Summary Every existing optimal stomatal model uses photosynthetic carbon assimilation as a proxy for plant evolutionary fitness. However, assimilation and growth are often decoupled, making assimilation less ideal for representing fitness when optimizing stomatal conductance to water vapor and carbon dioxide. Instead, growth should be considered a closer proxy for fitness. We hypothesize stomata have evolved to maximize turgor‐driven growth, instead of assimilation, over entire plants' lifetimes, improving their abilities to compete and reproduce. We develop a stomata model that dynamically maximizes whole‐stem growth following principles from turgor‐driven growth models. Stomata open to assimilate carbohydrates that supply growth and osmotically generate turgor, while stomata close to prevent losses of turgor and growth due to negative water potentials. In steady state, the growth optimization model captures realistic stomatal, growth, and carbohydrate responses to environmental cues, reconciles conflicting interpretations within existing stomatal optimization theories, and explains patterns of carbohydrate storage and xylem conductance observed during and after drought. Our growth optimization hypothesis introduces a new paradigm for stomatal optimization models, elevates the role of whole‐plant carbon use and carbon storage in stomatal functioning, and has the potential to simultaneously predict gross productivity, net productivity, and plant mortality through a single, consistent modeling framework.

Increasing evidence suggests that tree growth is sink-limited by environmental and internal controls rather than by carbon availability. However, the mechanisms underlying sink-limitations are not fully understood and thus not represented in large-scale vegetation models. We develop a simple, analytically-solved, mechanistic, turgor-driven growth model (TDGM) and a phloem transport model (PTM) to explore the mechanics of phloem transport and evaluate three hypotheses. First, phloem transport must be explicitly considered to accurately predict turgor distributions and thus growth. Second, turgor-limitations can explain growth-scaling with size (metabolic scaling). Third, turgor can explain realistic growth rates and increments. We show that mechanistic, sink-limited growth schemes based on plant turgor limitations are feasible for large-scale model implementations with minimal computational demands. Our PTM predicted nearly uniform sugar concentrations along the phloem transport path regardless of phloem conductances, stem water potential gradients, and the strength of sink-demands contrary to our first hypothesis, suggesting that phloem transport is not limited generally by phloem transport capacity per se but rather by carbon demand for growth and respiration. These results enabled TDGM implementation without explicit coupling to the PTM, further simplifying computation. We test the TDGM by comparing predictions of whole-tree growth rate to well-established observations (site indices) and allometric theory. Our simple TDGM predicts realistic tree heights, growth rates, and metabolic scaling over decadal to centurial timescales, suggesting that tree growth is generally sink- and turgor-limited. Like observed trees, our TDGM captures tree-size- and resource- based deviations from the classical ¾ power-law metabolic scaling for which turgor is responsible.

Summary Trees partition biomass in response to resource limitation and physiological activity. It is presumed that these strategies evolved to optimize some measure of fitness. If the optimization criterion can be specified, then allometry can be modeled from first principles without prescribed parameterization. We present the Tree Hydraulics and Optimal Resource Partitioning (THORP) model, which optimizes allometry by estimating allocation fractions to organs as proportional to their ratio of marginal gain to marginal cost, where gain is net canopy photosynthesis rate, and costs are senescence rates. Root total biomass and profile shape are predicted simultaneously by a unified optimization. Optimal partitioning is solved by a numerically efficient analytical solution. THORP’s predictions agree with reported tree biomass partitioning in response to size, water limitations, elevated CO2 and pruning. Roots were sensitive to soil moisture profiles and grew down to the groundwater table when present. Groundwater buffered against water stress regardless of meteorology, stabilizing allometry and root profiles as deep as c. 30 m. Much of plant allometry can be explained by hydraulic considerations. However, nutrient limitations cannot be fully ignored. Rooting mass and profiles were synchronized with hydrological conditions and groundwater even at considerable depths, illustrating that the below ground shapes whole‐tree allometry.

Algal‐fungal symbionts share water, nutrients, and gases via an architecture unique to lichens. Because lichen activity is controlled by moisture dynamics, understanding water transport is prerequisite to understand their fundamental biology. We propose a model of water distributions within foliose lichens governed by laws of fluid motion. Our model differentiates between water stored in symbionts, on extracellular surfaces, and in distinct morphological layers. We parameterize our model with hydraulic properties inverted from laboratory measurements of Flavoparmelia caperata and validate for wetting and drying. We ask: (1) Where is the bottleneck to water transport? (2) How do hydration and dehydration dynamics differ? and (3) What causes these differences? Resistance to vapor flow is concentrated at thallus surfaces and acts as the bottleneck for equilibrium, while internal resistances are small. The model captures hysteresis in hydration and desiccation, which are shown to be controlled by nonlinearities in hydraulic capacitance. Muting existing nonlinearities slowed drying and accelerated wetting, while exaggerating nonlinearities accelerated drying and slowed wetting. The hydraulic nonlinearity of F. caperata is considerable, which may reflect its preference for humid and stable environments. The model establishes the physical foundation for future investigations of transport of water, gas, and sugar between symbionts.