Amazonia trees have limited capacity to acclimate plant hydraulic properties in response to long-term drought.
Amazon rainforest
drought
embolism resistance
hydraulic traits
plant functional diversity
throughfall exclusion
tree size
tropical forest
Journal
Global change biology
ISSN: 1365-2486
Titre abrégé: Glob Chang Biol
Pays: England
ID NLM: 9888746
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
12
09
2019
revised:
30
12
2019
accepted:
02
02
2020
pubmed:
16
2
2020
medline:
17
9
2020
entrez:
16
2
2020
Statut:
ppublish
Résumé
The fate of tropical forests under future climate change is dependent on the capacity of their trees to adjust to drier conditions. The capacity of trees to withstand drought is likely to be determined by traits associated with their hydraulic systems. However, data on whether tropical trees can adjust hydraulic traits when experiencing drought remain rare. We measured plant hydraulic traits (e.g. hydraulic conductivity and embolism resistance) and plant hydraulic system status (e.g. leaf water potential, native embolism and safety margin) on >150 trees from 12 genera (36 species) and spanning a stem size range from 14 to 68 cm diameter at breast height at the world's only long-running tropical forest drought experiment. Hydraulic traits showed no adjustment following 15 years of experimentally imposed moisture deficit. This failure to adjust resulted in these drought-stressed trees experiencing significantly lower leaf water potentials, and higher, but variable, levels of native embolism in the branches. This result suggests that hydraulic damage caused by elevated levels of embolism is likely to be one of the key drivers of drought-induced mortality following long-term soil moisture deficit. We demonstrate that some hydraulic traits changed with tree size, however, the direction and magnitude of the change was controlled by taxonomic identity. Our results suggest that Amazonian trees, both small and large, have limited capacity to acclimate their hydraulic systems to future droughts, potentially making them more at risk of drought-induced mortality.
Substances chimiques
Water
059QF0KO0R
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
3569-3584Subventions
Organisme : Royal Society Newton International Fellowship
ID : NF170370
Pays : International
Organisme : Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Pays : International
Organisme : FAPESP/Microsoft
ID : 11/52072-0
Pays : International
Organisme : NERC Studentship
ID : NE/L002434/1
Pays : International
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 457914/2013-0/MCTI/CNPq/FNDCT/LBA/ESECAFLOR
Pays : International
Organisme : Natural Environment Research Council
ID : NE/J011002/1
Pays : International
Organisme : Ames Research Center NASA
ID : DP170104091
Pays : United States
Organisme : NERC Independent Fellowship
ID : NE/N014022/1
Pays : International
Informations de copyright
© 2020 John Wiley & Sons Ltd.
Références
Adams, H. D., Zeppel, M. J. B., Anderegg, W. R. L., Hartmann, H., Landhäusser, S. M., Tissue, D. T., … McDowell, N. G. (2017). A multi-species synthesis of physiological mechanisms in drought-induced tree mortality. Nature Ecology & Evolution, 1(9), 1285-1291. https://doi.org/10.1038/s41559-017-0248-x
Ambrose, A. R., Sillett, S. C., & Dawson, T. E. (2009). Effects of tree height on branch hydraulics, leaf structure and gas exchange in California redwoods. Plant, Cell & Environment, 32(7), 743-757. https://doi.org/10.1111/j.1365-3040.2009.01950.x
Anderegg, W. R. L., Anderegg, L. D. L., Berry, J. A., & Field, C. B. (2014). Loss of whole-tree hydraulic conductance during severe drought and multi-year forest die-off. Oecologia, 175(1), 11-23. https://doi.org/10.1007/s00442-013-2875-5
Awad, H., Barigah, T., Badel, E., Cochard, H., & Herbette, S. (2010). Poplar vulnerability to xylem cavitation acclimates to drier soil conditions. Physiologia Plantarum. https://doi.org/10.1111/j.1399-3054.2010.01367.x
Barros, F. D. V., Bittencourt, P. R. L., Brum, M., Restrepo-Coupe, N., Pereira, L., Teodoro, G. S., … Oliveira, R. S. (2019). Hydraulic traits explain differential responses of Amazonian forests to the 2015 El Niño-induced drought. New Phytologist, 223(3), 1253-1266. https://doi.org/10.1111/nph.15909
Barton, K. (2016). MuMIn: Multi-model inference. Retrieved from https://cran.r-project.org/web/packages/MuMIn/index.html
Beikircher, B., & Mayr, S. (2009). Intraspecific differences in drought tolerance and acclimation in hydraulics of Ligustrum vulgare and Viburnum lantana. Tree Physiology, 29(6), 765-775. https://doi.org/10.1093/treephys/tpp018
Bennett, A. C., McDowell, N. G., Allen, C. D., & Anderson-Teixeira, K. J. (2015). Larger trees suffer most during drought in forests worldwide. Nature Plants, 1(10), 15139. https://doi.org/10.1038/nplants.2015.139
Binks, O., Meir, P., Rowland, L., Costa, A. C. L., Vasconcelos, S. S., Oliveira, A. A. R., … Mencuccini, M. (2016). Plasticity in leaf-level water relations of tropical rainforest trees in response to experimental drought. New Phytologist, 211(2), 477-488. https://doi.org/10.1111/nph.13927
Binks, O., Mencuccini, M., Rowland, L., Costa, A. C. L., Carvalho, C. J. R., Bittencourt, P., … Meir, P. (2019). Foliar water uptake in Amazonian trees: Evidence and consequences. Global Change Biology, 25(8), 2678-2690. https://doi.org/10.1111/gcb.14666
Bittencourt, P. R., Pereira, L., & Oliveira, R. S. (2016). On xylem hydraulic efficiencies, wood space-use and the safety-efficiency tradeoff. New Phytologist, 211(4), 1152-1155. https://doi.org/10.1111/nph.14044
Bittencourt, P., Pereira, L., & Oliveira, R. (2018). Pneumatic method to measure plant xylem embolism. BIO-PROTOCOL, 8(20). https://doi.org/10.21769/BioProtoc.3059
Brodribb, T. J., & Cochard, H. (2009). Hydraulic failure defines the recovery and point of death in water-stressed conifers. Plant Physiology, 149(1), 575-584. https://doi.org/10.1104/pp.108.129783
Brum, M., Vadeboncoeur, M. A., Ivanov, V., Asbjornsen, H., Saleska, S., Alves, L. F., … Oliveira, R. S. (2019). Hydrological niche segregation defines forest structure and drought tolerance strategies in a seasonal Amazon forest. Journal of Ecology, 107(1), 318-333. https://doi.org/10.1111/1365-2745.13022
Choat, B., Brodribb, T. J., Brodersen, C. R., Duursma, R. A., López, R., & Medlyn, B. E. (2018). Triggers of tree mortality under drought. Nature, 558(7711), 531-539. https://doi.org/10.1038/s41586-018-0240-x
Choat, B., Jansen, S., Brodribb, T. J., Cochard, H., Delzon, S., Bhaskar, R., … Zanne, A. E. (2012). Global convergence in the vulnerability of forests to drought. Nature, 491, 752-755. https://doi.org/10.1038/nature11688
Christoffersen, B. O., Gloor, M., Fauset, S., Fyllas, N. M., Galbraith, D. R., Baker, T. R., … 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 Discussions, 1-60, https://doi.org/10.5194/gmd-2016-128
Ciemer, C., Boers, N., Hirota, M., Kurths, J., Müller-Hansen, F., Oliveira, R. S., & Winkelmann, R. (2019). Higher resilience to climatic disturbances in tropical vegetation exposed to more variable rainfall. Nature Geoscience, 12(3), 174-179. https://doi.org/10.1038/s41561-019-0312-z
Corlett, R. T. (2016). The impacts of droughts in tropical forests. Trends in Plant Science, 21(7), 584-593. https://doi.org/10.1016/j.tplants.2016.02.003
Cruiziat, P., Cochard, H., & Améglio, T. (2002). Hydraulic architecture of trees: Main concepts and results. Annals of Forest Science, 59(7), 723-752. https://doi.org/10.1051/forest:2002060
da Costa, A. C. L., Galbraith, D., Almeida, S., Portela, B. T. T., da Costa, M., de Athaydes Silva Junior, J., … Meir, P. (2010). Effect of 7 yr of experimental drought on vegetation dynamics and biomass storage of an eastern Amazonian rainforest. New Phytologist, 187(3), 579-591. https://doi.org/10.1111/j.1469-8137.2010.03309.x
da Costa, A. C. L., Metcalfe, D. B., Doughty, C. E., de Oliveira, A. A. R., Neto, G. F. C., da Costa, M. C., … Malhi, Y. (2014). Ecosystem respiration and net primary productivity after 8-10 years of experimental through-fall reduction in an eastern Amazon forest. Plant Ecology & Diversity, 7(1-2), 7-24. https://doi.org/10.1080/17550874.2013.798366
Dayer, S., Peña, J. P., Gindro, K., Torregrosa, L., Voinesco, F., Martínez, L., … Zufferey, V. (2017). Changes in leaf stomatal conductance, petiole hydraulics and vessel morphology in grapevine (Vitis vinifera cv. Chasselas) under different light and irrigation regimes. Functional Plant Biology, 44(7), 679. https://doi.org/10.1071/FP16041
Deckmyn, G., Evans, S. P., & Randle, T. J. (2006). Refined pipe theory for mechanistic modeling of wood development. Tree Physiology, 26(6), 703-717. https://doi.org/10.1093/treephys/26.6.703
Delzon, S. (2015). New insight into leaf drought tolerance. Functional Ecology, 29, 1247-1249. https://doi.org/10.1111/1365-2435.12500
Domec, J.-C., Warren, J. M., Meinzer, F. C., & Lachenbruch, B. (2009). Safety factors for xylem failure by implosion and air-seeding within roots, trunks and branches of young and old conifer trees. IAWA Journal, 30(2), 101-120. https://doi.org/10.1163/22941932-90000207
Duffy, P. B., Brando, P., Asner, G. P., & Field, C. B. (2015). Projections of future meteorological drought and wet periods in the Amazon. Proceedings of the National Academy of Sciences of the United States of America, 112(43), 13172-13177. https://doi.org/10.1073/pnas.1421010112
Egea, G., González-real, M. M., Baille, A., Nortes, P. A., Conesa, M. R., & Ruiz-salleres, I. (2012). Effects of water stress on irradiance acclimation of leaf traits in almond trees. Tree Physiology, 32(4), 450-463. https://doi.org/10.1093/treephys/tps016
Eller, C. B., de V Barros, F., Bittencourt, P. R. L., Rowland, L., Mencuccini, M., & Oliveira, R. S. (2018). Xylem hydraulic safety and construction costs determine tropical tree growth: Tree growth vs hydraulic safety trade-off. Plant, Cell & Environment, 41(3), 548-562. https://doi.org/10.1111/pce.13106
Espino, S., & Schenk, H. J. (2011). Mind the bubbles: Achieving stable measurements of maximum hydraulic conductivity through woody plant samples. Journal of Experimental Botany, 62(3), 1119-1132. https://doi.org/10.1093/jxb/erq338
Esquivel-Muelbert, A., Baker, T. R., Dexter, K. G., Lewis, S. L., ter Steege, H., Lopez-Gonzalez, G., … Phillips, O. L. (2017). Seasonal drought limits tree species across the Neotropics. Ecography, 40(5), 618-629. https://doi.org/10.1111/ecog.01904
Fauset, S., Johnson, M. O., Gloor, M., Baker, T. R., Monteagudo, M. A., Brienen, R. J. W., … Phillips, O. L. (2015). Hyperdominance in Amazonian forest carbon cycling. Nature Communications, 6, 6857. https://doi.org/10.1038/ncomms7857
Fisher, R. A., Williams, M., da Costa, A. L., Malhi, Y., da Costa, R. F., Almeida, S., & Meir, P. (2007). The response of an Eastern Amazonian rain forest to drought stress: Results and modelling analyses from a throughfall exclusion experiment. Global Change Biology, 13(11), 2361-2378. https://doi.org/10.1111/j.1365-2486.2007.01417.x
Fisher, R. A., Williams, M., de Lourdes Ruivo, M., de Costa, A. L., & Meir, P. (2008). Evaluating climatic and soil water controls on evapotranspiration at two Amazonian rainforest sites. Agricultural and Forest Meteorology, 148(6-7), 850-861. https://doi.org/10.1016/j.agrformet.2007.12.001
Galbraith, D., Levy, P. E., Sitch, S., Huntingford, C., Cox, P., Williams, M., & Meir, P. (2010). Multiple mechanisms of Amazonian forest biomass losses in three dynamic global vegetation models under climate change. New Phytologist, 187(3), 647-665. https://doi.org/10.1111/j.1469-8137.2010.03350.x
Gaylord, M. L., Kolb, T. E., & McDowell, N. G. (2015). Mechanisms of piñon pine mortality after severe drought: A retrospective study of mature trees. Tree Physiology, 35(8), 806-816. https://doi.org/10.1093/treephys/tpv038
Inoue, Y., Ichie, T., Kenzo, T., Yoneyama, A., Kumagai, T., & Nakashizuka, T. (2017). 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. Tree Physiology, 37(10), 1301-1311. https://doi.org/10.1093/treephys/tpx053
Kumagai, T., Kuraji, K., Noguchi, H., Tanaka, Y., Tanaka, K., & Suzuki, M. (2001). Vertical profiles of environmental factors within tropical rainforest, Lambir Hills National Park, Sarawak, Malaysia. Journal of Forest Research, 6(4), 257-264. https://doi.org/10.1007/BF02762466
Li, X., Blackman, C. J., Rymer, P. D., Quintans, D., Duursma, R. A., Choat, B., … Tissue, D. T. (2018). Xylem embolism measured retrospectively is linked to canopy dieback in natural populations of Eucalyptus piperita following drought. Tree Physiology, 38(8), 1193-1199. https://doi.org/10.1093/treephys/tpy052
Lopes, A. V., Chiang, J. C. H., Thompson, S. A., & Dracup, J. A. (2016). Trend and uncertainty in spatial-temporal patterns of hydrological droughts in the Amazon basin: Hydrological droughts in the Amazon. Geophysical Research Letters, 43(7), 3307-3316. https://doi.org/10.1002/2016GL067738
Malhi, Y., Aragao, L. E. O. C., Galbraith, D., Huntingford, C., Fisher, R., Zelazowski, P., … Meir, P. (2009). Exploring the likelihood and mechanism of a climate-change-induced dieback of the Amazon rainforest. Proceedings of the National Academy of Sciences of the United States of America, 106(49), 20610-20615. https://doi.org/10.1073/pnas.0804619106
Marengo, J. A., Souza, C. M., Thonicke, K., Burton, C., Halladay, K., Betts, R. A., … Soares, W. R. (2018). Changes in climate and land use over the Amazon region: Current and future variability and trends. Frontiers in Earth Science, 6, https://doi.org/10.3389/feart.2018.00228
Martin-StPaul, N. K., Longepierre, D., Huc, R., Delzon, S., Burlett, R., Joffre, R., … Cochard, H. (2014). How reliable are methods to assess xylem vulnerability to cavitation? The issue of ‘open vessel’ artifact in oaks. Tree Physiology, 34(8), 894-905. https://doi.org/10.1093/treephys/tpu059
Maseda, P. H., & Fernandez, R. J. (2006). Stay wet or else: Three ways in which plants can adjust hydraulically to their environment. Journal of Experimental Botany, 57(15), 3963-3977. https://doi.org/10.1093/jxb/erl127
McDowell, N. G., & Allen, C. D. (2015). Darcy's law predicts widespread forest mortality under climate warming. Nature Climate Change, 5(7), 669-672. https://doi.org/10.1038/nclimate2641
Meinzer, F. C., & McCulloh, K. A. (2013). Xylem recovery from drought-induced embolism: Where is the hydraulic point of no return? Tree Physiology, 33(4), 331-334. https://doi.org/10.1093/treephys/tpt022
Meir, P., Mencuccini, M., Binks, O., da Costa, A. L., Ferreira, L., & Rowland, L. (2018). Short-term effects of drought on tropical forest do not fully predict impacts of repeated or long-term drought: Gas exchange versus growth. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1760), 20170311. https://doi.org/10.1098/rstb.2017.0311
Meir, P., Wood, T. E., Galbraith, D. R., Brando, P. M., Da Costa, A. C. L., Rowland, L., & Ferreira, L. V. (2015). Threshold responses to soil moisture deficit by trees and soil in tropical rain forests: Insights from field experiments. BioScience, 65(9), 882-892. https://doi.org/10.1093/biosci/biv107
Nepstad, D. C., Tohver, I. M., Ray, D., Moutinho, P., & Cardinot, G. (2007). Mortality of large trees and lianas following experimental drought in an Amazon forest. Ecology, 88(9), 2259-2269. https://doi.org/10.1890/06-1046.1
Nieuwenhuis, R., te Grotenhuis, M., & Pelzer, B. (2012). Influence.ME: Tools for detecting influential data in mixed effects models. R Journal, 4(2), 38. https://doi.org/10.32614/rj-2012-011
Olson, M. E., Soriano, D., Rosell, J. A., Anfodillo, T., Donoghue, M. J., Edwards, E. J., … Méndez-Alonzo, R. (2018). Plant height and hydraulic vulnerability to drought and cold. Proceedings of the National Academy of Sciences of the United States of America, 115(29), 7551-7556. https://doi.org/10.1073/pnas.1721728115
Pammenter, N. W., & Vander Willigen, C. (1998). A mathematical and statistical analysis of the curves illustrating vulnerability of xylem to cavitation. Tree Physiology, 18(8-9), 589-593. https://doi.org/10.1093/treephys/18.8-9.589
Pereira, L., Bittencourt, P. R. L., Oliveira, R. S., Junior, M. B. M., Barros, F. V., Ribeiro, R. V., & Mazzafera, P. (2016). Plant pneumatics: Stem air flow is related to embolism - New perspectives on methods in plant hydraulics. New Phytologist, 211(1), 357-370. https://doi.org/10.1111/nph.13905
Pereira, L., & Mazzafera, P. (2012). A low cost apparatus for measuring the xylem hydraulic conductance in plants. Bragantia, 71(4), 583-587. https://doi.org/10.1590/S0006-87052013005000006
Pérez-Harguindeguy, N., Díaz, S., Garnier, E., Lavorel, S., Poorter, H., Jaureguiberry, P., … Cornelissen, J. H. C. (2013). New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany, 61(3), 167. https://doi.org/10.1071/BT12225
Phillips, O. L., van der Heijden, G., Lewis, S. L., López-González, G., Aragão, L. E. O. C., Lloyd, J., … Vilanova, E. (2010). Drought-mortality relationships for tropical forests. New Phytologist, 187(3), 631-646. https://doi.org/10.1111/j.1469-8137.2010.03359.x
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., & R Core Team. (2014). Nlme: Linear and nonlinear mixed effects models. R package version 3.1-118. Retrieved from http://CRAN.R-project.org/package=nlme
Prendin, A. L., Mayr, S., Beikircher, B., von Arx, G., & Petit, G. (2018). Xylem anatomical adjustments prioritize hydraulic efficiency over safety as Norway spruce trees grow taller. Tree Physiology, 38(8), 1088-1097. https://doi.org/10.1093/treephys/tpy065
R Core Team. (2016). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/
Rowland, L., da Costa, A., Oliveira, R., Bittencourt, P., Giles, A., Coughlin, I., … Meir, P. (under revision). The response of carbon assimilation and storage to long-term drought in tropical trees is dependent on light availability. Functional Ecology.
Rowland, L., da Costa, A. C. L., Galbraith, D. R., Oliveira, R. S., Binks, O. J., Oliveira, A. A. R., … Meir, P. (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
Rowland, L., Lobo-do-Vale, R. L., Christoffersen, B. O., Melém, E. A., Kruijt, B., Vasconcelos, S. S., … Meir, P. (2015). After more than a decade of soil moisture deficit, tropical rainforest trees maintain photosynthetic capacity, despite increased leaf respiration. Global Change Biology, 21(12), 4662-4672. https://doi.org/10.1111/gcb.13035
Schneider, C. A., Rasband, W. S., & Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nature Methods, 9(7), 671-675. https://doi.org/10.1038/nmeth.2089
Scholz, F. G., Bucci, S. J., Goldstein, G., Meinzer, F. C., Franco, A. C., & Miralles-Wilhelm, F. (2007). Biophysical properties and functional significance of stem water storage tissues in Neotropical savanna trees. Plant, Cell & Environment, 30(2), 236-248. https://doi.org/10.1111/j.1365-3040.2006.01623.x
Schuldt, B., Leuschner, C., Horna, V., Moser, G., Köhler, M., van Straaten, O., & Barus, H. (2011). Change in hydraulic properties and leaf traits in a tall rainforest tree species subjected to long-term throughfall exclusion in the perhumid tropics. Biogeosciences, 8(8), 2179-2194. https://doi.org/10.5194/bg-8-2179-2011
Smith, N. G., & Dukes, J. S. (2013). Plant respiration and photosynthesis in global-scale models: Incorporating acclimation to temperature and CO2. Global Change Biology, 19(1), 45-63. https://doi.org/10.1111/j.1365-2486.2012.02797.x
Sperry, J. S., Donnelly, J. R., & Tyree, M. T. (1988). A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell and Environment, 11(1), 35-40. https://doi.org/10.1111/j.1365-3040.1988.tb01774.x
Sperry, J. S., & Love, D. M. (2015). What plant hydraulics can tell us about responses to climate-change droughts. New Phytologist, 207(1), 14-27. https://doi.org/10.1111/nph.13354
Sterck, F., Anten, N. P. R., Schieving, F., & Zuidema, P. A. (2016). Trait acclimation mitigates mortality risks of tropical canopy trees under global warming. Frontiers in Plant Science, 7. https://doi.org/10.3389/fpls.2016.00607
ter Steege, H., Pitman, N. C. A., Sabatier, D., Baraloto, C., Salomao, R. P., Guevara, J. E., … Silman, M. R. (2013). Hyperdominance in the Amazonian tree flora. Science, 342(6156), 1243092. https://doi.org/10.1126/science.1243092
Thomas, R., Lello, J., Medeiros, R., Pollard, A., Robinson, P., Seward, A., … Vaughan, I. (2017). Data analysis with R statistical software: A guidebook for scientists. Cardiff, UK: Eco-Explore.
Tng, D. Y. P., Apgaua, D. M. G., Ishida, Y. F., Mencuccini, M., Lloyd, J., Laurance, W. F., & Laurance, S. G. W. (2018). Rainforest trees respond to drought by modifying their hydraulic architecture. Ecology and Evolution. https://doi.org/10.1002/ece3.4601
Tomasella, M., Beikircher, B., Häberle, K.-H., Hesse, B., Kallenbach, C., Matyssek, R., & Mayr, S. (2018). Acclimation of branch and leaf hydraulics in adult Fagus sylvatica and Picea abies in a forest through-fall exclusion experiment. Tree Physiology, 38(2), 198-211. https://doi.org/10.1093/treephys/tpx140
Urli, M., Porte, A. J., Cochard, H., Guengant, Y., Burlett, R., & Delzon, S. (2013). Xylem embolism threshold for catastrophic hydraulic failure in angiosperm trees. Tree Physiology, 33(7), 672-683. https://doi.org/10.1093/treephys/tpt030
Venturas, M. D., Mackinnon, E. D., Jacobsen, A. L., & Pratt, R. B. (2015). Excising stem samples underwater at native tension does not induce xylem cavitation: No evidence for a tension-cutting artefact. Plant, Cell & Environment, 38(6), 1060-1068. https://doi.org/10.1111/pce.12461
Way, D. A., & Yamori, W. (2014). Thermal acclimation of photosynthesis: On the importance of adjusting our definitions and accounting for thermal acclimation of respiration. Photosynthesis Research, 119(1-2), 89-100. https://doi.org/10.1007/s11120-013-9873-7
Yue, X., Zuo, X., Yu, Q., Xu, C., Lv, P., Zhang, J., … Smith, M. D. (2019). Response of plant functional traits of Leymus chinensis to extreme drought in Inner Mongolia grasslands. Plant Ecology, 220(2), 141-149. https://doi.org/10.1007/s11258-018-0887-2
Zach, A., Schuldt, B., Brix, S., Horna, V., Culmsee, H., & Leuschner, C. (2010). Vessel diameter and xylem hydraulic conductivity increase with tree height in tropical rainforest trees in Sulawesi, Indonesia. Flora - Morphology, Distribution, Functional Ecology of Plants, 205(8), 506-512. https://doi.org/10.1016/j.flora.2009.12.008
Zhang, Y. A., Lamarque, L. J., Torres-Ruiz, J. M., Schuldt, B., Karimi, Z., Li, S., … Jansen, S. (2018). Testing the plant pneumatic method to estimate xylem embolism resistance in stems of temperate trees. Tree Physiology, 38(7), 1016-1025. https://doi.org/10.1093/treephys/tpy015
Zhou, S.-X., Medlyn, B. E., & Prentice, I. C. (2016). Long-term water stress leads to acclimation of drought sensitivity of photosynthetic capacity in xeric but not riparian Eucalyptus species. Annals of Botany, 117(1), 133-144. https://doi.org/10.1093/aob/mcv161
Zuur, A., Ieno, E., Walker, N., Saveliev, A., & Smith, G. (2009). Mixed effects models and extensions in ecology with R. New York, NY: Springer Verlag.