Mediterranean winter rainfall in phase with African monsoons during the past 1.36 million years.

Mediterranean climates are characterized by strong seasonal contrasts between dry summers and wet winters. Changes in winter rainfall are critical for regional socioeconomic development, but are difficult to simulate accurately1 and reconstruct on Quaternary timescales. This is partly because regional hydroclimate records that cover multiple glacial-interglacial cycles2,3 with different orbital geometries, global ice volume and atmospheric greenhouse gas concentrations are scarce. Moreover, the underlying mechanisms of change and their persistence remain unexplored. Here we show that, over the past 1.36 million years, wet winters in the northcentral Mediterranean tend to occur with high contrasts in local, seasonal insolation and a vigorous African summer monsoon. Our proxy time series from Lake Ohrid on the Balkan Peninsula, together with a 784,000-year transient climate model hindcast, suggest that increased sea surface temperatures amplify local cyclone development and refuel North Atlantic low-pressure systems that enter the Mediterranean during phases of low continental ice volume and high concentrations of atmospheric greenhouse gases. A comparison with modern reanalysis data shows that current drivers of the amount of rainfall in the Mediterranean share some similarities to those that drive the reconstructed increases in precipitation. Our data cover multiple insolation maxima and are therefore an important benchmark for testing climate model performance.

Optimal allocation of leaf epidermal area for gas exchange.

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 (gsmax ) 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allometric relationships between stomatal traits were tested with a comprehensive compilation of published and unpublished data on 1057 species from all major clades.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 gsmax . 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.

Global CO2 rise leads to reduced maximum stomatal conductance in Florida vegetation.

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.

Climate forcing due to optimization of maximal leaf conductance in subtropical vegetation under rising CO2.

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.

A role for atmospheric CO2 in preindustrial climate forcing.

Complementary to measurements in Antarctic ice cores, stomatal frequency analysis of leaves of land plants preserved in peat and lake deposits can provide a proxy record of preindustrial atmospheric CO(2) concentration. CO(2) trends based on leaf remains of Quercus robur (English oak) from the Netherlands support the presence of significant CO(2) variability during the first half of the last millennium. The amplitude of the reconstructed multidecadal fluctuations, up to 34 parts per million by volume, considerably exceeds maximum shifts measured in Antarctic ice. Inferred changes in CO(2) radiative forcing are of a magnitude similar to variations ascribed to other mechanisms, particularly solar irradiance and volcanic activity, and may therefore call into question the concept of the Intergovernmental Panel on Climate Change, which assumes an insignificant role of CO(2) as a preindustrial climate-forcing factor. The stomata-based CO(2) trends correlate with coeval sea-surface temperature trends in the North Atlantic Ocean, suggesting the possibility of an oceanic source/sink mechanism for the recorded CO(2) changes.

Effects of experimental warming on Betula nana epidermal cell growth tested over its maximum climatological growth range.

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.

Deep drilling reveals massive shifts in evolutionary dynamics after formation of ancient ecosystem.

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.

Tree-ring isotopes suggest atmospheric drying limits temperature-growth responses of treeline bristlecone pine.

Altitudinally separated bristlecone pine populations in the White Mountains (California, USA) exhibit differential climate-growth responses as temperature and tree-water relations change with altitude. These populations provide a natural experiment to explore the ecophysiological adaptations of this unique tree species to the twentieth century climate variability. We developed absolutely dated annual ring-width chronologies, and cellulose stable carbon and oxygen isotope chronologies from bristlecone pine growing at the treeline (~3500 m) and ~200 m below for the period AD 1710-2010. These chronologies were interpreted in terms of ecophysiological adaptations to climate variability with a dual-isotope model and a leaf gas exchange model. Ring widths show positive tree growth anomalies at treeline and consistent slower growth below treeline in relation to the twentieth century warming and associated atmospheric drying until the 1980s. Growth rates of both populations declined during and after the 1980s when growing-season temperature and atmospheric vapour pressure deficit continued to increase. Our model-based interpretations of the cellulose stable isotopes indicate that positive treeline growth anomalies prior to the 1980s were related to increased stomatal conductance and leaf-level transpiration and photosynthesis. Reduced growth since the 1980s occurred with a shift to more conservative leaf gas exchange in both the treeline and below-treeline populations, whereas leaf-level photosynthesis continued to increase in response to rising atmospheric CO2 concentrations. Our results suggest that warming-induced atmospheric drying confounds positive growth responses of apparent temperature-limited bristlecone pine populations at treeline. In addition, the observed ecophysiological responses of attitudinally separated bristlecone pine populations illustrate the sensitivity of conifers to climate change.

Seasonality modulates the predictive skills of diatom based salinity transfer functions.

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.

Multi-Year Leaf-Level Response to Sub-Ambient and Elevated Experimental CO2 in Betula nana.

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.

Region-specific sensitivity of anemophilous pollen deposition to temperature and precipitation.

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.

Drought stress signals in modern and subfossil Quercus laurifolia (Fagaceae) leaves reflect winter precipitation in southern Florida tied to El Nino-Southern Oscillation activity.

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/mm(2), 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.