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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allometric relationships between stomatal traits were tested with a comprehensive compilation of published and unpublished data on 1057 species from all major clades.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 CO₂ (CO₂) is to reduce transpirational water loss by decreasing stomatal conductance (gs) 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 CO₂. Short-term stomatal opening-closing responses of vegetation to increasing CO₂ 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 CO₂ perturbations on stomatal conductance are still largely unknown. Here we reconstruct a 34% (±12%) reduction in maximum stomatal conductance (gsmax) per 100 ppm CO₂ increase as a result of the adaptation in stomatal density (D) and pore size at maximal stomatal opening (amax) of nine common species from Florida over the past 150 y. The species-specific gsmax values are determined by different evolutionary development, whereby the angiosperms sampled generally have numerous small stomata and high gsmax, and the conifers and fern have few large stomata and lower gsmax. Although angiosperms and conifers use different D and amax adaptation strategies, our data show a coherent response in gsmax to CO₂ rise of the past century. Understanding these adaptations of C3 plants to rising CO₂ 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.

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.

The value of diatoms as bioindicators in contemporary and palaeolimnological studies through transfer function development has increased in the last decades. While such models represent a tremendous advance in (palaeo) ecology, they leave behind important sources of uncertainties that are often ignored. In the present study we tackle two of the most important sources of uncertainty in the development of diatom salinity inference models: the effect of secondary variables associated to seasonality and the comparison of conventional cross-validation methods with a validation based on independent datasets. Samples (diatoms and environmental variables) were taken in spring, summer and autumn in the freshwater and brackish ditches of the province of North Holland in 1993. Different locations of the same province were sampled again in 2008-2010 to validate the models. We found that the abundance of the dominant species significantly changed between the seasons, leading to inconsistent estimates of species optima and tolerances. A model covering intra-annual variability (all seasons combined) provides averages of species optima and tolerances, reduces the effect of secondary variables due to the seasonality effects, thus providing the strongest relationship between salinity and diatom species. In addition, the ¨all-season¨ model also reduces the edge effects usually found in all unimodal-based calibration methods. While based on cross-validation all four models seem to perform relatively well, a validation with an independent dataset emphasizes the importance of using models covering intra-annual variability to perform realistic reconstructions.

Numerous long-term, free-air plant growth facilities currently explore vegetation responses to the ongoing climate change in northern latitudes. Open top chamber (OTC) experiments as well as the experimental set-ups with active warming focus on many facets of plant growth and performance, but information on morphological alterations of plant cells is still scarce. Here we compare the effects of in-situ warming on leaf epidermal cell expansion in dwarf birch, Betula nana in Finland, Greenland, and Poland. The localities of the three in-situ warming experiments represent contrasting regions of B . nana distribution, with the sites in Finland and Greenland representing the current main distribution in low and high Arctic, respectively, and the continental site in Poland as a B . nana relict Holocene microrefugium. We quantified the epidermal cell lateral expansion by microscopic analysis of B . nana leaf cuticles. The leaves were produced in paired experimental treatment plots with either artificial warming or ambient temperature. At all localities, the leaves were collected in two years at the end of the growing season to facilitate between-site and within-site comparison. The measured parameters included the epidermal cell area and circumference, and using these, the degree of cell wall undulation was calculated as an Undulation Index (UI). We found enhanced leaf epidermal cell expansion under experimental warming, except for the extremely low temperature Greenland site where no significant difference occurred between the treatments. These results demonstrate a strong response of leaf growth at individual cell level to growing season temperature, but also suggest that in harsh conditions other environmental factors may limit this response. Our results provide evidence of the relevance of climate warming for plant leaf maturation and underpin the importance of studies covering large geographical scales.

The strong link between stomatal frequency and CO2 in woody plants is key for understanding past CO2 dynamics, predicting future change, and evaluating the significant role of vegetation in the hydrological cycle. Experimental validation is required to evaluate the long-term adaptive leaf response of C3 plants to CO2 conditions; however, studies to date have only focused on short-term single-season experiments and may not capture (1) the full ontogeny of leaves to experimental CO2 exposure or (2) the true adjustment of structural stomatal properties to CO2, which we postulate is likely to occur over several growing seasons. We conducted controlled growth chamber experiments at 150 ppmv, 450 ppmv and 800 ppmv CO2 with woody C3 shrub Betula nana (dwarf birch) over two successive annual growing seasons and evaluated the structural stomatal response to atmospheric CO2 conditions. We find that while some adjustment of leaf morphological and stomatal parameters occurred in the first growing season where plants are exposed to experimental CO2 conditions, amplified adjustment of non-plastic stomatal properties such as stomatal conductance occurred in the second year of experimental CO2 exposure. We postulate that the species response limit to CO2 of B. nana may occur around 400-450 ppmv. Our findings strongly support the necessity for multi-annual experiments in C3 perennials in order to evaluate the effects of environmental conditions and provide a likely explanation of the contradictory results between historical and palaeobotanical records and experimental data.

Annual shoot length of the circumarctic dwarf shrub Cassiope tetragona has proved to be a reliable proxy for past and ongoing climate change in the Arctic. This is based on its strong linear relationship with monthly climate parameters. Monthly means are, however, coarse units for prediction of growth in marginal regions with short growing seasons. An alternative to monthly averages are parameters that quantify the growing season length (GSL) and its intensity (growing degree-days; GDD5). GDD5 is defined as the cumulative daily mean temperature above 5°C. GSL is defined as the number of days on which the average temperature exceeds 5°C. The aims of this study were to test whether these parameters are a better predictor of growth than monthly means and to reconstruct past High Arctic growing season climate. Correlative analysis shows that GDD5 is a better predictor of annual shoot length growth than mean monthly temperatures and GSL, both at C. tetragona’s European northern and southern distribution limit, as well as at its assumed climatic optimum. Svalbard Airport GDD5 was reconstructed back to 1857. The reconstruction shares 61% of variance with the instrumental record. This opens the possibility to obtain an Arctic network of climate reconstructions with high temporal and spatial resolution through construction of C. tetragona shoot length chronologies.

Understanding relations between climate and pollen production is important for several societal and ecological challenges, importantly pollen forecasting for pollinosis treatment, forensic studies, global change biology, and high-resolution palaeoecological studies of past vegetation and climate fluctuations. For these purposes, we investigate the role of climate variables on annual-scale variations in pollen influx, test the regional consistency of observed patterns, and evaluate the potential to reconstruct high-frequency signals from sediment archives. A 43-year pollen-trap record from the Netherlands is used to investigate relations between annual pollen influx, climate variables (monthly and seasonal temperature and precipitation values), and the North Atlantic Oscillation climate index. Spearman rank correlation analysis shows that specifically in Alnus, Betula, Corylus, Fraxinus, Quercus and Plantago both temperature in the year prior to (T-1), as well as in the growing season (T), are highly significant factors (TApril rs between 0.30 [P<0.05[ and 0.58 [P<0.0001]; TJuli-1 rs between 0.32 [P<0.05[ and 0.56 [P<0.0001]) in the annual pollen influx of wind-pollinated plants. Total annual pollen prediction models based on multiple climate variables yield R2 between 0.38 and 0.62 (P<0.0001). The effect of precipitation is minimal. A second trapping station in the SE Netherlands, shows consistent trends and annual variability, suggesting the climate factors are regionally relevant. Summer temperature is thought to influence the formation of reproductive structures, while temperature during the flowering season influences pollen release. This study provides a first predictive model for seasonal pollen forecasting, and also aides forensic studies. Furthermore, variations in pollen accumulation rates from a sub-fossil peat deposit are comparable with the pollen trap data. This suggests that high frequency variability pollen records from natural archives reflect annual past climate variability, and can be used in palaeoecological and -climatological studies to bridge between population- and species-scale responses to climate forcing.

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 pollen-inferred climate reconstructions from Lake Tulane during the (stadials around) Heinrich events and the Younger Dryas.

In the present study, structural xeromorphic features in modern and subfossil Quercus laurifolia leaves from southern Florida were quantified to reconstruct past precipitation changes in sensitive terrestrial settings. Absolute cell numbers/mm², quantified as epidermal cell density (ED) have been analyzed on leaves from herbarium collections as well as the leaves accumulated during the past 125 years in peat deposits. The results reveal a common principal correlation between the measured ED and winter precipitation (November through March, NDJFM: Herbarium r = -0.74; peat profiles FAK98 r = -0.72, FAK02 r = -0.53) providing a measure of seasonal drought stress. In Florida, the amount of winter precipitation depends on El Niño-Southern Oscillation (ENSO) activity, where El Niño years produce wet and cold winters, while La Niña winters are dry and warm. The negative correlation between cell numbers and winter precipitation has the potential to record precipitation variability from subfossil leaves on near-annual to decadal time scales. In subtropical, terrestrial environments, where traditional paleo-proxies are limited, systematic analysis of leaf morphological characteristics can provide important information on precipitation changes through time.