Stability of tropical forest tree carbon-water relations in a rainfall exclusion treatment through shifts in effective water uptake depth.
drought
gas exchange
nonstructural carbohydrates
plant hydraulics
process model
rainfall exclusion
rooting depth
turgor loss point
water potentials
wet 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:
12 2021
12 2021
Historique:
revised:
23
08
2021
received:
25
11
2020
accepted:
25
08
2021
pubmed:
2
9
2021
medline:
18
11
2021
entrez:
1
9
2021
Statut:
ppublish
Résumé
Increasing severity and frequency of drought is predicted for large portions of the terrestrial biosphere, with major impacts already documented in wet tropical forests. Using a 4-year rainfall exclusion experiment in the Daintree Rainforest in northeast Australia, we examined canopy tree responses to reduced precipitation and soil water availability by quantifying seasonal changes in plant hydraulic and carbon traits for 11 tree species between control and drought treatments. Even with reduced soil volumetric water content in the upper 1 m of soil in the drought treatment, we found no significant difference between treatments for predawn and midday leaf water potential, photosynthesis, stomatal conductance, foliar stable carbon isotope composition, leaf mass per area, turgor loss point, xylem vessel anatomy, or leaf and stem nonstructural carbohydrates. While empirical measurements of aboveground traits revealed homeostatic maintenance of plant water status and traits in response to reduced soil moisture, modeled belowground dynamics revealed that trees in the drought treatment shifted the depth from which water was acquired to deeper soil layers. These findings reveal that belowground acclimation of tree water uptake depth may buffer tropical rainforests from more severe droughts that may arise in future with climate change.
Substances chimiques
Water
059QF0KO0R
Carbon
7440-44-0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
6454-6466Informations de copyright
© 2021 John Wiley & Sons Ltd.
Références
Anderegg, W. R. L., Klein, T., Bartlett, M., Sack, L., Pellegrini, A. F. A., Choat, B., & Jansen, S. (2016). Meta-analysis reveals that hydraulic traits explain cross-species patterns of drought-induced tree mortality across the globe. Proceedings of the National Academy of Sciences of the United States of America, 113(18), 2-7. https://doi.org/10.1073/pnas.1525678113
Barbeta, A., Mejía-Chang, M., Ogaya, R., Voltas, J., Dawson, T. E., & Peñuelas, J. (2015). The combined effects of a long-term experimental drought and an extreme drought on the use of plant-water sources in a Mediterranean forest. Global Change Biology, 21(3), 1213-1225. https://doi.org/10.1111/gcb.12785
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(46), 13098-13103. https://doi.org/10.1073/pnas.1604088113
Blackman, C. J., Creek, D., Maier, C., Aspinwall, M. J., Drake, J. E., Pfautsch, S., O’Grady, A., Delzon, S., Medlyn, B. E., Tissue, D. T., Choat, B., & Meinzer, F. (2019). Drought response strategies and hydraulic traits contribute to mechanistic understanding of plant dry-down to hydraulic failure. Tree Physiology, 39(6), 910-924. https://doi.org/10.1093/treephys/tpz016
Bouche, P. S., Larter, M., Domec, J. C., Burlett, R., Gasson, P., Jansen, S., & Delzon, S. (2014). A broad survey of hydraulic and mechanical safety in the xylem of conifers. Journal of Experimental Botany, 65(15), 4419-4431. https://doi.org/10.1093/jxb/eru218
Brienen, R. J. W., Phillips, O. L., Feldpausch, T. R., Gloor, E., Baker, T. R., Lloyd, J., Lopez-Gonzalez, G., Monteagudo-Mendoza, A., Malhi, Y., Lewis, S. L., Vásquez Martinez, R., Alexiades, M., Álvarez Dávila, E., Alvarez-Loayza, P., Andrade, A., Aragão, L. E. O. C., Araujo-Murakami, A., Arets, E. J. M. M., Arroyo, L., … Zagt, R. J. (2015). Long-term decline of the Amazon carbon sink. Nature, 519(7543), 344-348. https://doi.org/10.1038/nature14283
Canadell, J., Jackson, R. B. B., Ehleringer, J. R., Mooney, H. A. A., Sala, O. E. E., & Schulze, E. D. (1996). Maximum rooting depth of vegetation types at the global scale. Oecologia, 108(4), 583-595. https://doi.org/10.1007/BF00329030
Cheesman, A. W., Duff, H., Hill, K., Cernusak, L. A., & McInerney, F. A. (2020). Isotopic and morphologic proxies for reconstructing light environment and leaf function of fossil leaves: A modern calibration in the Daintree Rainforest, Australia. American Journal of Botany, 107(8), 1165-1176. https://doi.org/10.1002/ajb2.1523
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., Bucci, S. J., Feild, T. S., Gleason, S. M., Hacke, U. G., Jacobsen, A. L., Lens, F., Maherali, H., Martínez-Vilalta, J., Mayr, S., Mencuccini, M., Mitchell, P. J., Nardini, A., Pittermann, J., … Zanne, A. E. (2012). Global convergence in the vulnerability of forests to drought. Nature, 491(7426), 752-755. https://doi.org/10.1038/nature11688
Crausbay, S. D., Ramirez, A. R., Carter, S. L., Cross, M. S., Hall, K. R., Bathke, D. J., Betancourt, J. L., Colt, S., Cravens, A. E., Dalton, M. S., Dunham, J. B., Hay, L. E., Hayes, M. J., McEvoy, J., McNutt, C. A., Moritz, M. A., Nislow, K. H., Raheem, N., & Sanford, T. (2017). Defining ecological drought for the twenty-first century. Bulletin of the American Meteorological Society, 98(12), 2543-2550. https://doi.org/10.1175/BAMS-D-16-0292.1
Cuddington, K., Fortin, M.-J., Gerber, L. R., Hastings, A., Liebhold, A., O'Connor, M., & Ray, C. (2013). Process-based models are required to manage ecological systems in a changing world. Ecosphere, 4(2), 1-12. https://doi.org/10.1890/ES12-00178.1
da Costa, A. C. L., Galbraith, D., Almeida, S., Portela, B. T. T., da Costa, M., de Athaydes Silva Junior, J., Braga, A. P., de Gonçalves, P. H. L., de Oliveira, A. A. R., Fisher, R., Phillips, O. L., Metcalfe, D. B., Levy, P., & 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
David, T. S., Henriques, M. O., Kurz-Besson, C., Nunes, J., Valente, F., Vaz, M., Pereira, J. S., Siegwolf, R., Chaves, M. M., Gazarini, L. C., & David, J. S. (2007). Water-use strategies in two co-occurring Mediterranean evergreen oaks: Surviving the summer drought. Tree Physiology, 27(6), 793-803. https://doi.org/10.1093/treephys/27.6.793
Dickman, L. T., McDowell, N. G., Grossiord, C., Collins, A. D., Wolfe, B. T., Detto, M., Wright, S. J., Medina-Vega, J. A., Goodsman, D., Rogers, A., Serbin, S. P., Wu, J., Ely, K. S., Michaletz, S. T., Xu, C., Kueppers, L., & Chambers, J. Q. (2019). Homoeostatic maintenance of nonstructural carbohydrates during the 2015-2016 El Niño drought across a tropical forest precipitation gradient. Plant Cell and Environment, 42(5), 1705-1714. https://doi.org/10.1111/pce.13501
Domec, J. C., & Gartner, B. L. (2002). Age- and position-related changes in hydraulic versus mechanical dysfunction of xylem: Inferring the design criteria for Douglas-fir wood structure. Tree Physiology, 22(2-3), 91-104. https://doi.org/10.1093/treephys/22.2-3.91
Duursma, R. A. (2015). Plantecophys - An R package for analysing and modelling leaf gas exchange data. PLoS ONE, 10(11), 1-13. https://doi.org/10.1371/journal.pone.0143346
Duursma, R., & Choat, B. (2017). fitplc - an R package to fit hydraulic vulnerability curves. Journal of Plant Hydraulics, 4, e002. https://doi.org/10.20870/jph.2017.e002
Eggemeyer, K. D., Awada, T., Harvey, F. E., Wedin, D. A., Zhou, X., & Zanner, C. W. (2009). Seasonal changes in depth of water uptake for encroaching trees Juniperus virginiana and Pinus ponderosa and two dominant C4 grasses in a semiarid grassland. Tree Physiology, 29(2), 157-169. https://doi.org/10.1093/treephys/tpn019
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
Franks, P. J., Drake, P. L., & Froend, R. H. (2007). Anisohydric but isohydrodynamic: Seasonally constant plant water potential gradient explained by a stomatal control mechanism incorporating variable plant hydraulic conductance. Plant, Cell and Environment, 30(1), 19-30. https://doi.org/10.1111/j.1365-3040.2006.01600.x
Hammond, W. M., Yu, K., Wilson, L. A., Will, R. E., Anderegg, W. R. L., & Adams, H. D. (2019). Dead or dying? Quantifying the point of no return from hydraulic failure in drought-induced tree mortality. New Phytologist, 223(4), 1834-1843. https://doi.org/10.1111/nph.15922
Hoch, G., Popp, M., & Körner, C. (2002). Altitudinal increase of mobile carbon pools in Pinus cembra suggests sink limitation of growth at the Swiss treeline. Oikos, 98(3), 361-374. https://doi.org/10.1034/j.1600-0706.2002.980301.x
Hubau, W., Lewis, S. L., Phillips, O. L., Affum-Baffoe, K., Beeckman, H., Cuní-Sanchez, A., Daniels, A. K., Ewango, C. E. N., Fauset, S., Mukinzi, J. M., Sheil, D., Sonké, B., Sullivan, M. J. P., Sunderland, T. C. H., Taedoumg, H., Thomas, S. C., White, L. J. T., Abernethy, K. A., Adu-Bredu, S., … Zemagho, L. (2020). Asynchronous carbon sink saturation in African and Amazonian tropical forests. Nature, 579(7797), 80-87. https://doi.org/10.1038/s41586-020-2035-0
Johnson, D. M., Domec, J. C., Carter Berry, Z., Schwantes, A. M., McCulloh, K. A., Woodruff, D. R., Wayne Polley, H., Wortemann, R., Swenson, J. J., Scott Mackay, D., McDowell, N. G., & Jackson, R. B. (2018). Co-occurring woody species have diverse hydraulic strategies and mortality rates during an extreme drought. Plant Cell and Environment, 41(3), 576-588. https://doi.org/10.1111/pce.13121
Klein, T., Rotenberg, E., Cohen-Hilaleh, E., Raz-Yaseef, N., Tatarinov, F., Preisler, Y., Ogée, J., Cohen, S., & Yakir, D. (2014). Quantifying transpirable soil water and its relations to tree water use dynamics in a water-limited pine forest. Ecohydrology, 7(2), 409-419. https://doi.org/10.1002/eco.1360
Laidlaw, M., Kitching, R., Goodall, K., Small, A., & Stork, N. (2007). Temporal and spatial variation in an Australian tropical rainforest. Austral Ecology, 32(1), 10-20. https://doi.org/10.1111/j.1442-9993.2007.01739.x
Landhäusser, S. M., Chow, P. S., Turin Dickman, L., Furze, M. E., Kuhlman, I., Schmid, S., Wiesenbauer, J., Wild, B., Gleixner, G., Hartmann, H., Hoch, G., McDowell, N. G., Richardson, A. D., Richter, A., & Adams, H. D. (2018). Standardized protocols and procedures can precisely and accurately quantify non-structural carbohydrates. Tree Physiology, 38(12), 1764-1778. https://doi.org/10.1093/treephys/tpy118
Leff, R. (2020). ezSperry-beta. https://github.com/RileyLeff/ezSperry-beta
Liddell, M. J. (2015). Soil pit data, soil characterisation, far north Queensland rainforest SuperSite, daintree rainforest observatory, cape tribulation, 2006, version 5. TERN Australian SuperSite Network. http://supersites.tern.org.au/knb/metacat/supersite.64/html
Liddell, M. J., & Laurance, S. (2015). Leaf area index data, far north queensland rainforest supersite, daintree rainforest observatory, cape tribulation, core 1 ha, 2014. TERN Australian SuperSite Network. http://supersites.tern.org.au/knb/metacat/supersite.238.13/html
Love, D. M., Venturas, M. D., Sperry, J. S., Brooks, P. D., Pettit, J. L., Wang, Y., Anderegg, W. R. L., Tai, X., & Mackay, D. S. (2019). Dependence of aspen stands on a subsurface water subsidy: Implications for climate change impacts. Water Resources Research, 55(3), 1833-1848. https://doi.org/10.1029/2018WR023468
Mackay, D. S., Savoy, P. R., Grossiord, C., Tai, X., Pleban, J. R., Wang, D. R., McDowell, N. G., Adams, H. D., & Sperry, J. S. (2020). Conifers depend on established roots during drought: Results from a coupled model of carbon allocation and hydraulics. New Phytologist, 225(2), 679-692. https://doi.org/10.1111/nph.16043
McAdam, S. A. (2015). Physiochemical quantification of Abscisic Acid levels in plant tissues with an added internal standard by ultra-performance liquid chromatography. Bio-Protocol, 5(18), e1599. https://doi.org/10.21769/BioProtoc.1599
McAdam, S. A., & Brodribb, T. J. (2014). Separating active and passive influences on stomatal control of transpiration. Plant Physiology, 164(4), 1578-1586. https://doi.org/10.1104/pp.113.231944
McDowell, N. G., Allen, C. D., Anderson-Teixeira, K., Aukema, B. H., Bond-Lamberty, B., Chini, L., Clark, J. S., Dietze, M., Grossiord, C., Hanbury-Brown, A., Hurtt, G. C., Jackson, R. B., Johnson, D. J., Kueppers, L., Lichstein, J. W., Ogle, K., Poulter, B., Pugh, T. A. M., Seidl, R., … Xu, C. (2020). Pervasive shifts in forest dynamics in a changing world. Science, 368(964), eaaz9463. https://doi.org/10.1126/science.aaz9463
McDowell, N. G., Beerling, D. J., Breshears, D. D., Fisher, R. A., Raffa, K. F., & Stitt, M. (2011). The interdependence of mechanisms underlying climate-driven vegetation mortality. Trends in Ecology & Evolution, 26(10), 523-532. https://doi.org/10.1016/j.tree.2011.06.003
Meir, P., Brando, P. M., Nepstad, D., Vasconcelos, S., Costa, A. C. L., Davidson, E., Almeida, S., Fisher, R. A., Sotta, E. D., Zarin, D., & Cardinot, G. (2009). The effects of drought on Amazonian rain forests. Amazonia and Global Change, 429-449. https://doi.org/10.1029/2009GM000882
Meir, P., Mencuccini, M., & Dewar, R. D. (2015). Drought-related tree mortality: addressing the gaps in understanding and prediction. New Phytologist, 207, 28-33. https://doi.org/10.1111/nph.13382
Meir, P., & Woodward, F. I. (2010). Amazonian rain forests and drought: Response and vulnerability. New Phytologist, 187(3), 553-557. https://doi.org/10.1111/j.1469-8137.2010.03390.x
Mencuccini, M. (2003). The ecological significance of long-distance water transport: Short-term regulation, long-term acclimation and the hydraulic costs of stature across plant life forms. Plant, Cell and Environment, 26(1), 163-182. https://doi.org/10.1046/j.1365-3040.2003.00991.x
Nepstad, D. C. (2002). The effects of partial throughfall exclusion on canopy processes, aboveground production, and biogeochemistry of an Amazon forest. Journal of Geophysical Research, 107(D20), 1-18. https://doi.org/10.1029/2001jd000360
Peters, J. M. R., López, R., Nolf, M., Hutley, L. B., Wardlaw, T., Cernusak, L. A., & Choat, B. (2021). Living on the edge: A continental-scale assessment of forest vulnerability to drought. Global Change Biology, 27(15), 3620-3641. https://doi.org/10.1111/gcb.15641
Phillips, O. L., van der Heijden, G., Lewis, S. L., López-González, G., Aragão, L. E. O. C., Lloyd, J., Malhi, Y., Monteagudo, A., Almeida, S., Dávila, E. A., Amaral, I., Andelman, S., Andrade, A., Arroyo, L., Aymard, G., Baker, T. R., Blanc, L., Bonal, D., de Oliveira, Á. C. A., … Vilanova, E. (2010). Drought-mortality relationships for tropical forests. New Phytologist, 187, 631-646. https://doi.org/10.1111/j.1469-8137.2010.03359.x
Pivovaroff, A. L., Pasquini, S. C., De Guzman, M. E., Alstad, K. P., Stemke, J. S., & Santiago, L. S. (2016). Multiple strategies for drought survival among woody plant species. Functional Ecology, 30(4), 517-526. https://doi.org/10.1111/1365-2435.12518
Pivovaroff, A. L., Wolfe, B. T., McDowell, N., Christoffersen, B., Davies, S., Dickman, L. T., Grossiord, C., Leff, R. T., Rogers, A., Serbin, S. P., Wright, S. J., Wu, J., Xu, C., & Chambers, J. Q. (2021). Hydraulic architecture explains species moisture dependency but not mortality rates across a tropical rainfall gradient. Biotropica, 53(4), 1213-1225. https://doi.org/10.1111/btp.12964
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(5), 3122-3133. https://doi.org/10.1111/gcb.15037
Poyatos, R., Aguadé, D., & Martínez-Vilalta, J. (2018). Below-ground hydraulic constraints during drought-induced decline in Scots pine. Annals of Forest Science, 75(4). https://doi.org/10.1007/s13595-018-0778-7
R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.r-project.org/
Rossatto, D. R., de Carvalho Ramos Silva, L., Villalobos-Vega, R., Sternberg, L. D. S. L., & Franco, A. C. (2012). Depth of water uptake in woody plants relates to groundwater level and vegetation structure along a topographic gradient in a neotropical savanna. Environmental and Experimental Botany, 77, 259-266. https://doi.org/10.1016/j.envexpbot.2011.11.025
RStudio Team. (2020). RStudio: Integrated development for R. RStudio, PBC. http://www.rstudio.com/
Snyder, K. A., & Williams, D. G. (2003). Defoliation alters water uptake by deep and shallow roots of Prosopis velutina (Velvet Mesquite). Functional Ecology, 17(3), 363-374. https://doi.org/10.1046/j.1365-2435.2003.00739.x
Sperry, J. S., & Love, D. M. (2015). What plant hydraulics can tell us about responses to climate-change droughts. New Phytologist, 207, 14-27. https://doi.org/10.1111/nph.13354
Sperry, J. S., Venturas, M. D., Anderegg, W. R. L., Mencuccini, M., Mackay, D. S., Wang, Y., & Love, D. M. (2017). Predicting stomatal responses to the environment from the optimization of photosynthetic gain and hydraulic cost. Plant Cell and Environment, 40(6), 816-830. https://doi.org/10.1111/pce.12852
Sperry, J. S., Wang, Y., Wolfe, B. T., Mackay, D. S., Anderegg, W. R. L., Mcdowell, N. G., & Pockman, W. T. (2016). Pragmatic hydraulic theory predicts stomatal responses to climatic water deficits. New Phytologist, 212(3), 577-589. https://doi.org/10.1111/nph.14059
Stahl, C., Hérault, B., Rossi, V., Burban, B., Bréchet, C., & Bonal, D. (2013). Depth of soil water uptake by tropical rainforest trees during dry periods: Does tree dimension matter? Oecologia, 173(4), 1191-1201. https://doi.org/10.1007/s00442-013-2724-6
TERN. (2020). TERN daintree rainforest SuperSite. https://www.TERN.org.au/tern-observatory/tern-ecosystem-processes/daintree-rainforest-supersite/
Tng, D. Y. P., Apgaua, D. M. G., Campbell, M. J., Cox, C. J., Crayn, D. M., Ishida, F. Y., Laidlaw, M. J., Liddell, M. J., Seager, M., & Laurance, S. G. W. (2016). Vegetation and floristics of a lowland tropical rainforest in northeast Australia. Biodiversity Data Journal, 4(1), 1-20. https://doi.org/10.3897/BDJ.4.e7599
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, 8(24), 12479-12491. https://doi.org/10.1002/ece3.4601
Trenberth, K. E., Dai, A., Van Der Schrier, G., Jones, P. D., Barichivich, J., Briffa, K. R., & Sheffield, J. (2014). Global warming and changes in drought. Nature Climate Change, 4(1), 17-22. https://doi.org/10.1038/nclimate2067
van Genuchten, M. T. (1980). A closed-form equation for predicting the hydraulic conductivity of unsaturated soils. Soil Science Society of America Journal, 44(5), 892-898. https://doi.org/10.2136/sssaj1980.03615995004400050002x
Vargas, G. (2019). Pressure volume curves. https://github.com/gevargu/Plant_Ecophysiology_Tools/tree/master/PressureVolumeCurves
Venturas, M. D., Sperry, J. S., Love, D. M., Frehner, E. H., Allred, M. G., Wang, Y., & Anderegg, W. R. L. (2018). A stomatal control model based on optimization of carbon gain versus hydraulic risk predicts aspen sapling responses to drought. New Phytologist, 220(3), 836-850. https://doi.org/10.1111/nph.15333
Vogado, N. O., Liddell, M. J., Laurance, S. G. W., Campbell, M. J., Cheesman, A. W., Engert, J. E., Palma, A. C., Ishida, F. Y., & Cernusak, L. A. (2020). The effects of an experimental drought on the ecophysiology and fruiting phenology of a tropical rainforest palm. Journal of Plant Ecology, 13(6), 744-753. https://doi.org/10.1093/jpe/rtaa069
Voltas, J., Lucabaugh, D., Chambel, M. R., & Ferrio, J. P. (2015). Intraspecific variation in the use of water sources by the circum-Mediterranean conifer Pinus halepensis. New Phytologist, 208(4), 1031-1041. https://doi.org/10.1111/nph.13569
Zhou, L., Tian, Y., Myneni, R. B., Ciais, P., Saatchi, S., Liu, Y. Y., Piao, S., Chen, H., Vermote, E. F., Song, C., & Hwang, T. (2014). Widespread decline of Congo rainforest greenness in the past decade. Nature, 508(7498), 86-90. https://doi.org/10.1038/nature13265
Ziegler, C., Coste, S., Stahl, C., Delzon, S., Levionnois, S., Cazal, J., Cochard, H., Esquivel-Muelbert, A., Goret, J. Y., Heuret, P., Jaouen, G., Santiago, L. S., & Bonal, D. (2019). Large hydraulic safety margins protect Neotropical canopy rainforest tree species against hydraulic failure during drought. Annals of Forest Science, 76(4). https://doi.org/10.1007/s13595-019-0905-0