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FOREST ECOLOGY

Ecosystem fluxes during drought and recovery in an experimental forest

Christiane Werner https://orcid.org/0000-0002-7676-9057 [email protected], Laura K. Meredith https://orcid.org/0000-0003-4244-4366, S. Nemiah Ladd https://orcid.org/0000-0002-0132-5785, Johannes Ingrisch https://orcid.org/0000-0002-8461-8689, Angelika Kübert https://orcid.org/0000-0003-3985-9261, Joost van Haren https://orcid.org/0000-0001-7879-5972, Michael Bahn https://orcid.org/0000-0001-7482-9776, Kinzie Bailey https://orcid.org/0000-0001-8210-8370, Ines Bamberger, Matthias Beyer https://orcid.org/0000-0002-1618-6036, Daniel Blomdahl https://orcid.org/0000-0002-2004-0937, Joseph Byron https://orcid.org/0000-0001-9452-0186, Erik Daber https://orcid.org/0000-0001-7910-1995, Jason Deleeuw, Michaela A. Dippold https://orcid.org/0000-0002-3657-4693, Jane Fudyma https://orcid.org/0000-0001-8834-9044, Juliana Gil-Loaiza https://orcid.org/0000-0002-2610-3812, Linnea K. Honeker https://orcid.org/0000-0002-1299-0879, Jia Hu https://orcid.org/0000-0001-6858-6659, Jianbei Huang https://orcid.org/0000-0001-5286-5645, Thomas Klüpfel, Jordan Krechmer https://orcid.org/0000-0003-3642-0659, Jürgen Kreuzwieser https://orcid.org/0000-0002-5251-9723, Kathrin Kühnhammer https://orcid.org/0000-0001-5266-2207, Marco M. Lehmann https://orcid.org/0000-0003-2962-3351, Kathiravan Meeran https://orcid.org/0000-0002-3987-5002, Pawel K. Misztal https://orcid.org/0000-0003-1060-1750, Wei-Ren Ng, Eva Pfannerstill https://orcid.org/0000-0001-7715-1200, Giovanni Pugliese https://orcid.org/0000-0002-2869-3588, Gemma Purser https://orcid.org/0000-0001-7062-6840, Joseph Roscioli https://orcid.org/0000-0002-7166-3579, Lingling Shi https://orcid.org/0000-0001-8213-689X, Malak Tfaily https://orcid.org/0000-0002-3036-2833, and Jonathan Williams https://orcid.org/0000-0001-9421-1703
Science16 Dec 2021Vol 374, Issue 6574pp. 1514-1518DOI: 10.1126/science.abj6789

An experimental forest ecosystem drought

Drought is affecting many of the world’ s forested ecosystems, but it has proved challenging to develop an ecosystem-level mechanistic understanding of the ways that drought affects carbon and water fluxes through forest ecosystems. Werner et al. used an experimental approach by imposing an artificial drought on an entire enclosed ecosystem: the Biosphere 2 Tropical Rainforest in Arizona (see the Perspective by Eisenhauer and Weigelt). The authors show that ecosystem-scale plant responses to drought depend on distinct plant functional groups, differing in their water-use strategies and their position in the forest canopy. The balance of these plant functional groups drives changes in carbon and water fluxes, as well as the release of volatile organic compounds into the atmosphere. —AMS

Abstract

Severe droughts endanger ecosystem functioning worldwide. We investigated how drought affects carbon and water fluxes as well as soil-plant-atmosphere interactions by tracing 13CO2 and deep water 2H2O label pulses and volatile organic compounds (VOCs) in an enclosed experimental rainforest. Ecosystem dynamics were driven by different plant functional group responses to drought. Drought-sensitive canopy trees dominated total fluxes but also exhibited the strongest response to topsoil drying. Although all canopy-forming trees had access to deep water, these reserves were spared until late in the drought. Belowground carbon transport was slowed, yet allocation of fresh carbon to VOCs remained high. Atmospheric VOC composition reflected increasing stress responses and dynamic soil-plant-atmosphere interactions, potentially affecting atmospheric chemistry and climate feedbacks. These interactions and distinct functional group strategies thus modulate drought impacts and ecosystem susceptibility to climate change.
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References (3761)

References and notes

1
G. B. Bonan, Forests and climate change: Forcings, feedbacks, and the climate benefits of forests. Science 320, 1444–1449 (2008).
2
M. Reichstein, M. Bahn, P. Ciais, D. Frank, M. D. Mahecha, S. I. Seneviratne, J. Zscheischler, C. Beer, N. Buchmann, D. C. Frank, D. Papale, A. Rammig, P. Smith, K. Thonicke, M. van der Velde, S. Vicca, A. Walz, M. Wattenbach, Climate extremes and the carbon cycle. Nature 500, 287–295 (2013).
3
A. Bastos, P. Ciais, P. Friedlingstein, S. Sitch, J. Pongratz, L. Fan, J. P. Wigneron, U. Weber, M. Reichstein, Z. Fu, P. Anthoni, A. Arneth, V. Haverd, A. K. Jain, E. Joetzjer, J. Knauer, S. Lienert, T. Loughran, P. C. McGuire, H. Tian, N. Viovy, S. Zaehle, Direct and seasonal legacy effects of the 2018 heat wave and drought on European ecosystem productivity. Sci. Adv. 6, eaba2724 (2020).
4
Y. Pan, R. A. Birdsey, J. Fang, R. Houghton, P. E. Kauppi, W. A. Kurz, O. L. Phillips, A. Shvidenko, S. L. Lewis, J. G. Canadell, P. Ciais, R. B. Jackson, S. W. Pacala, A. D. McGuire, S. Piao, A. Rautiainen, S. Sitch, D. Hayes, A large and persistent carbon sink in the world’s forests. Science 333, 988–993 (2011).
5
J.-P. Wigneron, L. Fan, P. Ciais, A. Bastos, M. Brandt, J. Chave, S. Saatchi, A. Baccini, R. Fensholt, xTropical forests did not recover from the strong 2015-2016 El Niño event. Sci. Adv. 6, eaay4603 (2020).
6
W. Hubau, S. L. Lewis, O. L. Phillips, K. Affum-Baffoe, H. Beeckman, A. Cuní-Sanchez, A. K. Daniels, C. E. N. Ewango, S. Fauset, J. M. Mukinzi, D. Sheil, B. Sonké, M. J. P. Sullivan, T. C. H. Sunderland, H. Taedoumg, S. C. Thomas, L. J. T. White, K. A. Abernethy, S. Adu-Bredu, C. A. Amani, T. R. Baker, L. F. Banin, F. Baya, S. K. Begne, A. C. Bennett, F. Benedet, R. Bitariho, Y. E. Bocko, P. Boeckx, P. Boundja, R. J. W. Brienen, T. Brncic, E. Chezeaux, G. B. Chuyong, C. J. Clark, M. Collins, J. A. Comiskey, D. A. Coomes, G. C. Dargie, T. de Haulleville, M. N. D. Kamdem, J.-L. Doucet, A. Esquivel-Muelbert, T. R. Feldpausch, A. Fofanah, E. G. Foli, M. Gilpin, E. Gloor, C. Gonmadje, S. Gourlet-Fleury, J. S. Hall, A. C. Hamilton, D. J. Harris, T. B. Hart, M. B. N. Hockemba, A. Hladik, S. A. Ifo, K. J. Jeffery, T. Jucker, E. K. Yakusu, E. Kearsley, D. Kenfack, A. Koch, M. E. Leal, A. Levesley, J. A. Lindsell, J. Lisingo, G. Lopez-Gonzalez, J. C. Lovett, J.-R. Makana, Y. Malhi, A. R. Marshall, J. Martin, E. H. Martin, F. M. Mbayu, V. P. Medjibe, V. Mihindou, E. T. A. Mitchard, S. Moore, P. K. T. Munishi, N. N. Bengone, L. Ojo, F. E. Ondo, K. S.-H. Peh, G. C. Pickavance, A. D. Poulsen, J. R. Poulsen, L. Qie, J. Reitsma, F. Rovero, M. D. Swaine, J. Talbot, J. Taplin, D. M. Taylor, D. W. Thomas, B. Toirambe, J. T. Mukendi, D. Tuagben, P. M. Umunay, G. M. F. van der Heijden, H. Verbeeck, J. Vleminckx, S. Willcock, H. Wöll, J. T. Woods, L. Zemagho, Asynchronous carbon sink saturation in African and Amazonian tropical forests. Nature 579, 80–87 (2020).
7
A. B. Guenther, X. Jiang, C. L. Heald, T. Sakulyanontvittaya, T. Duhl, L. K. Emmons, X. Wang, The Model of Emissions of Gases and Aerosols from Nature version 2.1 (MEGAN2.1): An extended and updated framework for modeling biogenic emissions. Geosci. Model Dev. 5, 1471–1492 (2012).
8
F. Loreto, J.-P. Schnitzler, Abiotic stresses and induced BVOCs. Trends Plant Sci. 15, 154–166 (2010).
9
A. Arneth, S. P. Harrison, S. Zaehle, K. Tsigaridis, S. Menon, P. J. Bartlein, J. Feichter, A. Korhola, M. Kulmala, D. O’Donnell, G. Schurgers, S. Sorvari, T. Vesala, Terrestrial biogeochemical feedbacks in the climate system. Nat. Geosci. 3, 525–532 (2010).
10
N. Unger, On the role of plant volatiles in anthropogenic global climate change. Geophys. Res. Lett. 41, 8563–8569 (2014).
11
H. Chu, D. D. Baldocchi, R. John, S. Wolf, M. Reichstein, Fluxes all of the time? A primer on the temporal representativeness of FLUXNET. J. Geophys. Res. Biogeosci. 122, 289–307 (2017).
12
W. R. L. Anderegg, A. G. Konings, A. T. Trugman, K. Yu, D. R. Bowling, R. Gabbitas, D. S. Karp, S. Pacala, J. S. Sperry, B. N. Sulman, N. Zenes, Hydraulic diversity of forests regulates ecosystem resilience during drought. Nature 561, 538–541 (2018).
13
T. J. Brodribb, J. Powers, H. Cochard, B. Choat, Hanging by a thread? Forests and drought. Science 368, 261–266 (2020).
14
H. Hartmann, M. Bahn, M. Carbone, A. D. Richardson, Plant carbon allocation in a changing world - challenges and progress: introduction to a Virtual Issue on carbon allocation: Introduction to a virtual issue on carbon allocation. New Phytol. 227, 981–988 (2020).
15
J. K. Holopainen, J. Gershenzon, Multiple stress factors and the emission of plant VOCs. Trends Plant Sci. 15, 176–184 (2010).
16
N. M. Levine, K. Zhang, M. Longo, A. Baccini, O. L. Phillips, S. L. Lewis, E. Alvarez-Dávila, A. C. Segalin de Andrade, R. J. W. Brienen, T. L. Erwin, T. R. Feldpausch, A. L. Monteagudo Mendoza, P. Nuñez Vargas, A. Prieto, J. E. Silva-Espejo, Y. Malhi, P. R. Moorcroft, Ecosystem heterogeneity determines the ecological resilience of the Amazon to climate change. Proc. Natl. Acad. Sci. U.S.A. 113, 793–797 (2016).
17
J. Joseph, D. Gao, B. Backes, C. Bloch, I. Brunner, G. Gleixner, M. Haeni, H. Hartmann, G. Hoch, C. Hug, A. Kahmen, M. M. Lehmann, M.-H. Li, J. Luster, M. Peter, C. Poll, A. Rigling, K. A. Rissanen, N. K. Ruehr, M. Saurer, M. Schaub, L. Schönbeck, B. Stern, F. M. Thomas, R. A. Werner, W. Werner, T. Wohlgemuth, F. Hagedorn, A. Gessler, Rhizosphere activity in an old-growth forest reacts rapidly to changes in soil moisture and shapes whole-tree carbon allocation. Proc. Natl. Acad. Sci. U.S.A. 117, 24885–24892 (2020).
18
F. I. Pugnaire, J. A. Morillo, J. Peñuelas, P. B. Reich, R. D. Bardgett, A. Gaxiola, D. A. Wardle, W. H. van der putten, Climate change effects on plant-soil feedbacks and consequences for biodiversity and functioning of terrestrial ecosystems. Sci. Adv. 5, eaaz1834 (2019),
19
See supplementary materials for ecosystem fluxes during drought and recovery in an experimental forest.
20
U. Rascher, E. G. Bobich, G. H. Lin, A. Walter, T. Morris, M. Naumann, C. J. Nichol, D. Pierce, K. Bil, V. Kudeyarov, J. A. Berry, Functional diversity of photosynthesis during drought in a model tropical rainforest - the contributions of leaf area, photosynthetic electron transport and stomatal conductance to reduction in net ecosystem carbon exchange. Plant Cell Environ. 27, 1239–1256 (2004).
21
M. N. Smith, T. C. Taylor, J. van Haren, R. Rosolem, N. Restrepo-Coupe, J. Adams, J. Wu, R. C. de Oliveira, R. da Silva, A. C. de Araujo, P. B. de Camargo, T. E. Huxman, S. R. Saleska, Empirical evidence for resilience of tropical forest photosynthesis in a warmer world. Nat. Plants 6, 1225–1230 (2020).
22
R. K. Monson, S. M. Weraduwage, M. Rosenkranz, J.-P. Schnitzler, T. D. Sharkey, Leaf isoprene emission as a trait that mediates the growth-defense tradeoff in the face of climate stress. Oecologia 197, 885–902 (2021).
23
C. Werner, L. Fasbender, K. M. Romek, A. M. Yáñez-Serrano, J. Kreuzwieser, Heat Waves Change Plant Carbon Allocation Among Primary and Secondary Metabolism Altering CO2 Assimilation, Respiration, and VOC Emissions. Front. Plant Sci. 11, 1242 (2020).
24
K. J. Jardine, J. Q. Chambers, J. Holm, A. B. Jardine, C. G. Fontes, R. F. Zorzanelli, K. T. Meyers, V. F. de Souza, S. Garcia, B. O. Gimenez, L. R. Piva, N. Higuchi, P. Artaxo, S. Martin, A. O. Manzi, Green Leaf Volatile Emissions during High Temperature and Drought Stress in a Central Amazon Rainforest. Plants 4, 678–690 (2015).
25
J. Aguirre-Gutiérrez, I. Oliveras, S. Rifai, S. Fauset, S. Adu-Bredu, K. Affum-Baffoe, T. R. Baker, T. R. Feldpausch, A. Gvozdevaite, W. Hubau, N. J. B. Kraft, S. L. Lewis, S. Moore, Ü. Niinemets, T. Peprah, O. L. Phillips, K. Ziemińska, B. Enquist, Y. Malhi, Drier tropical forests are susceptible to functional changes in response to a long-term drought. Ecol. Lett. 22, 855–865 (2019).
26
F. Zellweger, P. De Frenne, J. Lenoir, P. Vangansbeke, K. Verheyen, M. Bernhardt-Römermann, L. Baeten, R. Hédl, I. Berki, J. Brunet, H. Van Calster, M. Chudomelová, G. Decocq, T. Dirnböck, T. Durak, T. Heinken, B. Jaroszewicz, M. Kopecký, F. Máliš, M. Macek, M. Malicki, T. Naaf, T. A. Nagel, A. Ortmann-Ajkai, P. Petřík, R. Pielech, K. Reczyńska, W. Schmidt, T. Standovár, K. Świerkosz, B. Teleki, O. Vild, M. Wulf, D. Coomes, Forest microclimate dynamics drive plant responses to warming. Science 368, 772–775 (2020).
27
D. Epron, M. Bahn, D. Derrien, F. A. Lattanzi, J. Pumpanen, A. Gessler, P. Högberg, P. Maillard, M. Dannoura, D. Gérant, N. Buchmann, Pulse-labelling trees to study carbon allocation dynamics: A review of methods, current knowledge and future prospects. Tree Physiol. 32, 776–798 (2012).
28
N. K. Ruehr, C. A. Offermann, A. Gessler, J. B. Winkler, J. P. Ferrio, N. Buchmann, R. L. Barnard, Drought effects on allocation of recent carbon: From beech leaves to soil CO2 efflux. New Phytol. 184, 950–961 (2009).
29
J. Aguirre-Gutiérrez, Y. Malhi, S. L. Lewis, S. Fauset, S. Adu-Bredu, K. Affum-Baffoe, T. R. Baker, A. Gvozdevaite, W. Hubau, S. Moore, T. Peprah, K. Ziemińska, O. L. Phillips, I. Oliveras, Long-term droughts may drive drier tropical forests towards increased functional, taxonomic and phylogenetic homogeneity. Nat. Commun. 11, 3346 (2020).
30
S. Haberstroh, M. C. Caldeira, R. Lobo-do-Vale, J. I. Martins, J. Moemken, J. G. Pinto, C. Werner, Nonlinear plant-plant interactions modulate impact of extreme drought and recovery on a Mediterranean ecosystem. New Phytol. 231, 1784–1797 (2021).
31
W. R. L. Anderegg, A. T. Trugman, D. R. Bowling, G. Salvucci, S. E. Tuttle, Plant functional traits and climate influence drought intensification and land-atmosphere feedbacks. Proc. Natl. Acad. Sci. U.S.A. 116, 14071–14076 (2019).
32
M. Dubbert, C. Werner, Water fluxes mediated by vegetation: Emerging isotopic insights at the soil and atmosphere interfaces. New Phytol. 221, 1754–1763 (2019).
33
M. Sprenger, C. Stumpp, M. Weiler, W. Aeschbach, S. T. Allen, P. Benettin, M. Dubbert, A. Hartmann, M. Hrachowitz, J. W. Kirchner, J. J. McDonnell, N. Orlowski, D. Penna, S. Pfahl, M. Rinderer, N. Rodriguez, M. Schmidt, C. Werner, The Demographics of Water: A Review of Water Ages in the Critical Zone Rev. Geophys. 57, 800–834 (2019).
34
E. Y. Pfannerstill, A. C. Nölscher, A. M. Yáñez-Serrano, E. Bourtsoukidis, S. Keßel, R. H. H. Janssen, A. Tsokankunku, S. Wolff, M. Sörgel, M. O. Sá, A. Araújo, D. Walter, J. Lavrič, C. Q. Dias-Júnior, J. Kesselmeier, J. Williams,Total OH Reactivity Changes Over the Amazon Rainforest During an El Niño Event. Front. For. Glob. Change 1, 12 (2018).
35
U. Pöschl, S. T. Martin, B. Sinha, Q. Chen, S. S. Gunthe, J. A. Huffman, S. Borrmann, D. K. Farmer, R. M. Garland, G. Helas, J. L. Jimenez, S. M. King, A. Manzi, E. Mikhailov, T. Pauliquevis, M. D. Petters, A. J. Prenni, P. Roldin, D. Rose, J. Schneider, H. Su, S. R. Zorn, P. Artaxo, M. O. Andreae, Rainforest aerosols as biogenic nuclei of clouds and precipitation in the Amazon. Science 329, 1513–1516 (2010).
36
L. Meredith et al., B2WALD campaign team and contributions, Version 2, University of Arizona Research Data Repository (2021).
37
T. C. Taylor, S. M. McMahon, M. N. Smith, B. Boyle, C. Violle, J. van Haren, I. Simova, P. Meir, L. V. Ferreira, P. B. de Camargo, A. C. L. da Costa, B. J. Enquist, S. R. Saleska, Isoprene emission structures tropical tree biogeography and community assembly responses to climate. New Phytol. 220, 435–446 (2018).
38
L. S. Leigh, T. Burgess, B. D. Marino, Y. D. Wei, Tropical rainforest biome of Biosphere 2: Structure, composition and results of the first 2 years of operation. Ecol. Eng. 13, 65–93 (1999).
39
B. Osmond, G. Ananyev, J. Berry, C. Langdon, Z. Kolber, G. Lin, R. Monson, C. Nichol, U. Rascher, U. Schurr, S. Smith, D. Yakir, Changing the way we think about global change research: Scaling up in experimental ecosystem science. Glob. Change Biol. 10, 393–407 (2004).
40
E. Pegoraro, L. Abrell, J. Van Haren, G. Barron-Gafford, K. A. Grieve, Y. Malhi, R. Murthy, G. Lin, The effect of elevated atmospheric CO2 and drought on sources and sinks of isoprene in a temperate and tropical rainforest mesocosm. Glob. Change Biol. 11, 1234–1246 (2005).
41
E. Pegoraro, A. Rey, L. Abrell, J. Vanharen, G. H. Lin, Drought effect on isoprene production and consumption in Biosphere 2 tropical rainforest. Glob. Change Biol. 12, 456–469 (2006).
42
J. Evaristo, M. Kim, J. Haren, L. A. Pangle, C. J. Harman, P. A. Troch, J. J. McDonnell, Characterizing the Fluxes and Age Distribution of Soil Water, Plant Water, and Deep Percolation in a Model Tropical Ecosystem. Water Resour. Res. 55, 3307–3327 (2019).
43
J. L. M. van Haren, L. L. Handley, K. Y. Biel, V. N. Kudeyarov, J. E. T. McLain, D. A. Martens, D. C. Colodner, Drought-induced nitrous oxide flux dynamics in an enclosed tropical forest. Glob. Change Biol. 11, 1247–1257 (2005).
44
H. J. Scott, Characteristics of soils in the tropical rainforest biome of Biosphere 2 after 3 years. Ecol. Eng. 13, 95–106 (1999).
45
M. Finn, The mangrove mesocosm of Biosphere 2: Design, establishment and preliminary results. Ecol. Eng. 6, 21–56 (1996).
46
P. F. Scholander, E. D. Bradstreet, E. A. Hemmingsen, H. T. Hammel, Sap Pressure in Vascular Plants: Negative hydrostatic pressure can be measured in plants. Science 148, 339–346 (1965).
47
D. J. Barrett, J. T. Hatton, J. E. Ash, M. C. Ball, Evaluation of the heat pulse velocity technique for measurement of sap flow in rainforest and eucalypt forest species of south-eastern Australia. Plant Cell Environ. 18, 463–469 (1995).
48
F. C. Meinzer, B. J. Bond, J. M. Warren, D. R. Woodruff, Does water transport scale universally with tree size? Funct. Ecol. 19, 558–565 (2005).
49
S. D. Wullschleger, A. W. King, Radial variation in sap velocity as a function of stem diameter and sapwood thickness in yellow-poplar trees. Tree Physiol. 20, 511–518 (2000).
50
T. Gebauer, V. Horna, C. Leuschner, Variability in radial sap flux density patterns and sapwood area among seven co-occurring temperate broad-leaved tree species. Tree Physiol. 28, 1821–1830 (2008).
51
M. Altaf Arain, W. James Shuttleworth, B. Farnsworth, J. Adams, O. Lutfi Sen, Comparing micrometeorology of rain forests in Biosphere-2 and Amazon basin. Agric. For. Meteorol. 100, 273–289 (2000).
52
L. A. Pangle, S. B. DeLong, N. Abramson, J. Adams, G. A. Barron-Gafford, D. D. Breshears, P. D. Brooks, J. Chorover, W. E. Dietrich, K. Dontsova, M. Durcik, J. Espeleta, T. P. A. Ferre, R. Ferriere, W. Henderson, E. A. Hunt, T. E. Huxman, D. Millar, B. Murphy, G.-Y. Niu, M. Pavao-Zuckerman, J. D. Pelletier, C. Rasmussen, J. Ruiz, S. Saleska, M. Schaap, M. Sibayan, P. A. Troch, M. Tuller, J. van Haren, X. Zeng, The Landscape Evolution Observatory: A large-scale controllable infrastructure to study coupled Earth-surface processes. Geomorphology 244, 190–203 (2015).
53
A. L. Buck, New Equations for Computing Vapor Pressure and Enhancement Factor. J. Appl. Meteorol. 20, 1527–1532 (1981).
54
L. Fasbender, A. M. Yáñez-Serrano, J. Kreuzwieser, D. Dubbert, C. Werner, Real-time carbon allocation into biogenic volatile organic compounds (BVOCs) and respiratory carbon dioxide (CO2) traced by PTR-TOF-MS, 13CO2 laser spectroscopy and 13C-pyruvate labelling. PLOS ONE 13, e0204398 (2018).
55
J. de Gouw, C. Warneke, T. Karl, G. Eerdekens, C. van der Veen, R. Fall, Sensitivity and specificity of atmospheric trace gas detection by proton-transfer-reaction mass spectrometry. Int. J. Mass Spectrom. 223-224, 365–382 (2003).
56
R. Holzinger, PTRwid: A new widget tool for processing PTR-TOF-MS data. Atmos. Meas. Tech. 8, 3903–3922 (2015).
57
J. de Gouw, C. Warneke, Measurements of volatile organic compounds in the earth’s atmosphere using proton-transfer-reaction mass spectrometry. Mass Spectrom. Rev. 26, 223–257 (2007).
58
R. Holzinger, W. J. F. Acton, W. J. Bloss, M. Breitenlechner, L. R. Crilley, S. Dusanter, M. Gonin, V. Gros, F. N. Keutsch, A. Kiendler-Scharr, L. J. Kramer, J. E. Krechmer, B. Languille, N. Locoge, F. Lopez-Hilfiker, D. Materić, S. Moreno, E. Nemitz, L. L. J. Quéléver, R. Sarda Esteve, S. Sauvage, S. Schallhart, R. Sommariva, R. Tillmann, S. Wedel, D. R. Worton, K. Xu, A. Zaytsev, Validity and limitations of simple reaction kinetics to calculate concentrations of organic compounds from ion counts in PTR-MS. Atmos. Meas. Tech. 12, 6193–6208 (2019).
59
J. M. Zobitz, J. P. Keener, H. Schnyder, D. R. Bowling, Sensitivity analysis and quantification of uncertainty for isotopic mixing relationships in carbon cycle research. Agric. For. Meteorol. 136, 56–75 (2006).
60
J. Pinheiro, D. Bates, S. DebRoy, D. Sakar, R Core Team, nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-152 (2021).
61
S. Wood, Generalized Additive Models: An Introduction with R (CRC Press, 2006).

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Published In

Science
Volume 374 | Issue 6574
17 December 2021

Submission history

Received: 30 May 2021
Accepted: 13 October 2021
Published in print: 17 December 2021

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Acknowledgments

We acknowledge valuable support from all members of the B2WALD team, as detailed in the B2WALD contribution list (36).
Funding: This work was funded by the European Research Council [ERC consolidator grant 647008 (VOCO2) to C.W.] and financial support from the Philecology Foundation to Biosphere 2 to L.K.M., with in-kind support detailed elsewhere (36).
Author contributions: C.W., L.K.M., and S.N.L. conceived and designed the study; all authors collected and/or analyzed data; C.W. wrote the first draft with input from L.K.M. and S.N.L. Data analysis was led by J.I., A.K., J.v.H., D.B., J.K., L.K.M., S.N.L., and C.W., with input from all authors. All authors revised the manuscript.
Competing interests: The authors declare no competing interests.
Data and materials availability: All data used in this manuscript are publicly available (DOI: 10.25422/azu.data.14632593).

Authors

Affiliations

Ecosystem Physiology, Faculty of Environment and Natural Resources, Albert-Ludwig-University of Freiburg, Freiburg, Germany.
School of Natural Resources and the Environment, University of Arizona, Tucson, AZ, USA.
Biosphere 2, University of Arizona, Oracle, AZ, USA.
BIO5 Institute, The University of Arizona, Tucson, AZ, USA.
Ecosystem Physiology, Faculty of Environment and Natural Resources, Albert-Ludwig-University of Freiburg, Freiburg, Germany.
Ecosystem Physiology, Faculty of Environment and Natural Resources, Albert-Ludwig-University of Freiburg, Freiburg, Germany.
Department of Ecology, University of Innsbruck, Innsbruck, Austria.
Ecosystem Physiology, Faculty of Environment and Natural Resources, Albert-Ludwig-University of Freiburg, Freiburg, Germany.
Biosphere 2, University of Arizona, Oracle, AZ, USA.
Honors College, University of Arizona, Tucson, AZ, USA.
Department of Ecology, University of Innsbruck, Innsbruck, Austria.
School of Natural Resources and the Environment, University of Arizona, Tucson, AZ, USA.
Ines Bamberger
Ecosystem Physiology, Faculty of Environment and Natural Resources, Albert-Ludwig-University of Freiburg, Freiburg, Germany.
Present address: Atmospheric Chemistry Group, University of Bayreuth, Bayreuth (BayCEER), Germany.
Institute of Geoecology - Environmental Geochemistry, Technical University Braunschweig, Braunschweig, Germany.
Department of Civil, Architectural and Environmental Engineering, University of Texas at Austin, Austin, TX, USA.
Department of Atmospheric Chemistry, Max Planck Institute for Chemistry, Mainz, Germany.
Ecosystem Physiology, Faculty of Environment and Natural Resources, Albert-Ludwig-University of Freiburg, Freiburg, Germany.
Jason Deleeuw
Biosphere 2, University of Arizona, Oracle, AZ, USA.
Biogeochemistry of Agroecosystems, University of Göttingen, Göttingen, Germany.
Geo-Biosphere Interactions, University of Tuebingen, Tuebingen, Germany.
Department of Environmental Science, University of Arizona, Tucson, AZ, USA.
Present address: Department of Land, Air and Water Resources, University of California Davis, Davis, CA, USA.
School of Natural Resources and the Environment, University of Arizona, Tucson, AZ, USA.
Biosphere 2, University of Arizona, Oracle, AZ, USA.
School of Natural Resources and the Environment, University of Arizona, Tucson, AZ, USA.
Max Planck Institute for Biogeochemistry, Jena, Germany.
Thomas Klüpfel
Department of Atmospheric Chemistry, Max Planck Institute for Chemistry, Mainz, Germany.
Aerodyne Research, Billerica, MA, USA.
Ecosystem Physiology, Faculty of Environment and Natural Resources, Albert-Ludwig-University of Freiburg, Freiburg, Germany.
Ecosystem Physiology, Faculty of Environment and Natural Resources, Albert-Ludwig-University of Freiburg, Freiburg, Germany.
Institute of Geoecology - Environmental Geochemistry, Technical University Braunschweig, Braunschweig, Germany.
Forest Dynamics, Swiss Federal Institute for Forest, Snow and Landscape Research (WSL), Birmensdorf, Switzerland.
Department of Ecology, University of Innsbruck, Innsbruck, Austria.
Department of Civil, Architectural and Environmental Engineering, University of Texas at Austin, Austin, TX, USA.
Wei-Ren Ng
Biosphere 2, University of Arizona, Oracle, AZ, USA.
Department of Atmospheric Chemistry, Max Planck Institute for Chemistry, Mainz, Germany.
Present address: Department of Environmental Science, Policy, and Management, University of California at Berkeley, Berkeley, CA, USA.
Ecosystem Physiology, Faculty of Environment and Natural Resources, Albert-Ludwig-University of Freiburg, Freiburg, Germany.
Department of Atmospheric Chemistry, Max Planck Institute for Chemistry, Mainz, Germany.
Centre for Ecology and Hydrology, University of Edinburgh, Edinburgh, UK.
Aerodyne Research, Billerica, MA, USA.
Biogeochemistry of Agroecosystems, University of Göttingen, Göttingen, Germany.
Geo-Biosphere Interactions, University of Tuebingen, Tuebingen, Germany.
BIO5 Institute, The University of Arizona, Tucson, AZ, USA.
Geo-Biosphere Interactions, University of Tuebingen, Tuebingen, Germany.
Pacific Northwest National Laboratory, Richland, WA, USA.
Department of Atmospheric Chemistry, Max Planck Institute for Chemistry, Mainz, Germany.
Energy, Environment and Water Research Center, The Cyprus Institute, Nicosia, Cyprus.

Funding Information

Philecology Foundation to Biosphere:

Notes

*Corresponding author. Email: [email protected]
These authors contributed equally to this work.

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  1. Ecosystem effects of environmental extremes, Science, 374, 6574, (1442-1443), (2021)./doi/10.1126/science.abn1406
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