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From air to land: understanding water resources through plant-based multidisciplinary research
Science & Society
From air to land: understanding water resources through plant-based multidisciplinary research Lucas C.R. Silva Department of Land, Air & Water Resources, Plant & Environmental Sciences, University of California, Davis, CA 95616, USA
Current global challenges require solutions that cannot be delivered by any one field alone. New developments in the analysis and interpretation of plant-derived climatic records bridge traditional disciplines, advancing understanding of phenomena of great ecological and societal significance, specifically, those related to changes in the terrestrial water cycle.
The challenge The extraordinary growth of human populations over past centuries has been recognized as a driver of global transformations. Beyond direct land use impacts, human-induced changes in atmospheric composition and climate have altered the structure and function of natural ecosystems [1], exerting significant pressure on managed lands responsible for food and energy production [2]. Across biomes, the effect of climate warming is largely determined by its influence on the availability of nutrient and water resources essential for plant growth. Alterations in global carbon and nutrient cycles have long been documented and linked to human activities [3], but changes in the water cycle remain largely uncertain. For example, the Intergovernmental Panel on Climate Change describes the recent human-induced warming as ‘unprecedented over decades to millennia’. By contrast, changes in the water cycle are tentatively described as ‘likely affected by anthropogenic influence’. This discrepancy highlights a major gap in knowledge, limiting our ability to predict causes and manage consequences of climatic change. Need for an improved historical perspective Every natural and managed system that has persisted through time must have acquired some degree of resilience to climatic fluctuations. Therefore, the pursuit of solutions for challenges imposed by climatic change is in many ways synonymous with the search for historical knowledge to support theoretical and practical inquiry into sustainability. Associations between changes in the terrestrial water cycle and the decline of natural and managed systems explain why many ancient societies collapsed [4]. Some examples include extreme drought events, which coincided with the abandonment of long-established Akkadian Corresponding author: Silva, L.C.R. ([email protected]). Keywords: climatic change; drought; human–environment systems; soil–plant–atmosphere interactions; socioecology; stable isotopes; water-use efficiency. 1360-1385/ ß 2015 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2015.05.007
settlements in Mesopotamia; the decline of Mayan settlements in Central America during extended dry periods punctuated by severe droughts; and intense monsoons that caused the demise of the Cambodian ‘hydraulic’ capital Angkor, once the most extensive city in the world. By contrast, successful societal trajectories have been attributed not only to favorable environmental conditions, but also to continuous adaptation needed to overcome challenges imposed by climatic fluctuations. The notion of socioecological memory, which provides the basis for resilience theory [5], offers a representation of how historical understanding shapes responses to crisis (Figure 1). These responses fall within one of three categories: (i) no effective response; (ii) response without experience; and (iii) response with experience. In this conceptual model, the most effective response involves learning through past experiences and solutions designed to solve lower-scale reverberations of larger-scale crises [5]. For example, ‘no effective response’ characterizes a rigid centralized management plan, which often exacerbates the crisis, as opposed to a flexible decentralized adaptive one. In the case of global climatic impacts, knowledge and understanding of regional environmental and societal histories is crucial for the formulation of effective responses to solve local problems while mitigating the larger crisis. Contributions from plant sciences Much of our confidence in the ability of modern societies to adapt to climatic change stems from increasingly sophisticated irrigation and plant breeding techniques. However, we still lack basic understanding of how water resources influence the long-term sustainability of natural and managed lands. Even in regions where modern agriculture has successfully adapted to dry climates, such as the Central Valley of California and Aravah Valley of Israel, traditional methods (e.g., evaporation pans, sap flow sensors, and reference grass surfaces) provide inaccurate estimates of land water fluxes to the atmosphere. A recent global assessment of the distinct isotopic effect of transpiration and evaporation integrated in large lakes and rivers suggests that >80% of the terrestrial water loss to the atmosphere happens through plant transpiration [6], but this is still debated. A warming-induced intensification of water losses to the atmosphere has been inferred from runoff data and hydrological models, but water fluxes vary widely with land cover and management [7], making evapotranspiration the least understood of the terrestrial climate forcings. It has become apparent that the impacts of shifting water regimes cannot be predicted from the isolated Trends in Plant Science, July 2015, Vol. 20, No. 7
399
Science & Society
Exacerb
Crisis
ang Mig
ang
Trends in Plant Science July 2015, Vol. 20, No. 7
Adapve change No effecve response
Experience Response without experience
Learning TRENDS in Plant Science
Figure 1. Three generic responses to environmental crises, adapted from socioecological theory [5], including: (i) no effective response, which can amplify the crisis; (ii) reacting without experience, which can lead to ineffective responses or effective ones; and (iii) mitigating the large-scale crisis through local adaptive change informed by active learning and experience.
evaluation of plants, soils, or the atmosphere. Consideration of interactions between fast and small processes (e.g., leaf gas exchange and photosynthesis) and slow and large processes (e.g., soil development and species migration) is critical, as these regulate ecosystem carbon and water exchange, influencing global and local manifestations of global climatic change. At the landscape level, the partition between evaporation and transpiration is a function of canopy structure, ecosystem distribution, and productivity. At the community level, plant diversity is an important factor regulating the use and allocation of limiting resources, influencing root depth and soil infiltration, and affecting groundwater recharge. At the individual level, water losses are controlled by stomatal conductance, which varies among plant species depending on water availability and concentration of carbon dioxide in the atmosphere. Among the numerous methods used to measure these different processes, the study of plant isotope signals is particularly well suited for determining the effect of climatic fluctuations. Because plants respond to climatic variability, they create a natural archive of environmental history preserved in stable isotopes of photosynthesized compounds recovered from living tissue as well as from soils and sediments. Accordingly, historical knowledge of water resources can be generated by plant-derived records, which integrate the effects of atmospheric transport, physiologically regulated fluxes, and biomass decomposition, reflecting the net outcome of multi-scale interactions (Figure 2). Plant-based hydrological records The analysis of carbon isotopes of plant biomass has been used for several decades to measure water-use efficiency (i.e., the amount of carbon assimilated relative to the amount of water lost during transpiration) [8]. This same method has been recently employed to study hydrological shifts in ancient environments, such as those associated with the emergence of irrigation technology in response to drought events in the Fertile Crescent several millennia ago, inferred from the analysis of fossilized seeds [9]. 400
Combined with carbon, the study of plant oxygen isotopes has improved reconstructions of hydrological change by isolating confounding effects caused, for example, by the influence of soil fertility on plant water-use efficiency [10]. In contemporary settings, carbon isotope analysis is a powerful tool to select management strategies and plant traits that enhance water-use efficiency. However, inherent differences in metabolism limit carbon isotope analyses to C3 plants, generally excluding important crops [e.g., maize (Zea mays), sugarcane (Saccharum officinarum), and sorghum (Sorghum vulgare)] and tropical environments that are typically dominated by C4 plants (e.g., grasslands and savannas). The use of both oxygen and hydrogen isotopes provides a more general proxy for plant water use; an application that rests on the assumption that all species record changes in environmental water. This has been demonstrated by experimental and observational studies, such as the comparison between the hydrogen and oxygen isotopic composition of leaf water and cellulose, used to partition evaporation and transpiration [11]; a principle that also holds in the analysis of preserved plant compounds across geological timescales. Significant advances are now expected from the application of multi-element isotopic analyses to compounds that persist after the deposition of plant residues. The value of hydrogen isotopic composition of plant lipids recovered in soils and sediments has already been recognized as a paleo-hydrological proxy [12]. Recent analytical developments that have disclosed the oxygen isotope record of plant lipids [13] and hemicellulose-derived sugars in soils [14] now promise a more nuanced interpretation of water regime shifts as affected by evapotranspiration. These pioneering efforts have begun to indicate the possibility of compiling integrated sequences of plant-derived climatic records across biomes. Analyses and interpretation of hydrological shifts require empirical validation and simultaneous measurement of multiple isotopes applied to suitable compounds; an effort currently being undertaken by several research institutions around the world. Further developments will come from comparative analyses of isotopic records and direct measurements of water exchange across heterogeneous vegetation and moisture inputs in modern systems. Stable isotope measurements have already been used to quantify evaporation and transpiration fluxes, validated by direct micrometeorological observations (e.g., eddy covariance), and have proven superior to traditional sap flow measurements [15]. Greater understanding will come from the empirical determination of predictive functions based on modern and historic thresholds that characterize hydrologically-driven regime shifts in natural and managed systems. Broad significance The climate crisis is in many respects a human issue; one that might arguably be better addressed by disciplines within the humanities, such as political sciences, sociology, and economics. However, scientists have an obligation to generate and communicate reliable information to support decisions that favor effective adaptive responses. At the crossroads of ecological and societal transformations,
Science & Society
Trends in Plant Science July 2015, Vol. 20, No. 7
Exacerb
Crisis
ang Mig
ang
Historical knowledge
Lier deposion
Intercepon
Adapve change No effecve response
Experience Response without experience
Learning
Soil evaporaon, infiltraon, ground water depth, decomposion effect
Plant community composion, canopy and root structure, physiological effect
Water W t uptake t k
Atmosphere water input, seasonality, vapor pressure deficit, transport effect
T Transpiraon i Precipitaon TRENDS in Plant Science
Figure 2. Critical processes involved in the interpretation of climatic signals from plant-derived isotopic records, including land, air, and water resources, which provide the historical knowledge needed for learning and adapting (Figure 1).
merging the impact of human influence with physical forces is essential to identifying causes and mitigating consequences of alterations in the water cycle. The examples discussed above are only a few from the vast literature that shapes emerging research on hydrological processes regulated by soil–plant–atmosphere interactions. Although a universal protocol to study these interactions has yet to be formalized, it is clear that a next phase of understanding will demand integration of concepts from three fields: (i) physiology – understanding how plant-level processes influence water dynamics and the preservation of climatic signals in photosynthesized compounds; (ii) ecology – interpreting how communities and ecosystems respond to global and influence local climatic manifestations; and (iii) biogeochemistry – understanding how isotopic records are preserved in plant compounds before and after biomass deposition. The value of such trend in plant sciences lies in a more objective assessment of past and present experiences, required for guiding effective responses to the global climate crisis (Figures 1 and 2). Once sufficiently reproduced, plant-derived records have the potential to elucidate causal links between climatic change and societal trajectories, providing the metrics necessary to project future scenarios. Acknowledgments This work is supported by the California Department of Food and Agriculture Project #26491 and by the NSF-NIFA Water Sustainability and Climate Program #2014-67003-22077.
References 1 Grimm, N.B. et al. (2013) The impacts of climate change on ecosystem structure and function. Front. Ecol. Environ. 11, 474–482
2 Wheeler, T. and von Braun, J. (2013) Climate change impacts on global food security. Science 341, 508–513 3 Vitousek, P.M. (1994) Beyond global warming: ecology and global change. Ecology 75, 1861–1876 4 Diamond, J. (2011) Collapse: How Societies Choose to Fail or Succeed. (2nd edn), Penguin 5 Berkes, F. and Folke, C. (2002) Back to the future: ecosystem dynamics and local knowledge. In Panarchy: Understanding Transformations in Human and Natural Systems (Gunderson, L.H. and Holling, C.S., eds), pp. 121–146, Island Press 6 Jasechko, S. et al. (2013) Terrestrial water fluxes dominated by transpiration. Nature 496, 347–350 7 Baldocchi, D. (2014) Biogeochemistry: managing land and climate. Nat. Clim. Change 4, 330–331 8 Farquhar, G.D. et al. (1989) Carbon isotope discrimination and photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 503–537 9 Riehl, S. et al. (2014) Drought stress variability in ancient Near Eastern agricultural systems evidenced by d13C in barley grain. Proc. Natl. Acad. Sci. U.S.A. 111, 12348–12353 10 Maxwell, T. et al. (2014) Using multielement isotopic analysis to decipher drought impacts and adaptive management in ancient agricultural systems. Proc. Natl. Acad. Sci. U.S.A. 111, E4807–E4808 11 Voelker, S. et al. (2014) Reconstructing relative humidity from plant d18O and dD as deuterium deviations from the global meteoric water line. Ecol. Appl. 24, 960–975 12 Sachse, D. et al. (2012) Molecular paleohydrology: interpreting the hydrogen-isotopic composition of lipid biomarkers from photosynthesizing organisms. Annu. Rev. Earth Planet. Sci. 40, 221–249 13 Silva, L.C.R. et al. (2015) Beyond the cellulose: Oxygen isotope composition of plant lipids as a proxy for terrestrial water balance. Geochem. Persp. Lett. 1, 33–42 14 Zech, M. et al. (2014) Oxygen isotope ratios (18O/16O) of hemicellulosederived sugar biomarkers in plants, soils and sediments as paleoclimate proxy I: Insight from a climate chamber experiment. Geochim. Cosmochim. Acta 126, 614–623 15 Williams, D.G. et al. (2004) Evapotranspiration components determined by stable isotope, sap flow and eddy covariance techniques. Agric. For. Meteorol. 125, 241–258
401
From air to land: understanding water resources through plant-based multidisciplinary research Lucas C.R. Silva Department of Land, Air & Water Resources, Plant & Environmental Sciences, University of California, Davis, CA 95616, USA
Current global challenges require solutions that cannot be delivered by any one field alone. New developments in the analysis and interpretation of plant-derived climatic records bridge traditional disciplines, advancing understanding of phenomena of great ecological and societal significance, specifically, those related to changes in the terrestrial water cycle.
The challenge The extraordinary growth of human populations over past centuries has been recognized as a driver of global transformations. Beyond direct land use impacts, human-induced changes in atmospheric composition and climate have altered the structure and function of natural ecosystems [1], exerting significant pressure on managed lands responsible for food and energy production [2]. Across biomes, the effect of climate warming is largely determined by its influence on the availability of nutrient and water resources essential for plant growth. Alterations in global carbon and nutrient cycles have long been documented and linked to human activities [3], but changes in the water cycle remain largely uncertain. For example, the Intergovernmental Panel on Climate Change describes the recent human-induced warming as ‘unprecedented over decades to millennia’. By contrast, changes in the water cycle are tentatively described as ‘likely affected by anthropogenic influence’. This discrepancy highlights a major gap in knowledge, limiting our ability to predict causes and manage consequences of climatic change. Need for an improved historical perspective Every natural and managed system that has persisted through time must have acquired some degree of resilience to climatic fluctuations. Therefore, the pursuit of solutions for challenges imposed by climatic change is in many ways synonymous with the search for historical knowledge to support theoretical and practical inquiry into sustainability. Associations between changes in the terrestrial water cycle and the decline of natural and managed systems explain why many ancient societies collapsed [4]. Some examples include extreme drought events, which coincided with the abandonment of long-established Akkadian Corresponding author: Silva, L.C.R. ([email protected]). Keywords: climatic change; drought; human–environment systems; soil–plant–atmosphere interactions; socioecology; stable isotopes; water-use efficiency. 1360-1385/ ß 2015 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2015.05.007
settlements in Mesopotamia; the decline of Mayan settlements in Central America during extended dry periods punctuated by severe droughts; and intense monsoons that caused the demise of the Cambodian ‘hydraulic’ capital Angkor, once the most extensive city in the world. By contrast, successful societal trajectories have been attributed not only to favorable environmental conditions, but also to continuous adaptation needed to overcome challenges imposed by climatic fluctuations. The notion of socioecological memory, which provides the basis for resilience theory [5], offers a representation of how historical understanding shapes responses to crisis (Figure 1). These responses fall within one of three categories: (i) no effective response; (ii) response without experience; and (iii) response with experience. In this conceptual model, the most effective response involves learning through past experiences and solutions designed to solve lower-scale reverberations of larger-scale crises [5]. For example, ‘no effective response’ characterizes a rigid centralized management plan, which often exacerbates the crisis, as opposed to a flexible decentralized adaptive one. In the case of global climatic impacts, knowledge and understanding of regional environmental and societal histories is crucial for the formulation of effective responses to solve local problems while mitigating the larger crisis. Contributions from plant sciences Much of our confidence in the ability of modern societies to adapt to climatic change stems from increasingly sophisticated irrigation and plant breeding techniques. However, we still lack basic understanding of how water resources influence the long-term sustainability of natural and managed lands. Even in regions where modern agriculture has successfully adapted to dry climates, such as the Central Valley of California and Aravah Valley of Israel, traditional methods (e.g., evaporation pans, sap flow sensors, and reference grass surfaces) provide inaccurate estimates of land water fluxes to the atmosphere. A recent global assessment of the distinct isotopic effect of transpiration and evaporation integrated in large lakes and rivers suggests that >80% of the terrestrial water loss to the atmosphere happens through plant transpiration [6], but this is still debated. A warming-induced intensification of water losses to the atmosphere has been inferred from runoff data and hydrological models, but water fluxes vary widely with land cover and management [7], making evapotranspiration the least understood of the terrestrial climate forcings. It has become apparent that the impacts of shifting water regimes cannot be predicted from the isolated Trends in Plant Science, July 2015, Vol. 20, No. 7
399
Science & Society
Exacerb
Crisis
ang Mig
ang
Trends in Plant Science July 2015, Vol. 20, No. 7
Adapve change No effecve response
Experience Response without experience
Learning TRENDS in Plant Science
Figure 1. Three generic responses to environmental crises, adapted from socioecological theory [5], including: (i) no effective response, which can amplify the crisis; (ii) reacting without experience, which can lead to ineffective responses or effective ones; and (iii) mitigating the large-scale crisis through local adaptive change informed by active learning and experience.
evaluation of plants, soils, or the atmosphere. Consideration of interactions between fast and small processes (e.g., leaf gas exchange and photosynthesis) and slow and large processes (e.g., soil development and species migration) is critical, as these regulate ecosystem carbon and water exchange, influencing global and local manifestations of global climatic change. At the landscape level, the partition between evaporation and transpiration is a function of canopy structure, ecosystem distribution, and productivity. At the community level, plant diversity is an important factor regulating the use and allocation of limiting resources, influencing root depth and soil infiltration, and affecting groundwater recharge. At the individual level, water losses are controlled by stomatal conductance, which varies among plant species depending on water availability and concentration of carbon dioxide in the atmosphere. Among the numerous methods used to measure these different processes, the study of plant isotope signals is particularly well suited for determining the effect of climatic fluctuations. Because plants respond to climatic variability, they create a natural archive of environmental history preserved in stable isotopes of photosynthesized compounds recovered from living tissue as well as from soils and sediments. Accordingly, historical knowledge of water resources can be generated by plant-derived records, which integrate the effects of atmospheric transport, physiologically regulated fluxes, and biomass decomposition, reflecting the net outcome of multi-scale interactions (Figure 2). Plant-based hydrological records The analysis of carbon isotopes of plant biomass has been used for several decades to measure water-use efficiency (i.e., the amount of carbon assimilated relative to the amount of water lost during transpiration) [8]. This same method has been recently employed to study hydrological shifts in ancient environments, such as those associated with the emergence of irrigation technology in response to drought events in the Fertile Crescent several millennia ago, inferred from the analysis of fossilized seeds [9]. 400
Combined with carbon, the study of plant oxygen isotopes has improved reconstructions of hydrological change by isolating confounding effects caused, for example, by the influence of soil fertility on plant water-use efficiency [10]. In contemporary settings, carbon isotope analysis is a powerful tool to select management strategies and plant traits that enhance water-use efficiency. However, inherent differences in metabolism limit carbon isotope analyses to C3 plants, generally excluding important crops [e.g., maize (Zea mays), sugarcane (Saccharum officinarum), and sorghum (Sorghum vulgare)] and tropical environments that are typically dominated by C4 plants (e.g., grasslands and savannas). The use of both oxygen and hydrogen isotopes provides a more general proxy for plant water use; an application that rests on the assumption that all species record changes in environmental water. This has been demonstrated by experimental and observational studies, such as the comparison between the hydrogen and oxygen isotopic composition of leaf water and cellulose, used to partition evaporation and transpiration [11]; a principle that also holds in the analysis of preserved plant compounds across geological timescales. Significant advances are now expected from the application of multi-element isotopic analyses to compounds that persist after the deposition of plant residues. The value of hydrogen isotopic composition of plant lipids recovered in soils and sediments has already been recognized as a paleo-hydrological proxy [12]. Recent analytical developments that have disclosed the oxygen isotope record of plant lipids [13] and hemicellulose-derived sugars in soils [14] now promise a more nuanced interpretation of water regime shifts as affected by evapotranspiration. These pioneering efforts have begun to indicate the possibility of compiling integrated sequences of plant-derived climatic records across biomes. Analyses and interpretation of hydrological shifts require empirical validation and simultaneous measurement of multiple isotopes applied to suitable compounds; an effort currently being undertaken by several research institutions around the world. Further developments will come from comparative analyses of isotopic records and direct measurements of water exchange across heterogeneous vegetation and moisture inputs in modern systems. Stable isotope measurements have already been used to quantify evaporation and transpiration fluxes, validated by direct micrometeorological observations (e.g., eddy covariance), and have proven superior to traditional sap flow measurements [15]. Greater understanding will come from the empirical determination of predictive functions based on modern and historic thresholds that characterize hydrologically-driven regime shifts in natural and managed systems. Broad significance The climate crisis is in many respects a human issue; one that might arguably be better addressed by disciplines within the humanities, such as political sciences, sociology, and economics. However, scientists have an obligation to generate and communicate reliable information to support decisions that favor effective adaptive responses. At the crossroads of ecological and societal transformations,
Science & Society
Trends in Plant Science July 2015, Vol. 20, No. 7
Exacerb
Crisis
ang Mig
ang
Historical knowledge
Lier deposion
Intercepon
Adapve change No effecve response
Experience Response without experience
Learning
Soil evaporaon, infiltraon, ground water depth, decomposion effect
Plant community composion, canopy and root structure, physiological effect
Water W t uptake t k
Atmosphere water input, seasonality, vapor pressure deficit, transport effect
T Transpiraon i Precipitaon TRENDS in Plant Science
Figure 2. Critical processes involved in the interpretation of climatic signals from plant-derived isotopic records, including land, air, and water resources, which provide the historical knowledge needed for learning and adapting (Figure 1).
merging the impact of human influence with physical forces is essential to identifying causes and mitigating consequences of alterations in the water cycle. The examples discussed above are only a few from the vast literature that shapes emerging research on hydrological processes regulated by soil–plant–atmosphere interactions. Although a universal protocol to study these interactions has yet to be formalized, it is clear that a next phase of understanding will demand integration of concepts from three fields: (i) physiology – understanding how plant-level processes influence water dynamics and the preservation of climatic signals in photosynthesized compounds; (ii) ecology – interpreting how communities and ecosystems respond to global and influence local climatic manifestations; and (iii) biogeochemistry – understanding how isotopic records are preserved in plant compounds before and after biomass deposition. The value of such trend in plant sciences lies in a more objective assessment of past and present experiences, required for guiding effective responses to the global climate crisis (Figures 1 and 2). Once sufficiently reproduced, plant-derived records have the potential to elucidate causal links between climatic change and societal trajectories, providing the metrics necessary to project future scenarios. Acknowledgments This work is supported by the California Department of Food and Agriculture Project #26491 and by the NSF-NIFA Water Sustainability and Climate Program #2014-67003-22077.
References 1 Grimm, N.B. et al. (2013) The impacts of climate change on ecosystem structure and function. Front. Ecol. Environ. 11, 474–482
2 Wheeler, T. and von Braun, J. (2013) Climate change impacts on global food security. Science 341, 508–513 3 Vitousek, P.M. (1994) Beyond global warming: ecology and global change. Ecology 75, 1861–1876 4 Diamond, J. (2011) Collapse: How Societies Choose to Fail or Succeed. (2nd edn), Penguin 5 Berkes, F. and Folke, C. (2002) Back to the future: ecosystem dynamics and local knowledge. In Panarchy: Understanding Transformations in Human and Natural Systems (Gunderson, L.H. and Holling, C.S., eds), pp. 121–146, Island Press 6 Jasechko, S. et al. (2013) Terrestrial water fluxes dominated by transpiration. Nature 496, 347–350 7 Baldocchi, D. (2014) Biogeochemistry: managing land and climate. Nat. Clim. Change 4, 330–331 8 Farquhar, G.D. et al. (1989) Carbon isotope discrimination and photosynthesis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40, 503–537 9 Riehl, S. et al. (2014) Drought stress variability in ancient Near Eastern agricultural systems evidenced by d13C in barley grain. Proc. Natl. Acad. Sci. U.S.A. 111, 12348–12353 10 Maxwell, T. et al. (2014) Using multielement isotopic analysis to decipher drought impacts and adaptive management in ancient agricultural systems. Proc. Natl. Acad. Sci. U.S.A. 111, E4807–E4808 11 Voelker, S. et al. (2014) Reconstructing relative humidity from plant d18O and dD as deuterium deviations from the global meteoric water line. Ecol. Appl. 24, 960–975 12 Sachse, D. et al. (2012) Molecular paleohydrology: interpreting the hydrogen-isotopic composition of lipid biomarkers from photosynthesizing organisms. Annu. Rev. Earth Planet. Sci. 40, 221–249 13 Silva, L.C.R. et al. (2015) Beyond the cellulose: Oxygen isotope composition of plant lipids as a proxy for terrestrial water balance. Geochem. Persp. Lett. 1, 33–42 14 Zech, M. et al. (2014) Oxygen isotope ratios (18O/16O) of hemicellulosederived sugar biomarkers in plants, soils and sediments as paleoclimate proxy I: Insight from a climate chamber experiment. Geochim. Cosmochim. Acta 126, 614–623 15 Williams, D.G. et al. (2004) Evapotranspiration components determined by stable isotope, sap flow and eddy covariance techniques. Agric. For. Meteorol. 125, 241–258
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