Homeostatic maintenance of non-structural carbohydrates during the 2015-2016 El Niño drought across a tropical forest precipitation gradient

Dickman, L. Turin; McDowell, Nate G.; Grossiord, Charlotte; Collins, Adam D.; Wolfe, Brett T.; Detto, Matteo; Wright, S. Joseph; Medina-Vega, José A.; Goodsman, Devin; Rogers, Alistair; Serbin, Shawn P.; Wu, Jin; Ely, Kim S.; Michaletz, Sean T.; Xu, Chonggang; Kueppers, Lara; Chambers, Jeffrey Q.

doi:10.1111/pce.13501

Homeostatic maintenance of non-structural carbohydrates during the 2015-2016 El Niño drought across a tropical forest precipitation gradient

Journal Article · Tue Dec 11 00:00:00 EST 2018 · Plant, Cell and Environment

DOI:https://doi.org/10.1111/pce.13501· OSTI ID:1484869

Dickman, L. Turin ^[1]; McDowell, Nate G. ^[2]; Grossiord, Charlotte ^[3]; Collins, Adam D. ^[1]; Wolfe, Brett T. ^[4]; Detto, Matteo ^[5]; Wright, S. Joseph ^[4]; Medina-Vega, José A. ^[6]; Goodsman, Devin ^[1]; ^[7]; Serbin, Shawn P. ^[7]; Wu, Jin ^[7]; Ely, Kim S. ^[7]; Michaletz, Sean T. ^[8]; Xu, Chonggang ^[1]; Kueppers, Lara ^[9]; Chambers, Jeffrey Q. ^[9]

Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Atmospheric Science and Global Change Div. (ASGC)
Swiss Federal Research Inst. WSL, Birmensdorf (Switzerland)
Smithsonian Tropical Research Inst., Balboa (Panama)
Princeton Univ., NJ (United States). Dept. of Ecology and Evolutionary Biology
Smithsonian Tropical Research Inst., Balboa (Panama); Wageningen Univ. and Research, Wageningen (The Netherlands). Forest Ecology and Forest Management Group
Brookhaven National Lab. (BNL), Upton, NY (United States). Environmental & Climate Sciences Dept.
Univ. of British Columbia, Vancouver, BC (Canada). Dept. of Botany and Biodiversity Research Centre
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Earth and Environmental Sciences Area

Non-structural carbohydrates (NSCs) are essential for maintenance of plant metabolism, and may be sensitive to both short- and long-term climatic variation. NSC variation in moist tropical forests has rarely been studied, so regulation of NSCs in these systems is poorly understood. We measured foliar and branch NSC content in 23 tree species at three sites located across a large precipitation gradient in Panama during the 2015-2016 El Niño to examine how short- and long-term climatic variation impact carbohydrate dynamics. Across all sites, leaf NSCs increased over diurnal time-periods. There was no significant difference in total NSCs as the drought progressed (leaf p=0.32, branch p=0.30), nor across the rainfall gradient (leaf p=0.91, branch p=0.96). Foliar soluble sugars decreased while starch increased over the duration of the dry period, suggesting greater partitioning of NSCs to storage than metabolism or transport as drought progressed. There was large variation across species at all sites, but total foliar NSCs were positively correlated with leaf mass per area, while branch sugars were positively related to leaf temperature and negatively correlated with daily photosynthesis and wood density. The NSC homeostasis across a wide range of conditions suggests that NSCs are an allocation priority in moist tropical forests.

View Accepted Manuscript (DOE)

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Los Alamos National Laboratory (LANL), Los Alamos, NM (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: 89233218CNA000001; AC02-05CH11231; SC0012704

OSTI ID:: 1484869

Alternate ID(s):: OSTI ID: 1530825
OSTI ID: 1561916
OSTI ID: 1489970

Report Number(s):: BNL--209646-2018-JAAM; LA-UR--18-31290

Journal Information:: Plant, Cell and Environment, Journal Name: Plant, Cell and Environment Journal Issue: 5 Vol. 42; ISSN 0140-7791

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (63)

Simultaneous Inference in General Parametric Models Hothorn, Torsten; Bretz, Frank; Westfall, Peter Biometrical Journal, Vol. 50, Issue 3 https://doi.org/10.1002/bimj.200810425	journal	June 2008
Dynamics of non-structural carbohydrates in terrestrial plants: a global synthesis Martínez-Vilalta, Jordi; Sala, Anna; Asensio, Dolores Ecological Monographs, Vol. 86, Issue 4 https://doi.org/10.1002/ecm.1231	journal	November 2016
Application of a Single-solute Non-steady-state Phloem Model to the Study of Long-distance Assimilate Transport Thompson, Matthew V.; Holbrook, N. Michele Journal of Theoretical Biology, Vol. 220, Issue 4 https://doi.org/10.1006/jtbi.2003.3115	journal	February 2003
Mixed effects models and extensions in ecology with R Zuur, Alain F.; Ieno, Elena N.; Walker, Neil Statistics for Biology and Health https://doi.org/10.1007/978-0-387-87458-6	book	January 2009
Leaf carbohydrate responses to CO2 enrichment at the top of a tropical forest Würth, Mirjam K. R.; Winter, Klaus; Körner, Christian Oecologia, Vol. 116, Issue 1-2 https://doi.org/10.1007/PL00013821	journal	August 1998
Seasonal patterns of carbohydrate storage in four tropical tree species Newell, Elizabeth A.; Mulkey, Stephen S.; Wright, Joseph S. Oecologia, Vol. 131, Issue 3 https://doi.org/10.1007/s00442-002-0888-6	journal	May 2002
Non-structural carbohydrate pools in a tropical forest Würth, Mirjam K. R.; Peláez-Riedl, Susanna; Wright, S. Joseph. Oecologia, Vol. 143, Issue 1 https://doi.org/10.1007/s00442-004-1773-2	journal	December 2004
Trends in wood density and structure are linked to prevention of xylem implosion by negative pressure Hacke, Uwe G.; Sperry, John S.; Pockman, William T. Oecologia, Vol. 126, Issue 4 https://doi.org/10.1007/s004420100628	journal	February 2001
Variation in wood density and anatomy in a widespread mangrove species Santini, Nadia S.; Schmitz, Nele; Lovelock, Catherine E. Trees, Vol. 26, Issue 5 https://doi.org/10.1007/s00468-012-0729-0	journal	April 2012
Reserve carbohydrate levels in the boles and structural roots of five multipurpose tree species in a seasonally dry tropical climate Latt, C. R.; Nair, P. K. R.; Kang, B. T. Forest Ecology and Management, Vol. 146, Issue 1-3 https://doi.org/10.1016/S0378-1127(00)00456-4	journal	June 2001
A model for leaf temperature decoupling from air temperature Blonder, Benjamin; Michaletz, Sean T. Agricultural and Forest Meteorology, Vol. 262 https://doi.org/10.1016/j.agrformet.2018.07.012	journal	November 2018
Plant Thermoregulation: Energetics, Trait–Environment Interactions, and Carbon Economics Michaletz, Sean T.; Weiser, Michael D.; Zhou, Jizhong Trends in Ecology & Evolution, Vol. 30, Issue 12 https://doi.org/10.1016/j.tree.2015.09.006	journal	December 2015
Changes in tree species abundance in a Neotropical forest: impact of climate change Condit, Richard; Hubbell, Stephen P.; Foster, Robin B. Journal of Tropical Ecology, Vol. 12, Issue 2 https://doi.org/10.1017/S0266467400009433	journal	March 1996
Altitudinal increase of mobile carbon pools in Pinus cembra suggests sink limitation of growth at the Swiss treeline Hoch, Gunter; Popp, Marianne; Korner, Christian Oikos, Vol. 98, Issue 3 https://doi.org/10.1034/j.1600-0706.2002.980301.x	journal	September 2002
Effect of interannual climate variability on carbon storage in Amazonian ecosystems Tian, Hanqin; Melillo, Jerry M.; Kicklighter, David W. Nature, Vol. 396, Issue 6712 https://doi.org/10.1038/25328	journal	December 1998
The Amazon basin in transition Davidson, Eric A.; de Araújo, Alessandro C.; Artaxo, Paulo Nature, Vol. 481, Issue 7381 https://doi.org/10.1038/nature10717	journal	January 2012
Global convergence in the vulnerability of forests to drought Choat, Brendan; Jansen, Steven; Brodribb, Tim J. Nature, Vol. 491, Issue 7426 https://doi.org/10.1038/nature11688	journal	November 2012
Death from drought in tropical forests is triggered by hydraulics not carbon starvation Rowland, L.; da Costa, A. C. L.; Galbraith, D. R. Nature, Vol. 528, Issue 7580 https://doi.org/10.1038/nature15539	journal	November 2015
Increasing frequency of extreme El Niño events due to greenhouse warming Cai, Wenju; Borlace, Simon; Lengaigne, Matthieu Nature Climate Change, Vol. 4, Issue 2 https://doi.org/10.1038/nclimate2100	journal	January 2014
Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels O’Brien, Michael J.; Leuzinger, Sebastian; Philipson, Christopher D. Nature Climate Change, Vol. 4, Issue 8 https://doi.org/10.1038/nclimate2281	journal	June 2014
The energetic and carbon economic origins of leaf thermoregulation Michaletz, Sean T.; Weiser, Michael D.; McDowell, Nate G. Nature Plants, Vol. 2, Issue 9 https://doi.org/10.1038/nplants.2016.129	journal	August 2016
A multi-species synthesis of physiological mechanisms in drought-induced tree mortality Adams, Henry D.; Zeppel, Melanie J. B.; Anderegg, William R. L. Nature Ecology & Evolution, Vol. 1, Issue 9 https://doi.org/10.1038/s41559-017-0248-x	journal	August 2017
Non-structural carbon compounds in temperate forest trees Hoch, G.; Richter, A.; Korner, Ch. Plant, Cell and Environment, Vol. 26, Issue 7 https://doi.org/10.1046/j.0016-8025.2003.01032.x	journal	July 2003
Carbon limitation in trees Korner, Christian Journal of Ecology, Vol. 91, Issue 1 https://doi.org/10.1046/j.1365-2745.2003.00742.x	journal	February 2003
Positive Feedbacks among Forest Fragmentation, Drought, and Climate Change in the Amazon Laurance, William F.; Williamson, G. Bruce Conservation Biology, Vol. 15, Issue 6 https://doi.org/10.1046/j.1523-1739.2001.01093.x	journal	December 2001
Persistent effects of a severe drought on Amazonian forest canopy Saatchi, S.; Asefi-Najafabady, S.; Malhi, Y. Proceedings of the National Academy of Sciences, Vol. 110, Issue 2 https://doi.org/10.1073/pnas.1204651110	journal	December 2012
A fully traits-based approach to modeling global vegetation distribution van Bodegom, P. M.; Douma, J. C.; Verheijen, L. M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 38 https://doi.org/10.1073/pnas.1304551110	journal	September 2014
Interannual variations in vegetation activities and climate variability caused by ENSO in tropical rainforests Nagai, S.; Ichii, K.; Morimoto, H. International Journal of Remote Sensing, Vol. 28, Issue 6 https://doi.org/10.1080/01431160600904972	journal	March 2007
Higher absorbed solar radiation partly offset the negative effects of water stress on the photosynthesis of Amazon forests during the 2015 drought Li, Xing; Xiao, Jingfeng; He, Binbin Environmental Research Letters, Vol. 13, Issue 4 https://doi.org/10.1088/1748-9326/aab0b1	journal	March 2018
Sink regulation of photosynthesis Paul, Matthew J.; Foyer, Christine H. Journal of Experimental Botany, Vol. 52, Issue 360 https://doi.org/10.1093/jexbot/52.360.1383	journal	July 2001
Supply and demand: sink regulation of sugar accumulation in sugarcane McCormick, A. J.; Watt, D. A.; Cramer, M. D. Journal of Experimental Botany, Vol. 60, Issue 2 https://doi.org/10.1093/jxb/ern310	journal	January 2009
Atmospheric CO2 and the ratio of intercellular to ambient CO2 concentrations in plants Ehleringer, J. R.; Cerling, T. E. Tree Physiology, Vol. 15, Issue 2 https://doi.org/10.1093/treephys/15.2.105	journal	February 1995
Allocation to carbon storage pools in Norway spruce saplings under drought and low CO2 Hartmann, H.; McDowell, N. G.; Trumbore, S. Tree Physiology, Vol. 35, Issue 3 https://doi.org/10.1093/treephys/tpv019	journal	March 2015
Non-structural carbohydrates in woody plants compared among laboratories Quentin, Audrey G.; Pinkard, Elizabeth A.; Ryan, Michael G. Tree Physiology https://doi.org/10.1093/treephys/tpv073	journal	September 2015
Standardized protocols and procedures can precisely and accurately quantify non-structural carbohydrates Landhäusser, Simon M.; Chow, Pak S.; Dickman, L. Turin Tree Physiology, Vol. 38, Issue 12 https://doi.org/10.1093/treephys/tpy118	journal	October 2018
Do Xylem Fibers Affect Vessel Cavitation Resistance? Jacobsen, Anna L.; Ewers, Frank W.; Pratt, R. Brandon Plant Physiology, Vol. 139, Issue 1 https://doi.org/10.1104/pp.104.058404	journal	August 2005
Mechanisms Linking Drought, Hydraulics, Carbon Metabolism, and Vegetation Mortality McDowell, Nathan G. Plant Physiology, Vol. 155, Issue 3 https://doi.org/10.1104/pp.110.170704	journal	January 2011
The Effect of Leaf Temperature and Photorespiratory Conditions on Export of Sugars during Steady-State Photosynthesis in Salvia splendens Jiao, J.; Grodzinski, B. Plant Physiology, Vol. 111, Issue 1 https://doi.org/10.1104/pp.111.1.169	journal	May 1996
Transcriptome Response to Embolism Formation in Stems of Populus trichocarpa Provides Insight into Signaling and the Biology of Refilling Secchi, Francesca; Gilbert, Matthew E.; Zwieniecki, Maciej A. Plant Physiology, Vol. 157, Issue 3 https://doi.org/10.1104/pp.111.185124	journal	September 2011
Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest Myers, Jonathan A.; Kitajima, Kaoru Journal of Ecology, Vol. 95, Issue 2 https://doi.org/10.1111/j.1365-2745.2006.01207.x	journal	March 2007
Leaf photosynthesis and carbohydrate dynamics of soybeans grown throughout their life-cycle under Free-Air Carbon dioxide Enrichment Rogers, A.; Allen, D. J.; Davey, P. A. Plant, Cell and Environment, Vol. 27, Issue 4 https://doi.org/10.1111/j.1365-3040.2004.01163.x	journal	April 2004
Causes and consequences of variation in leaf mass per area (LMA): a meta‐analysis Poorter, Hendrik; Niinemets, Ülo; Poorter, Lourens New Phytologist, Vol. 182, Issue 3 https://doi.org/10.1111/j.1469-8137.2009.02830.x	journal	April 2009
Assessing uncertainties in a second-generation dynamic vegetation model caused by ecological scale limitations Fisher, Rosie; McDowell, Nate; Purves, Drew New Phytologist, Vol. 187, Issue 3 https://doi.org/10.1111/j.1469-8137.2010.03340.x	journal	July 2010
Evaluating theories of drought-induced vegetation mortality using a multimodel-experiment framework McDowell, Nate G.; Fisher, Rosie A.; Xu, Chonggang New Phytologist, Vol. 200, Issue 2 https://doi.org/10.1111/nph.12465	journal	September 2013
A new look at water transport regulation in plants Martínez-Vilalta, Jordi; Poyatos, Rafael; Aguadé, David New Phytologist, Vol. 204, Issue 1 https://doi.org/10.1111/nph.12912	journal	July 2014
Does leaf shedding protect stems from cavitation during seasonal droughts? A test of the hydraulic fuse hypothesis Wolfe, Brett T.; Sperry, John S.; Kursar, Thomas A. New Phytologist, Vol. 212, Issue 4 https://doi.org/10.1111/nph.14087	journal	July 2016
Tropical rainforest carbon sink declines during El Niño as a result of reduced photosynthesis and increased respiration rates Cavaleri, Molly A.; Coble, Adam P.; Ryan, Michael G. New Phytologist, Vol. 216, Issue 1 https://doi.org/10.1111/nph.14724	journal	August 2017
Terrestrial biosphere models underestimate photosynthetic capacity and CO ₂ assimilation in the Arctic Rogers, Alistair; Serbin, Shawn P.; Ely, Kim S. New Phytologist, Vol. 216, Issue 4 https://doi.org/10.1111/nph.14740	journal	September 2017
Sugars from woody tissue photosynthesis reduce xylem vulnerability to cavitation De Baerdemaeker, Niels J. F.; Salomón, Roberto Luis; De Roo, Linus New Phytologist, Vol. 216, Issue 3 https://doi.org/10.1111/nph.14787	journal	September 2017
Drivers and mechanisms of tree mortality in moist tropical forests McDowell, Nate; Allen, Craig D.; Anderson-Teixeira, Kristina New Phytologist, Vol. 219, Issue 3 https://doi.org/10.1111/nph.15027	journal	February 2018
Homeostatic levels of nonstructural carbohydrates after 13 yr of drought and irrigation in Pinus sylvestris Schönbeck, Leonie; Gessler, Arthur; Hoch, Günter New Phytologist, Vol. 219, Issue 4 https://doi.org/10.1111/nph.15224	journal	May 2018
Carbohydrate dynamics and mortality in a piñon-juniper woodland under three future precipitation scenarios: Carbohydrate dynamics in piñon-juniper woodland Dickman, Lee T.; Mcdowell, Nate G.; Sevanto, Sanna Plant, Cell & Environment, Vol. 38, Issue 4 https://doi.org/10.1111/pce.12441	journal	October 2014
The functional role of xylem parenchyma cells and aquaporins during recovery from severe water stress: Response of xylem parenchyma cells to embolism Secchi, Francesca; Pagliarani, Chiara; Zwieniecki, Maciej A. Plant, Cell & Environment, Vol. 40, Issue 6 https://doi.org/10.1111/pce.12831	journal	October 2016
Terrestrial Gross Carbon Dioxide Uptake: Global Distribution and Covariation with Climate Beer, C.; Reichstein, M.; Tomelleri, E. Science, Vol. 329, Issue 5993 https://doi.org/10.1126/science.1184984	journal	July 2010
Nonstructural Carbon in Woody Plants Dietze, Michael C.; Sala, Anna; Carbone, Mariah S. Annual Review of Plant Biology, Vol. 65, Issue 1 https://doi.org/10.1146/annurev-arplant-050213-040054	journal	April 2014
The Structure, Distribution, and Biomass of the World's Forests Pan, Yude; Birdsey, Richard A.; Phillips, Oliver L. Annual Review of Ecology, Evolution, and Systematics, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-ecolsys-110512-135914	journal	November 2013
The Ecology and Economics of Storage in Plants Chapin, F. S.; Schulze, E.; Mooney, H. A. Annual Review of Ecology and Systematics, Vol. 21, Issue 1 https://doi.org/10.1146/annurev.es.21.110190.002231	journal	November 1990
Carbohydrate Storage and Light Requirements of Tropical Moist and dry Forest tree Species Poorter, Lourens; Kitajima, Kaoru Ecology, Vol. 88, Issue 4 https://doi.org/10.1890/06-0984	journal	April 2007
Resprouting as a persistence strategy of tropical forest trees: relations with carbohydrate storage and shade tolerance Poorter, Lourens; Kitajima, Kaoru; Mercado, Pablo Ecology, Vol. 91, Issue 9 https://doi.org/10.1890/09-0862.1	journal	September 2010
Homeostatic Maintenance Of Ponderosa Pine Gas Exchange In Response To Stand Density Changes McDowell, Nate G.; Adams, Henry D.; Bailey, John D. Ecological Applications, Vol. 16, Issue 3 https://doi.org/10.1890/1051-0761(2006)016[1164:HMOPPG]2.0.CO;2	journal	June 2006
Amyloglucosidase Hydrolysis Can Overestimate Starch Concentration of Plants Denison, R. F.; Fedders, J. M.; Tong, C. B. S. Agronomy Journal, Vol. 82, Issue 2 https://doi.org/10.2134/agronj1990.00021962008200020039x	journal	January 1990
Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels O'Brien, Michael J.; Leuzinger, Sebastian; Philipson, Christopher D. Nature Publishing Group https://doi.org/10.5167/uzh-98172	text	January 2014
Simultaneous Inference in General Parametric Models Hothorn, Torsten; Bretz, Frank; Westfall, Peter Universitätsbibliothek der Ludwig-Maximilians-Universität München https://doi.org/10.5282/ubm/epub.2120	text	January 2008

Cited By (5)

Spectroscopy can predict key leaf traits associated with source–sink balance and carbon–nitrogen status Ely, Kim S.; Burnett, Angela C.; Lieberman-Cribbin, Wil Journal of Experimental Botany, Vol. 70, Issue 6 https://doi.org/10.1093/jxb/erz061	journal	February 2019
Drought and the interannual variability of stem growth in an aseasonal, everwet forest Hogan, J. Aaron; McMahon, Sean M.; Buzzard, Vanessa Biotropica, Vol. 51, Issue 2 https://doi.org/10.1111/btp.12624	journal	February 2019
The response of stomatal conductance to seasonal drought in tropical forests Wu, Jin; Serbin, Shawn P.; Ely, Kim S. Global Change Biology, Vol. 26, Issue 2 https://doi.org/10.1111/gcb.14820	journal	October 2019
Testing for changes in biomass dynamics in large‐scale forest datasets Rutishauser, Ervan; Wright, Stuart J.; Condit, Richard Global Change Biology, Vol. 26, Issue 3 https://doi.org/10.1111/gcb.14833	journal	October 2019
Wood allocation trade‐offs between fiber wall, fiber lumen, and axial parenchyma drive drought resistance in neotropical trees Janssen, Thomas A. J.; Hölttä, Teemu; Fleischer, Katrin Plant, Cell & Environment, Vol. 43, Issue 4 https://doi.org/10.1111/pce.13687	journal	February 2020

Similar Records

Homeostatic maintenance of nonstructural carbohydrates during the 2015-2016 El Niño drought across a tropical forest precipitation gradient

Journal Article · Wed May 01 00:00:00 EDT 2019 · Plant, Cell & Environment · OSTI ID:1530825

Related Subjects

54 ENVIRONMENTAL SCIENCES
Biological Science
ENSO
Earth Sciences
NSC
Panama
climate
storage
sugars
tropics
vegetation

Homeostatic maintenance of non-structural carbohydrates during the 2015-2016 El Niño drought across a tropical forest precipitation gradient

Citation Formats

References (63)

Cited By (5)

Similar Records

Related Subjects