STRADIVARI Project III: Plant Hydraulics and Water Use Strategies: From Optimization to Resilience

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Two centuries after Darwin's experiments (Darwin 1898; Scarth 1927), the role of stomatal kinetics in climate, atmospheric, hydrologic, agricultural, and ecosystem sciences remains pivotal (Hetherington and Woodward, 2003). Stomatal aperture dynamically regulates the exchange of water vapor and CO2 between plants and the atmosphere, influencing processes like atmospheric CO2 concentration, water cycling feedback on air temperature (Katul et al., 2012), sensible heat flux, and boundary layer dynamics tied to rainfall predisposition (Siqueira et al., 2009; Manoli et al., 2016). For every CO2 molecule absorbed during photosynthesis, hundreds of water vapor molecules are lost, the leaf water potential becomes more negative and this lifts the water column connecting the soil reservoir to the leaf, creates tension in the xylem, increases vulnerability to cavitation and embolism spread in a resulting feedback that further reduce leaf water potential, potentially leading to "runaway" cavitation. Over five decades, optimization theories describing stomatal kinetics have advanced significantly, incorporating soil-plant hydraulics, soil water availability, and energy constraints. However, critical gaps remain in integrating existing optimization schemes and explicitly linking schemes to plant water use strategies (WUS). WUS reflects balance between instantaneous and delayed gains, with isohydric plants prioritizing delayed gains while anisohydric plants favor immediate benefits (Manzoni et al., 2013).

Kruse

D'Amato and Rigon (2025) present a plant hydraulics framework emphasizing simplified mathematical approaches that initially omit plant capacitance. They propose replacing algebraic equations with partial differential equations analogous to the R2 equation to capture time lags observed in sap-flow experiments (Kume et al., 2008; Ferraz et al., 2015) and dynamic phenomena including water storage, discharge, and refilling (Phillips et al. 2009; Oliva Carrasco et al., 2015; Wang et al., 2019), processes fundamental to plant resilience under water stress: isohydric plants prioritize delayed gains, while anisohydric plants favor immediate benefits (Manzoni et al., 2013). In this context, D'Amato and Rigon (2025) challenges conventional wisdom by questioning whether plants evolved for resilience over optimality suggesting that plants may prioritize homeostasis amid fluctuating conditions rather than maximizing efficiency. Their work, using the water potential as a unifying variable, examines resilience as a fundamental evolutionary strategy, arguing that stability, not optimization, governs plant-water dynamics. Testing this hypothesis could transform our understanding of plant water management under climate change.
Paradigm-Shifting Innovation: D'Amato and Rigon (2025) challenge conventional wisdom by questioning whether plants evolved for resilience over optimality suggesting that plants may prioritize homeostasis amid fluctuating conditions rather than maximizing efficiency. Their work, using the water potential as a unifying variable, examines resilience as a fundamental evolutionary strategy, arguing that stability, not optimization, governs plant-water dynamics. Testing this hypothesis could transform our understanding of plant water management under climate change.
STRADIVARI breakthrough: Advancing the 1D Prospero model to 3D Rosalia and plant hydraulics modeling by providing tools to investigate resilience-based stomatal control versus optimization theories through virtual experiments. Rosalia model will implement complete Richards-like equations for plant water transport (following D'Amato and Rigon, 2025 theoretical framework) coupled with allometric scaling laws (Oleson et al., 2014) to bridge individual plant behavior to ecosystem-scale responses. The Rosalia component enables systematic comparison of plant hydraulic responses with and without water capacitance, coupled to allometric studies on vegetation populations. Rather than definitively resolving the resilience vs. optimization debate, STRADIVARI provides researchers with computational tools to explore conditions where different strategies emerge, enabling hypothesis testing through controlled virtual experiments that complement field observations.

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References - Plant Hydraulics and Water Use Strategies

• Darwin, F. 1898. "IX. Observations on Stomata." Philosophical Transactions of the Royal Society of London 190(0): 531-621.
• D'Amato, Concetta, and Riccardo Rigon. 2025. "Elementary Mathematics Helps to Shed Light on the Transpiration Budget under Water Stress." Ecohydrology: Ecosystems, Land and Water Process Interactions, Ecohydrogeomorphology 18(2).
• Dewar, R. C. 2002. "The Ball-Berry-Leuning and Tardieu-Davies Stomatal Models: Synthesis and Extension Within a Spatially Aggregated Picture of Guard Cell Function." Plant, Cell & Environment 25(11): 1383-1398.
• Ferraz, T. M., et al. 2015. "Relationships Between Sap-Flow Measurements, Whole-Canopy Transpiration and Reference Evapotranspiration in Field-Grown Papaya." Theoretical and Experimental Plant Physiology 27(3): 251-262.
• Hetherington, Alistair M., and F. Ian Woodward. 2003. "The Role of Stomata in Sensing and Driving Environmental Change." Nature 424(6951): 901-8.
• Javaux, Mathieu, et al. 2013. "Root Water Uptake: From Three-Dimensional Biophysical Processes to Macroscopic Modeling Approaches." Vadose Zone Journal 12(4): 0-16.
• Katul, Gabriel G., et al. 2012. "Evapotranspiration: A Process Driving Mass Transport and Energy Exchange in the Soil-Plant-Atmosphere-Climate System." Reviews of Geophysics 50(3): 1083.
• Kennedy, D., et al. 2019. "Implementing plant hydraulics in the community land model, version 5." Journal of Advances in Modeling Earth Systems 11: 485-513.
• Kume, T., et al. 2008. "Less Than 20-min Time Lags Between Transpiration and Stem Sap Flow in Emergent Trees in a Bornean Tropical Rainforest." Agricultural and Forest Meteorology 148(6): 1181-1189.
• Manoli, Gabriele, et al. 2016. "Soil-Plant-Atmosphere Conditions Regulating Convective Cloud Formation above Southeastern US Pine Plantations." Global Change Biology 22(6): 2238-54.
• Manzoni, Stefano, et al. 2013. "Hydraulic Limits on Maximum Plant Transpiration and the Emergence of the Safety-Efficiency Trade-Off." The New Phytologist 198(1): 169-78.
• Oleson, Mark E., et al. 2014. "Universal Hydraulics of the Flowering Plants: Vessel Diameter Scales with Stem Length across Angiosperm Lineages, Habits and Climates." Ecology Letters 17(8): 988-97.
• Oliva Carrasco, L., et al. 2015. "Water Storage Dynamics in the Main Stem of Subtropical Tree Species Differing in Wood Density, Growth Rate and Life History Traits." Tree Physiology 35(4): 354-365.
• Phillips, N. G., et al. 2009. "Using Branch and Basal Trunk Sap Flow Measurements to Estimate Whole-Plant Water Capacitance: Comment on Burgess and Dawson (2008)." Plant and Soil 315(1): 315-324.
• Scarth, G. W. 1927. "Stomatal Movement: Its Regulation and Regulatory rÔle a Review." Protoplasma 2(1): 498-511.
• Wang, H., D. Tetzlaff, and C. Soulsby. 2019. "Hysteretic Response of Sap Flow in Scots Pine (Pinus sylvestris) to Meteorological Forcing in a Humid Low Energy Headwater Catchment." Ecohydrology 12(6): e2125.

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