuccini, M., & Meir, P. (2020). The response of carbon assimilation and storage to long-term drought in tropical trees is dependent on light availability. Functional Ecology, 35, 43-53. https://doi.org/10.1111/1365-2435.13689
Rowland, L., Martinez-Vilalta, J., & Mencuccini, M. (2021). Hard times for high expectations from hydraulics predicting drought-induced forest. New Phytologist, 230, 1685-1687.
Rubio, V. E., & Detto, M. (2017). Spatiotemporal variability of soil respiration in a seasonal tropical forest. Ecology and Evolution, 7(17), 7104-7116.
Rüger, N., Condit, R., Dent, D. H., DeWalt, S. J., Hubbell, S. P., Lichstein, J. W., Lopez, O. R., Wirth, C., & Farrior, C. E. (2020). Demographic tradeoffs predict tropical forest dynamics. Science, 368, 165-168. https://doi.org/10.1126/science.aaz4797
Sack, L., Cowan, P. D., Jaikumar, N., & Holbrook, N. M. (2003). The “hydrology” of leaves: Co-ordination of structure and function in temperate woody species. Plant, Cell and Environment, 26, 1343-1356. https://doi.org/10.1046/j.0016-8025.2003.01058.x
Sack, L., & Holbrook, N. M. (2006). Leaf hydraulics. Annual Review of Plant Biology, 57, 361-381. https://doi.org/10.1146/annurev.arplant.56.032604.144141
Santiago, L. S., Goldstein, G., Meinzer, F. C., Fisher, J. B., Machado, K., Woodruff, D., & Jones, T. (2004). Leaf photosynthetic traits scale with hydraulic conductivity and wood density in Panamanian forest canopy trees. Oecologia, 140, 543-550. https://doi.org/10.1007/s00442-004-1624-1
Santos, V. A. H. F. D., Ferreira, M. J., Rodrigues, J. V. F. C., Garcia, M. N., Ceron, J. V. B., Nelson, B. W., & Saleska, S. R. (2018). Causes of reduced leaf-level photosynthesis during strong El Niño drought in a Central Amazon forest. Global Change Biology, 24, 4266-4279. https://doi.org/10.1111/gcb.14293
Scoffoni, C., & Sack, L. (2017). The causes and consequences of leaf hydraulic decline with dehydration. Journal of Experimental Botany, 68, 4479-4496. https://doi.org/10.1093/jxb/erx252
Singh, D., Tsiang, M., Rajaratnam, B., & Diffenbaugh, N. S. (2014). Observed changes in extreme wet and dry spells during the south Asian summer monsoon season. Nature Climate Change, 4, 456-461. https://doi.org/10.1038/nclimate2208
Solander, K. C., Newman, B. D., Carioca de Araujo, A., Barnard, H. R., Berry, Z. C., Bonal, D., Bretfeld, M., Burban, B., Antonio Candido, L., Célleri, R., Chambers, J. Q., Christoffersen, B. O., Detto, M., Dorigo, W. A., Ewers, B. E., José Filgueiras Ferreira, S., Knohl, A., Leung, L. R., McDowell, N. G., … Xu, C. (2020). The pantropical response of soil moisture to El Niño. Hydrology and Earth System Sciences, 24, 2303-2322. https://doi.org/10.5194/hess-24-2303-2020
Speckman, H. N., Frank, J. M., Bradford, J. B., Miles, B. L., Massman, W. J., Parton, W. J., & Ryan, M. G. (2015). Forest ecosystem respiration estimated from eddy covariance and chamber measurements under high turbulence and substantial tree mortality from bark beetles. Global Change Biology, 21, 708-721. https://doi.org/10.1111/gcb.12731
Sperry, J. S., Adler, F. R., Campbell, G. S., & Comstock, J. P. (1998). Limitation of plant water use by rhizosphere and xylem conductance: Results from a model. Plant, Cell and Environment, 21, 347-359. https://doi.org/10.1046/j.1365-3040.1998.00287.x
Sperry, J. S., Venturas, M. D., Anderegg, W. R. L., Mencuccini, M., Mackay, D. S., Wang, Y., & Love, D. M. (2016). Predicting stomatal responses to the environment from the optimization of photosynthetic gain and hydraulic cost. Plant, Cell and Environment, 40, 816-830.
Stiegler, C., Meijide, A., Fan, Y., Ali, A. A., June, T., & Knohl, A. (2019). El Niño-southern oscillation (ENSO) event reduces CO2 uptake of an Indonesian oil palm plantation. Biogeosciences, 16, 2873-2890.
Still, C. J., Rastogi, B., Page, G. F. M., Griffith, D. M., Sibley, A., Schulze, M., Hawkins, L., Pau, S., Detto, M., & Helliker, B. R. (2021). Imaging canopy temperature: Shedding (thermal) light on ecosystem processes. New Phytologist, 230(5), 1746-1753. https://doi.org/10.1111/nph.17321
Tang, H., & Dubayah, R. (2017). Light-driven growth in Amazon evergreen forests explained by seasonal variations of vertical canopy structure. Proceedings of the National Academy of Sciences of the United States of America, 114, 2640-2644. https://doi.org/10.1073/pnas.1616943114
Tyree, M. T., Cochard, H., Cruiziat, P., Sinclair, B., & Ameglio, T. (1993). Drought-induced leaf shedding in walnut: Evidence for vulnerability segmentation. Plant, Cell and Environment, 16, 879-882. https://doi.org/10.1111/j.1365-3040.1993.tb00511.x
Wagner, F. H., Hérault, B., Bonal, D., Stahl, C., Anderson, L. O., Baker, T. R., Becker, G. S., Beeckman, H., Boanerges Souza, D., Botosso, P. C., Bowman, D. M. J. S., Bräuning, A., Brede, B., Brown, F. I., Camarero, J. J., Camargo, P. B., Cardoso, F. C. G., Carvalho, F. A., Castro, W., … Aragão, L. E. O. C. (2016). Climate seasonality limits leaf carbon assimilation and wood productivity in tropical forests. Biogeosciences, 13, 2537-2562. https://doi.org/10.5194/bg-13-2537-2016
Walker, A. P., Beckerman, A. P., Gu, L., Kattge, J., Cernusak, L. A., Domingues, T. F., Scales, J. C., Wohlfahrt, G., Wullschleger, S. D., & Ian Woodward, F. (2014). The relationship of leaf photosynthetic traits - Vcmax and Jmax - to leaf nitrogen, leaf phosphorus, and specific leaf area: A meta-analysis and modeling study. Ecology and Evolution, 4, 3218-3235.
Watson, G. S. (1964). Smooth regression analysis. The Indian Journal of Statistics, 26, 359-372.
Wilson, K., Goldstein, A., Falge, E., Aubinet, M., Baldocchi, D., Berbigier, P., Bernhofer, C., Ceulemans, R., Dolman, H., Field, C., Grelle, A., Ibrom, A., Law, B. E., Kowalski, A., Meyers, T., Moncrieff, J., Monson, R., Oechel, W., Tenhunen, J., … Verma, S. (2002). Energy balance closure at FLUXNET sites. Agricultural & Forest Meteorology, 113, 223-243. https://doi.org/10.1016/S0168-1923(02)00109-0
Wirth, R., Weber, B., & Ryel, R. J. (2001). Spatial and temporal variability of canopy structure in a tropical moist forest. Acta Oecologica, 22, 235-244. https://doi.org/10.1016/S1146-609X(01)01123-7
Wolf, A., Anderegg, W. R. L., & Pacala, S. W. (2016). Optimal stomatal behavior with competition for water and risk of hydraulic impairment. Proceedings of the National Academy of Sciences of the United States of America, 113, E7222-E7230. https://doi.org/10.1073/pnas.1615144113
Wolfe, B., Cozzarelli, C. Y., & Jaén Barrios, N. (2021). Stem hydraulic conductivity and vulnerability to cavitation for 26 tree species in Panama.
Wolfe, B. T., Sperry, J. S., & Kursar, T. A. (2016). Does leaf shedding protect stems from cavitation during seasonal droughts? A test of the hydraulic fuse hypothesis. New Phytologist, 212, 1007-1018. https://doi.org/10.1111/nph.14087
Wolfe, B., Wu, J., Ely, K., Serbin, S., Rogers, A., Dickman, T., Collins, A., Detto, M., Grossiord, C., McDowell, N., & Michaletz, S. (2021). Leaf water potential, Feb2016-May2016, PA-SLZ, PA-PNM, PA-BCI: Panama. 1.0. NGEE Tropics Data Collection. (dataset).
Wright, S. J. (1996). Phenological responses to seasonality in tropical forest plants. In S. S. Mulkey, R. L. Chazdon, & A. P. Smith (Eds.), Tropical forest plant ecophysiology (pp. 440-460). Chapman and Hall.
Wright, S. J., & Cornejo, F. (1990). Seasonal drought and leaf fall in a Tropical Forest. Ecology, 71, 1165-1175. https://doi.org/10.2307/1937384
Wright, S. J., & van Schaik, C. P. (1994). Light and the phenology of tropical trees. American Naturalist, 143, 192-199. https://doi.org/10.1086/285600
Wu, J., Albert, L. P., Lopes, A. P., Restrepo-Coupe, N., Hayek, M., Wiedemann, K. T., Guan, K., Stark, S. C., Christoffersen, B., Prohaska, N., Tavares, J. V., Marostica, S., Kobayashi, H., Ferreira, M. L., Campos, K. S., da Silva, R., Brando, P. M., Dye, D. G., Huxman, T. E., … Saleska, S. R. (2016). Leaf development and demography explain photosynthetic seasonality in Amazon evergreen forests. Science, 351, 972-976. https://doi.org/10.1126/science.aad5068
Wu, J., Serbin, S. P., Ely, K. S., Wolfe, B. T., Dickman, L. T., Grossiord, C., Michaletz, S. T., Collins, A. D., Detto, M., McDowell, N. G., Wright, S. J., & Rogers, A. (2020). The response of stomatal conductance to seasonal drought in tropical forests. Global Change Biology, 26, 823-839. https://doi.org/10.1111/gcb.14820
Xu, X., Medvigy, D., Joseph Wright, S., Kitajima, K., Wu, J., Albert, L. P., Martins, G. A., Saleska, S. R., & Pacala, S. W. (2017). Variations of leaf longevity in tropical moist forests predicted by a trait-driven carbon optimality model. Ecology Letters, 20, 1097-1106. https://doi.org/10.1111/ele.12804
Xu, X., Medvigy, D., Powers, J. S., Becknell, J. M., & Guan, K. (2016). Diversity in plant hydraulic traits explains seasonal and inter-annual variations of vegetation dynamics in seasonally dry tropical forests. New Phytologist, 212, 80-95. https://doi.org/10.1111/nph.14009
Yan, J., Zhang, Y., Yu, G., Zhou, G., Zhang, L., Li, K., Tan, Z., & Sha, L. (2013). Seasonal and inter-annual variations in net ecosystem exchange of two old-growth forests in southern China. Agricultural & Forest Meteorology, 182-183, 257-265. https://doi.org/10.1016/j.agrformet.2013.03.002
Yang, J. (2018). Amazon droughts and forest responses: Largely reduced forest photosynthesis but slightly increased canopy greenness during the extreme drought of 2015/2016. Global Change Biology, 12, 3218-3221.
Yuan, H., Dai, Y., Dickinson, R. E., Pinty, B., Shangguan, W., Zhang, S., Wang, L., & Zhu, S. (2017). Reexamination and further development of two-stream canopy radiative transfer models for global land modeling. Journal of Advances in Modeling Earth Systems, 9, 113-129. https://doi.org/10.1002/2016MS000773
Zhu, J., Zhang, M., Zhang, Y., Zeng, X., & Xiao, X. (2018). Response of Tropical terrestrial gross primary production to the super El Niño Event in 2015. Journal of Geophysical Research: Biogeosciences, 123, 3193-3203. https://doi.org/10.1029/2018JG004571