Optimal stomatal control models have shown great potential in predicting stomatal behavior and improving carbon cycle modeling. Basic stomatal optimality theory posits that stomatal regulation ...maximizes the carbon gain relative to a penalty of stomatal opening. All models take a similar approach to calculate instantaneous carbon gain from stomatal opening (the gain function). Where the models diverge is in how they calculate the corresponding penalty (the penalty function). In this review, we compare and evaluate 10 different optimization models in howthey quantify the penalty andhowwell they predict stomatal responses to the environment. Weevaluate models in two ways. First, we compare their penalty functions against seven criteria that ensure a unique and qualitatively realistic solution. Second, we quantitatively test model against multiple leaf gas-exchange datasets. The optimization models with better predictive skills have penalty functions that meet our seven criteria and use fitting parameters that are both few in number and physiology based. The most skilled models are those with a penalty function based on stress-induced hydraulic failure. We conclude by proposing a new model that has a hydraulics-based penalty function that meets all seven criteria and demonstrates a highly predictive skill against our test datasets.
Drought‐related tree mortality occurs globally and may increase in the future, but we lack sufficient mechanistic understanding to accurately predict it. Here we present the first field assessment of ...the physiological mechanisms leading to mortality in an ecosystem‐scale rainfall manipulation of a piñon–juniper (Pinus edulis–Juniperus monosperma) woodland. We measured transpiration (E) and modelled the transpiration rate initiating hydraulic failure (Ecrit). We predicted that isohydric piñon would experience mortality after prolonged periods of severely limited gas exchange as required to avoid hydraulic failure; anisohydric juniper would also avoid hydraulic failure, but sustain gas exchange due to its greater cavitation resistance. After 1 year of treatment, 67% of droughted mature piñon died with concomitant infestation by bark beetles (Ips confusus) and bluestain fungus (Ophiostoma spp.); no mortality occurred in juniper or in control piñon. As predicted, both species avoided hydraulic failure, but safety margins from Ecrit were much smaller in piñon, especially droughted piñon, which also experienced chronically low hydraulic conductance. The defining characteristic of trees that died was a 7 month period of near‐zero gas exchange, versus 2 months for surviving piñon. Hydraulic limits to gas exchange, not hydraulic failure per se, promoted drought‐related mortality in piñon pine.
Hydraulic systems of plants have evolved in the context of carbon allocation and fitness trade‐offs of maximizing carbon gain and water transport in the face of short and long‐term fluctuations in ...environmental conditions. The resulting diversity of traits include a continuum of isohydry‐anisohydry or high to low relative stomatal closure during drought, shedding of canopy foliage or disconnecting roots from soil to survive drought, and adjusting root areas to efficiently manage canopy water costs associated with photosynthesis. These traits are examined within TREES, an integrated model that explicitly couples photosynthesis and carbon allocation to soil‐plant hydraulics and canopy processes. Key advances of the model are its ability to account for differences in soil and xylem cavitation, transience of hydraulic impairment associated with delayed or no refilling of xylem, and carbon allocation to plant structures based on photosynthetic uptake of carbon and hydraulic limitations to water transport. The model was used to examine hydraulic traits of cooccurring isohydric (piñon pine) and anisohydric (one‐seed juniper) trees from a field‐based experimental drought. Model predictions of both transpiration and leaf water potential were improved when there was no refilling of xylem over simulations where xylem was able refill in response to soil water recharge. Model experiments with alternative root‐to‐leaf area ratios (RR/L) showed the RR/L that supports maximum cumulative water use is not beneficial for supporting maximum carbon gain during extended drought, illustrating how a process model reveals trade‐offs in plant traits.
Key Points:
Stomatal conductance is modeled using physical equations with xylem cavitation
Simulation of drought transpiration and leaf water potential was improved
Transient response to cavitation helps to explain optimal hydraulic traits
We tested the hypothesis that greater cavitation resistance correlates with less total inter-vessel pit area per vessel (the pit area hypothesis) and evaluated a trade-off between cavitation safety ...and transport efficiency. Fourteen species of diverse growth form (vine, ring- and diffuse-porous tree, shrub) and family affinity were added to published data predominately from the Rosaceae (29 species total). Two types of vulnerability-to-cavitation curves were found. Ring-porous trees and vines showed an abrupt drop in hydraulic conductivity with increasing negative pressure, whereas hydraulic conductivity in diffuse-porous species generally decreased gradually. The ring-porous type curve was not an artifact of the centrifuge method because it was obtained also with the air-in-jection technique. A safety versus efficiency trade-off was evident when curves were compared across species: for a given pressure, there was a limited range of optimal vulnerability curves. The pit area hypothesis was supported by a strong relationship (r2 = 0.77) between increasing cavitation resistance and diminishing pit membrane area per vessel (A(P)). Small A(P) was associated with small vessel surface area and hence narrow vessel diameter (D) and short vessel length (L)-consistent with an increase in vessel flow resistance with cavitation resistance. This trade-off was amplified at the tissue level by an increase in xylem/vessel area ratio with cavitation resistance. Ring-porous species were more efficient than diffuse-porous species on a vessel basis but not on a xylem basis owing to higher xylem/vessel area ratios in ring-porous anatomy. Across four orders of magnitude, lumen and end-wall resistivities maintained a relatively tight proportionality with a near-optimal mean of 56% of the total vessel resistivity residing in the end-wall. This was consistent with an underlying scaling of L to D(3/2) across species. Pit flow resistance did not increase with cavitation safety, suggesting that cavitation pressure was not related to mean pit membrane porosity.
Ice formation in the xylem sap produces air bubbles that under negative xylem pressures may expand and cause embolism in the xylem conduits. We used the centrifuge method to evaluate the relationship ...between freeze-thaw embolism and conduit diameter across a range of xylem pressures (Psubscript x) in the conifers Pinus contorta and Juniperus scopulorum. Vulnerability curves showing loss of conductivity (embolism) with Psubscript x down to -8 MPa were generated with versus without superimposing a freeze-thaw treatment. In both species, the freeze-thaw plus water-stress treatment caused more embolism than water stress alone. We estimated the critical conduit diameter (Dsubscript f) above which a tracheid will embolize due to freezing and thawing and found that it decreased from 35 microm at a Psubscript x of -0.5 MPa to 6 microm at -8 MPa. Further analysis showed that the proportionality between diameter of the air bubble nucleating the cavitation and the diameter of the conduit (kL) declined with increasingly negative Psubscript x. This suggests that the bubbles causing cavitation are smaller in proportion to tracheid diameter in narrow tracheids than in wider ones. A possible reason for this is that the rate of dissolving increases with bubble pressure, which is inversely proportional to bubble diameter (La Place's law). Hence, smaller bubbles shrink faster than bigger ones. Last, we used the empirical relationship between Psubscript x and Dsubscript f to model the freeze-thaw response in conifer species.
ABSTRACT
The hypothesis that greater safety from cavitation by air‐seeding through inter‐vessel pits comes at the cost of less porous pit membranes with greater flow resistance was tested . Sixteen ...vessel‐bearing species were compared: 11 from the Rosaceae, four from other angiosperm families, and one fern. Unexpectedly, there was no relationship between pit resistance (and hence the prevailing membrane porosity) and cavitation pressure. There was, however, an inverse relationship between pit area per vessel and vulnerability to cavitation (r2 = 0.75). This suggests that cavitation is caused by the rare largest membrane pore per vessel, the average size of which increases with total pit area per vessel. If safety from cavitation constrains pit membrane surface area, it also limits vessel surface area and the minimum vessel resistivity. This trade‐off was consistent with an approximately three‐fold increase in vessel resistivity with cavitation pressure dropping from −0.8 to −6.6 MPa. The trade‐off was compensated for by a reduction in the percentage of vessel wall pitted: from 10–16% in vulnerable species to 2–4% in resistant species. Across species, end‐wall pitting accounted for 53 ± 3% of the total xylem resistivity. This corresponded to vessels achieving on average 94 ± 2% of their maximum possible conductivity if vessel surface area is constrained.
Eudicot angiosperms with greater vulnerability to xylem cavitation tend to have vessels with greater total area of inter-vessel pits, which inspired the 'rare pit' hypothesis: the more pits per ...vessel, by chance the leakier will be the vessel's single air-seeding pit and the lower the air-seeding threshold for cavitation to spread between vessels. Here, we demonstrate the feasibility of the hypothesis, using probability theory to model the axial propagation of air through air-injected stems. In the presence of rare, leaky pits, air-seeding pressures through short stems with few vessel ends in series should be low; pressures should increase in longer stems as more end-walls must be breached. Measurements on three Acer species conformed closely to model predictions, confirming the rare presence of leaky pits. The model indicated that pits air-seeding at or below the mean cavitation pressure (MCP) occurred at similarly low frequencies in all species. Average end-wall air-seeding pressures predicted by the model closely matched species' MCPs. Differences in species' vulnerability were primarily attributed to differences in frequency of the leakiest pits rather than pit number or area per vessel. Adjustments in membrane properties and extent of pitting per vessel apparently combine to influence cavitation resistance across species.
The standard centrifuge method has been frequently used to measure vulnerability to xylem cavitation. This method has recently been questioned. It was hypothesized that open vessels lead to ...exponential vulnerability curves, which were thought to be indicative of measurement artifact. We tested this hypothesis in stems of olive (Olea europea) because its long vessels were recently claimed to produce a centrifuge artifact. We evaluated three predictions that followed from the open vessel artifact hypothesis: shorter stems, with more open vessels, would be more vulnerable than longer stems; standard centrifuge‐based curves would be more vulnerable than dehydration‐based curves; and open vessels would cause an exponential shape of centrifuge‐based curves. Experimental evidence did not support these predictions. Centrifuge curves did not vary when the proportion of open vessels was altered. Centrifuge and dehydration curves were similar. At highly negative xylem pressure, centrifuge‐based curves slightly overestimated vulnerability compared to the dehydration curve. This divergence was eliminated by centrifuging each stem only once. The standard centrifuge method produced accurate curves of samples containing open vessels, supporting the validity of this technique and confirming its utility in understanding plant hydraulics. Seven recommendations for avoiding artefacts and standardizing vulnerability curve methodology are provided.
Corner's rule states that thicker twigs bear larger leaves. The exact nature of this relationship and why it should occur has been the subject of numerous studies. It is obvious that thicker twigs ...should support greater total leaf area (Formula: see text) for hydraulical and mechanical reasons. But it is not obvious why mean leaf size (Formula: see text) should scale positively with Formula: see text We asked what this scaling relationship is within species and how variable it is across species. We then developed a model to explain why these relationships exist.
To minimize potential sources of variability, we compared twig properties from six co-occurring and functionally similar species: Acer grandidentatum, Amelanchier alnifolia, Betula occidentalis, Cornus sericea, Populus fremontii and Symphoricarpos oreophilus We modelled the economics of leaf display, weighing the benefit from light absorption against the cost of leaf tissue, to predict the optimal Formula: see text combinations under different canopy openings.
We observed a common Formula: see text by Formula: see text exponent of 0.6, meaning that Formula: see textand leaf number on twigs increased in a specific coordination. Common scaling exponents were not supported for relationships between any other measured twig properties. The model consistently predicted positive Formula: see text by Formula: see text scaling when twigs optimally filled canopy openings. The observed 0·6 exponent was predicted when self-shading decreased with larger canopy opening.
Our results suggest Corner's rule may be better understood when recast as positive Formula: see text by Formula: see text scaling. Our model provides a tentative explanation of observed Formula: see text by Formula: see text scaling and suggests different scaling may exist in different environments.
Coniferous, diffuse-porous and ring-porous trees vary in their xylem anatomy, but the functional consequences of these differences are not well understood from the scale of the conduit to the ...individual. Hydraulic and anatomical measurements were made on branches and trunks from 16 species from temperate and tropical areas, representing all three wood types. Scaling of stem conductivity (Kh) with stem diameter was used to model the hydraulic conductance of the stem network. Ring-porous trees showed the steepest increase in Kh with stem size. Temperate diffuse-porous trees were at the opposite extreme, and conifers and tropical diffuse-porous species were intermediate. Scaling of Kh was influenced by differences in the allometry of conduit diameter (taper) and packing (number per wood area) with stem size. The Kh trends were mirrored by the modeled stem-network conductances. Ring-porous species had the greatest network conductance and this value increased isometrically with trunk basal area, indicating that conductance per unit sapwood was independent of tree size. Conductances were lowest and most size-dependent in conifers. The results indicate that differences in conduit taper and packing between functional types propagate to the network level and have an important influence on metabolic scaling concepts.
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