Summary A long‐standing research focus in phytology has been to understand how plants allocate leaf epidermal space to stomata in order to achieve an economic balance between the plant's carbon needs and water use. Here, we present a quantitative theoretical framework to predict allometric relationships between morphological stomatal traits in relation to leaf gas exchange and the required allocation of epidermal area to stomata.Our theoretical framework was derived from first principles of diffusion and geometry based on the hypothesis that selection for higher anatomical maximum stomatal conductance (g smax) involves a trade‐off to minimize the fraction of the epidermis that is allocated to stomata. Predicted allometric relationships between stomatal traits were tested with a comprehensive compilation of published and unpublished data on 1057 species from all major clades.In support of our theoretical framework, stomatal traits of this phylogenetically diverse sample reflect spatially optimal allometry that minimizes investment in the allocation of epidermal area when plants evolve towards higher g smax.Our results specifically highlight that the stomatal morphology of angiosperms evolved along spatially optimal allometric relationships. We propose that the resulting wide range of viable stomatal trait combinations equips angiosperms with developmental and evolutionary flexibility in leaf gas exchange unrivalled by gymnosperms and pteridophytes.
A principle response of C3 plants to increasing concentrations of atmospheric CO 2 (CO 2 ) is to reduce transpirational water loss by decreasing stomatal conductance (g s ) and simultaneously increase assimilation rates. Via this adaptation, vegetation has the ability to alter hydrology and climate. Therefore, it is important to determine the adaptation of vegetation to the expected anthropogenic rise in CO 2 . Short-term stomatal opening-closing responses of vegetation to increasing CO 2 are described by free-air carbon enrichments growth experiments, and evolutionary adaptations are known from the geological record. However, to date the effects of decadal to centennial CO 2 perturbations on stomatal conductance are still largely unknown. Here we reconstruct a 34% (±12%) reduction in maximum stomatal conductance (g smax ) per 100 ppm CO 2 increase as a result of the adaptation in stomatal density (D) and pore size at maximal stomatal opening (a max ) of nine common species from Florida over the past 150 y. The species-specific g smax values are determined by different evolutionary development, whereby the angiosperms sampled generally have numerous small stomata and high g smax , and the conifers and fern have few large stomata and lower g smax . Although angiosperms and conifers use different D and a max adaptation strategies, our data show a coherent response in g smax to CO 2 rise of the past century. Understanding these adaptations of C3 plants to rising CO 2 after decadal to centennial environmental changes is essential for quantification of plant physiological forcing at timescales relevant for global warming, and they are likely to continue until the limits of their phenotypic plasticity are reached. cuticular analysis | subtropical vegetation L and plants play a crucial role in regulating our planet's hydrological and energy balance by transpiring water through the stomatal pores on their leaf surfaces. A fundamental response of C3 plants to increasing atmospheric CO 2 concentration (CO 2 ) is to minimize transpirational water loss by reducing diffusive stomatal conductance (g s ) and simultaneously increasing assimilation rates (1). The resulting increased intrinsic water-use efficiency (iWUE: the ratio of assimilation to g s ) improves the vegetation's drought resistance and reduces the cost associated with the leaf's water transport system like leaf venation (2, 3). On a regional to global scale, decreasing rates of transpiration concurrently affect climate through reduced cloud formation and precipitation (4) and with this exert a physiological feedback on climate and hydrology on top of the radiative forcing of increasing CO 2 (5-7). In the light of continuing anthropogenic climate change, it is therefore imperative to determine how plants adapt to rising atmospheric CO 2 .During their 400 million year history, land plants have been exposed to large variations in environmental conditions that prompted genetic adaptations toward mechanisms that optimize individual fitness. Over this period, plant ad...
Plant physiological adaptation to the global rise in atmospheric CO 2 concentration (CO 2 ) is identified as a crucial climatic forcing. To optimize functioning under rising CO 2 , plants reduce the diffusive stomatal conductance of their leaves (g s ) dynamically by closing stomata and structurally by growing leaves with altered stomatal densities and pore sizes. The structural adaptations reduce maximal stomatal conductance (g smax ) and constrain the dynamic responses of g s . Here, we develop and validate models that simulate structural stomatal adaptations based on diffusion of CO 2 and water vapor through stomata, photosynthesis, and optimization of carbon gain under the constraint of a plant physiological cost of water loss. We propose that the ongoing optimization of g smax is eventually limited by species-specific limits to phenotypic plasticity. Our model reproduces observed structural stomatal adaptations and predicts that adaptation will continue beyond double CO 2 . Owing to their distinct stomatal dimensions, angiosperms reach their phenotypic response limits on average at 740 ppm and conifers on average at 1,250 ppm CO 2 . Further, our simulations predict that doubling today's CO 2 will decrease the annual transpiration flux of subtropical vegetation in Florida by ≈60 W·m −2 . We conclude that plant adaptation to rising CO 2 is altering the freshwater cycle and climate and will continue to do so throughout this century.climate change | physiological forcing | plant evolution P lants respond to the complex of environmental signals they perceive by plastic changes in their phenotype to increase individual fitness (1). The most apparent environmental change that induces phenotypic adaptations in plants is the global increase in atmospheric CO 2 concentration (CO 2 ) (2). In response to this rise in CO 2 , plants reduce the diffusive stomatal conductance of their leaves [g s (mol·m −2 ·s −1 )] to increase drought resistance (3) and reduce physiological costs associated with water transport (4). Plants can reduce g s by dynamically closing their stomata within minutes (5, 6), and structurally within the lifespan of an individual by growing leaves with altered stomatal density [D (number of stomata·m −2 )] and pore size at maximal stomatal opening [a max (m 2 )] (7, 8). Structural adaptations thereby reduce maximal stomatal conductance [g smax (mol·m −2 · s −1 )], which critically reduces actual g s , especially when stomata are fully open during times with ample light and water (9).Reduction of g s via structural adaptation of g smax has the potential to reduce transpiration fluxes and, thus, cause land surface warming in addition to changes in the global hydrological cycle with rising CO 2 (10). This climatic effect is termed the physiological forcing of CO 2 , which acts beside and independent of its radiative forcing. Despite advances to quantify this physiological forcing with global climate models (11, 12), these models rely on semiempirical relations to simulate g s from environmental variables (...
Investigating the many internal feedbacks within the climate system is a vital component of the effort to quantify the full effects of future anthropogenic climate change. The stomatal apertures of plants tend to close and decrease in number under elevated CO2 concentrations, increasing water‐use efficiency (WUE) and reducing canopy evapotranspiration. Experimental and modelling studies reveal huge variations in these changes such that the warming associated with reduced evapotranspiration (known as physiological forcing) is neither well understood or constrained. Palaeo‐observations of changes in stomatal response and plant WUE under rising CO2 might be used to better understand the processes underlying the physiological forcing feedback and to link measured changes in plant WUE to a specific physiological change in stomata. Here we use time series of tree ring (Pinus sylvestris L.) δ13C and subfossil leaf (Betula nana L.) measurements of stomatal density and geometry to derive records of changes in intrinsic water‐use efficiency (iWUE) and maximum stomatal conductance in the Boreal zone of northern Finland and Sweden. We investigate the rate of change in both proxies, over the recent past. The independent lines of evidence from these two different Boreal species indicate increased iWUE and reduced maximum stomatal conductance of similar magnitude from preindustrial times (ca. ad 1850) to around ad 1970. After this maximum stomatal conductance continues to decrease to ad 2000 in B. nana but iWUE in P. sylvestris reaches a plateau. We suggest that northern boreal P. sylvestris might have reached a threshold in its ability to increase WUE as CO2 rises.
The scarcity of high-resolution empirical data directly tracking diversity over time limits our understanding of speciation and extinction dynamics and the drivers of rate changes. Here, we analyze a continuous species-level fossil record of endemic diatoms from ancient Lake Ohrid, along with environmental and climate indicator time series since lake formation 1.36 million years (Ma) ago. We show that speciation and extinction rates nearly simultaneously decreased in the environmentally dynamic phase after ecosystem formation and stabilized after deep-water conditions established in Lake Ohrid. As the lake deepens, we also see a switch in the macroevolutionary trade-off, resulting in a transition from a volatile assemblage of short-lived endemic species to a stable community of long-lived species. Our results emphasize the importance of the interplay between environmental/climate change, ecosystem stability, and environmental limits to diversity for diversification processes. The study also provides a new understanding of evolutionary dynamics in long-lived ecosystems.
Recurrent phases of increased pine at Lake Tulane, Florida have previously been related to strong stadials terminated by so-called Heinrich events. The climatic significance of these pine phases has been interpreted in different ways. Using a pollen-climate inference model, we quantified the climate changes and consistently found that mean summer precipitation (P JJA ) increased (0.5-0.9 mm/day) and mean November temperature increased (2.0-3.0°C) during pine phases coeval with Heinrich events and the Younger Dryas. Marine sea surface temperature records indicate that potential sources for these moisture and heat anomalies are in the Gulf of Mexico and the western tropical Atlantic. We explain this low latitude warming by an increased Loop Current facilitated by persistence of the Atlantic Warm Pool during summer. This hypothesis is supported by a climate model sensitivity analysis. A positive heat anomaly in the Gulf of Mexico and equatorial Atlantic best approximates the polleninferred climate reconstructions from Lake Tulane during the (stadials around) Heinrich events and the Younger Dryas.
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