Global gene flow releases invasive plants from environmental constraints on genetic diversity.

When plants establish outside their native range, their ability to adapt to the new environment is influenced by both demography and dispersal. However, the relative importance of these two factors is poorly understood. To quantify the influence of demography and dispersal on patterns of genetic diversity underlying adaptation, we used data from a globally distributed demographic research network comprising 35 native and 18 nonnative populations of Plantago lanceolata Species-specific simulation experiments showed that dispersal would dilute demographic influences on genetic diversity at local scales. Populations in the native European range had strong spatial genetic structure associated with geographic distance and precipitation seasonality. In contrast, nonnative populations had weaker spatial genetic structure that was not associated with environmental gradients but with higher within-population genetic diversity. Our findings show that dispersal caused by repeated, long-distance, human-mediated introductions has allowed invasive plant populations to overcome environmental constraints on genetic diversity, even without strong demographic changes. The impact of invasive plants may, therefore, increase with repeated introductions, highlighting the need to constrain future introductions of species even if they already exist in an area.

Phenotypic plasticity masks range-wide genetic differentiation for vegetative but not reproductive traits in a short-lived plant.

Genetic differentiation and phenotypic plasticity jointly shape intraspecific trait variation, but their roles differ among traits. In short-lived plants, reproductive traits may be more genetically determined due to their impact on fitness, whereas vegetative traits may show higher plasticity to buffer short-term perturbations. Combining a multi-treatment greenhouse experiment with observational field data throughout the range of a widespread short-lived herb, Plantago lanceolata, we (1) disentangled genetic and plastic responses of functional traits to a set of environmental drivers and (2) assessed how genetic differentiation and plasticity shape observational trait-environment relationships. Reproductive traits showed distinct genetic differentiation that largely determined observational patterns, but only when correcting traits for differences in biomass. Vegetative traits showed higher plasticity and opposite genetic and plastic responses, masking the genetic component underlying field-observed trait variation. Our study suggests that genetic differentiation may be inferred from observational data only for the traits most closely related to fitness.

Global patterns of biomass allocation in woody species with different tolerances of shade and drought: evidence for multiple strategies.

The optimal partitioning theory predicts that plants of a given species acclimate to different environments by allocating a larger proportion of biomass to the organs acquiring the most limiting resource. Are similar patterns found across species adapted to environments with contrasting levels of abiotic stress? We tested the optimal partitioning theory by analysing how fractional biomass allocation to leaves, stems and roots differed between woody species with different tolerances of shade and drought in plants of different age and size (seedlings to mature trees) using a global dataset including 604 species. No overarching biomass allocation patterns at different tolerance values across species were found. Biomass allocation varied among functional types as a result of phenological (deciduous vs evergreen broad-leaved species) and broad phylogenetical (angiosperms vs gymnosperms) differences. Furthermore, the direction of biomass allocation responses between tolerant and intolerant species was often opposite to that predicted by the optimal partitioning theory. We conclude that plant functional type is the major determinant of biomass allocation in woody species. We propose that interactions between plant functional type, ontogeny and species-specific stress tolerance adaptations allow woody species with different shade and drought tolerances to display multiple biomass partitioning strategies.

The triangular space of abiotic stress tolerance in woody species: a unified trade-off model.

Tolerance of abiotic stress in woody plants is known to be constrained by biological trade-offs between different forms of stress, especially shade and drought. However, there is still considerable uncertainty on the relationship between tolerances and the limits on tolerance combinations. Using the most extensive database available on shade, drought, waterlogging and cold tolerance for 799 northern hemisphere woody species, we determined the number of dimensions needed to summarise their tolerance combinations, and the best trade-off model among those currently available, for description of the interdependence between tolerances. Two principal component analysis (PCA) dimensions summarised stress tolerance combinations. They defined a triangular stress tolerance space (STS). The first STS dimension reflected segregation between drought-tolerant and waterlogging-tolerant species. The second reflected shade tolerance, which is independent of the other tolerances. Cold tolerance scaled weakly with both dimensions. Tolerance combinations across the species in the database were limited by boundary-line trade-offs. The STS reconciles all major theories about trade-offs between abiotic stress tolerances, providing a unified trade-off model and a set of coordinates that can be used to examine how other aspects of plant biology, such as plant functional traits, change within the limits of abiotic stress tolerance.

Temperature and pH define the realised niche space of arbuscular mycorrhizal fungi.

The arbuscular mycorrhizal (AM) fungi are a globally distributed group of soil organisms that play critical roles in ecosystem function. However, the ecological niches of individual AM fungal taxa are poorly understood. We collected > 300 soil samples from natural ecosystems worldwide and modelled the realised niches of AM fungal virtual taxa (VT; approximately species-level phylogroups). We found that environmental and spatial variables jointly explained VT distribution worldwide, with temperature and pH being the most important abiotic drivers, and spatial effects generally occurring at local to regional scales. While dispersal limitation could explain some variation in VT distribution, VT relative abundance was almost exclusively driven by environmental variables. Several environmental and spatial effects on VT distribution and relative abundance were correlated with phylogeny, indicating that closely related VT exhibit similar niche optima and widths. Major clades within the Glomeraceae exhibited distinct niche optima, Acaulosporaceae generally had niche optima in low pH and low temperature conditions, and Gigasporaceae generally had niche optima in high precipitation conditions. Identification of the realised niche space occupied by individual and phylogenetic groups of soil microbial taxa provides a basis for building detailed hypotheses about how soil communities respond to gradients and manipulation in ecosystems worldwide.

Are stomata in ferns and allies sluggish? Stomatal responses to CO2 , humidity and light and their scaling with size and density.

Fast stomatal reactions enable plants to successfully cope with a constantly changing environment yet there is an ongoing debate on the stomatal regulation mechanisms in basal plant groups. We measured stomatal morphological parameters in 29 fern and allied species from temperate to tropical biomes and two outgroup angiosperm species. Stomatal dynamic responses to environmental drivers were measured in 16 ferns and the two angiosperms using a gas-exchange system. Principal components analyses were used to further reveal the structure-function relationships in stomata. We show a > 10-fold variation for stomatal opening delays and 20-fold variation for stomatal closing delays in ferns. Across species, stomatal responses to vapor pressure deficit (VPD) were the fastest, while light and [CO2 ] responses were slower. In most cases the outgroup species' reaction speeds to changes in environmental variables were similar to those of ferns. Correlations between stomatal response rate and size were apparent for stomatal opening in light and low [CO2 ] while not evident for closing reactions and changes in VPD. No correlations between stomatal density and response speed were observed. Together, this study demonstrates different mechanisms controlling stomatal reactions in ferns at different environmental stimuli, which should be considered in future studies relating stomatal morphology and function.

Contrasting co-occurrence patterns of photobiont and cystobasidiomycete yeast associated with common epiphytic lichen species.

The popular dual definition of lichen symbiosis is under question with recent findings of additional microbial partners living within the lichen body. Here we compare the distribution and co-occurrence patterns of lichen photobiont and recently described secondary fungus (Cyphobasidiales yeast) to evaluate their dependency on lichen host fungus (mycobiont). We sequenced the nuclear internal transcribed spacer (ITS) strands for mycobiont, photobiont, and yeast from six widespread northern hemisphere epiphytic lichen species collected from 25 sites in Switzerland and Estonia. Interaction network analyses and multivariate analyses were conducted on operational taxonomic units based on ITS sequence data. Our study demonstrates the frequent presence of cystobasidiomycete yeasts in studied lichens and shows that they are much less mycobiont-specific than the photobionts. Individuals of different lichen species growing on the same tree trunk consistently hosted the same or closely related mycobiont-specific Trebouxia lineage over geographic distances while the cystobasidiomycete yeasts were unevenly distributed over the study area - contrasting communities were found between Estonia and Switzerland. These results contradict previous findings of high mycobiont species specificity of Cyphobasidiales yeast at large geographic scales. Our results suggest that the yeast might not be as intimately associated with the symbiosis as is the photobiont.

Extremely thick cell walls and low mesophyll conductance: welcome to the world of ancient living!

Mesophyll conductance is thought to be an important photosynthetic limitation in gymnosperms, but they currently constitute the most understudied plant group in regard to the extent to which photosynthesis and intrinsic water use efficiency are limited by mesophyll conductance. A comprehensive analysis of leaf gas exchange, photosynthetic limitations, mesophyll conductance (calculated by three methods previously used for across-species comparisons), and the underlying ultra-anatomical, morphological and chemical traits in 11 gymnosperm species varying in evolutionary history was performed to gain insight into the evolution of structural and physiological controls on photosynthesis at the lower return end of the leaf economics spectrum. Two primitive herbaceous species were included in order to provide greater evolutionary context. Low mesophyll conductance was the main limiting factor of photosynthesis in the majority of species. The strongest sources of limitation were extremely thick mesophyll cell walls, high chloroplast thickness and variation in chloroplast shape and size, and the low exposed surface area of chloroplasts per unit leaf area. In gymnosperms, the negative relationship between net assimilation per mass and leaf mass per area reflected an increased mesophyll cell wall thickness, whereas the easy-to-measure integrative trait of leaf mass per area failed to predict the underlying ultrastructural traits limiting mesophyll conductance.

The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait.

Ferns and fern allies have low photosynthetic rates compared with seed plants. Their photosynthesis is thought to be limited principally by physical CO2 diffusion from the atmosphere to chloroplasts. The aim of this study was to understand the reasons for low photosynthesis in species of ferns and fern allies (Lycopodiopsida and Polypodiopsida). We performed a comprehensive assessment of the foliar gas-exchange and mesophyll structural traits involved in photosynthetic function for 35 species of ferns and fern allies. Additionally, the leaf economics spectrum (the interrelationships between photosynthetic capacity and leaf/frond traits such as leaf dry mass per unit area or nitrogen content) was tested. Low mesophyll conductance to CO2 was the main cause for low photosynthesis in ferns and fern allies, which, in turn, was associated with thick cell walls and reduced chloroplast distribution towards intercellular mesophyll air spaces. Generally, the leaf economics spectrum in ferns follows a trend similar to that in seed plants. Nevertheless, ferns and allies had less nitrogen per unit DW than seed plants (i.e. the same slope but a different intercept) and lower photosynthesis rates per leaf mass area and per unit of nitrogen.

A compendium of temperature responses of Rubisco kinetic traits: variability among and within photosynthetic groups and impacts on photosynthesis modeling.

The present study provides a synthesis of the in vitro and in vivo temperature responses of Rubisco Michaelis-Menten constants for CO2 (Kc) and O2 (Ko), specificity factor (Sc,o) and maximum carboxylase turnover rate (kcatc) for 49 species from all the main photosynthetic kingdoms of life. Novel correction routines were developed for in vitro data to remove the effects of study-to-study differences in Rubisco assays. The compilation revealed differences in the energy of activation (∆Ha) of Rubisco kinetics between higher plants and other photosynthetic groups, although photosynthetic bacteria and algae were under-represented and very few species have been investigated so far. Within plants, the variation in Rubisco temperature responses was related to species' climate and photosynthetic mechanism, with differences in ∆Ha for kcatc among C3 plants from cool and warm environments, and in ∆Ha for kcatc and Kc among C3 and C4 plants. A negative correlation was observed among ∆Ha for Sc/o and species' growth temperature for all data pooled, supporting the convergent adjustment of the temperature sensitivity of Rubisco kinetics to species' thermal history. Simulations of the influence of varying temperature dependences of Rubisco kinetics on Rubisco-limited photosynthesis suggested improved photosynthetic performance of C3 plants from cool habitats at lower temperatures, and C3 plants from warm habitats at higher temperatures, especially at higher CO2 concentration. Thus, variation in Rubisco kinetics for different groups of photosynthetic organisms might need consideration to improve prediction of photosynthesis in future climates. Comparisons between in vitro and in vivo data revealed common trends, but also highlighted a large variability among both types of Rubisco kinetics currently used to simulate photosynthesis, emphasizing the need for more experimental work to fill in the gaps in Rubisco datasets and improve scaling from enzyme kinetics to realized photosynthesis.

Trait-based analysis of decline in plant species ranges during the 20th century: a regional comparison between the UK and Estonia.

Although the distribution ranges and abundance of many plant species have declined dramatically in recent decades, detailed analysis of these changes and their cause have only become possible following the publication of second- and third-generation national distribution atlases. Decline can now be compared both between species and in different parts of species' ranges. We extracted data from distribution atlases to compare range persistence of 736 plant species common to both the UK and Estonia between survey periods encompassing almost the same years (1969 and 1999 in the UK and 1970 and 2004 in Estonia). We determined which traits were most closely associated with variation in species persistence, whether these were the same in each country, and the extent to which they explained differences in persistence between the countries. Mean range size declined less in Estonia than in the UK (24.3% vs. 30.3%). One-third of species in Estonia (239) maintained >90% of their distribution range compared with one-fifth (141) in the UK. In Estonia, 99 species lost >50% of their range compared with 127 species in the UK. Persistence was very positively related to original range in both countries. Major differences in species persistence between the studied countries were primarily determined by biogeographic (affiliation to floristic element) and ecoevolutionary (plant strategy) factors. In contrast, within-country persistence was most strongly determined by tolerance of anthropogenic activities. Decline of species in the families Orchidaceae and Potamogetonaceae was significantly greater in the UK than in Estonia. Almost all of the 736 common and native European plant species in our study are currently declining in their range due to pressure from anthropogenic activities. Those species with low tolerance of human activity, with biotic pollination vectors and in the families referred to above are the most vulnerable, especially where human population density is high.

Polytolerance to abiotic stresses: how universal is the shade-drought tolerance trade-off in woody species?

AIMS: According to traditional ecophysiological theories stress tolerance of plants is predominately determined by universal physiochemical constraints. Plant acclimation to environmental stress therefore compromises plant performance under a different stress, hindering successful toleration of several abiotic stress factors simultaneously. Yet, recent studies have shown that these trade-offs are less exclusive than postulated so far, leaving more wiggle room for gaining polytolerance through adaptations We tested whether the polytolerance to shade and drought depends on cold and waterlogging tolerances - hypothesizing that polytolerance patterns in different species groups (angiosperms vs. gymnosperms; deciduous vs. evergreen; species originating from North America, Europe and East Asia) depend on the length of the vegetation period and species's dormancy through limiting the duration of favourable growing season. LOCATION: Northern hemisphere. METHODS: Our study analyzed four main abiotic stress factors - shade, drought, cold and waterlogging stress - for 806 Northern hemisphere woody species using cross-calibrated tolerance rankings. The importance of trade-offs among species ecological potentials was evaluated using the species-specific estimates of polytolerance to chosen factors. RESULTS: We found that both cold and waterlogging tolerance are negatively related to species' capabilities of simultaneously tolerating low light and water conditions. While this pattern was different in angiosperms and gymnosperms, species region of origin and leaf type had no effect on this relationship. MAIN CONCLUSIONS: Our results demonstrate that adaptation to different abiotic stress factors in woody plants is highly complex. Vegetation period length and dormancy are the key factors explaining why woody plants are less capable of tolerating both shade and drought in habitats where vegetation period is relatively short and water table high. While dormancy enables angiosperms to more successfully face additional stress factors besides shade and drought, gymnosperms have lower polytolerance, but are better tolerators of shade and drought when other environmental factors are favorable.

A negative heterogeneity-diversity relationship found in experimental grassland communities.

Recent meta-analyses and simulation studies have suggested that the relationship between soil resource heterogeneity and plant diversity (heterogeneity-diversity relationship; HDR) may be negative when heterogeneity occurs at small spatial scales. To explore different mechanisms that can explain a negative HDR, we conducted a mesocosm experiment combining a gradient of soil nutrient availability (low, medium, high) and scale of heterogeneity (homogeneous, large-scale heterogeneous, small-scale heterogeneous). The two heterogeneous treatments were created using chessboard combinations of low and high fertility patches, and had the same overall fertility as the homogeneous medium treatment. Soil patches were designed to be relatively larger (156 cm(2)) and smaller (39 cm(2)) than plant root extent. We found plant diversity was significantly lower in the small-scale heterogeneous treatment compared to the homogeneous treatment of the same fertility. Additionally, low fertility patches in the small-scale heterogeneous treatment had lower diversity than patches of the same size in the low fertility treatment. Shoot and root biomass were larger in the small-scale heterogeneous treatment than in the homogeneous treatment of the same fertility. Further, we found that soil resource heterogeneity may reduce diversity indirectly by increasing shoot biomass, thereby enhancing asymmetric competition for light resources. When soil resource heterogeneity occurs at small spatial scales it can lower plant diversity by increasing asymmetric competition belowground, since plants with large root systems can forage among patches and exploit soil resources. Additionally, small-scale soil heterogeneity may lower diversity indirectly, through increasing light competition, when nutrient uptake by competitive species increases shoot biomass production.

Microfragmentation concept explains non-positive environmental heterogeneity-diversity relationships.

Although recent studies have revealed that the relationship between diversity and environmental heterogeneity is not always positive, as classical niche theory predicts, scientists have had difficulty interpreting these results from an ecological perspective. We propose a new concept-microfragmentation-to explain how small-scale heterogeneity can have neutral or even negative effect on species diversity. We define microfragmentation as a community level process of splitting habitat into a more heterogeneous environment that can have non-positive effects on the diversity through habitat loss and subsequent isolation. We provide support for the microfragmentation concept with results from spatially explicit heterogeneity-diversity model simulations, in which varying sets of species (with different ratios of specialist and generalist species) were modeled at different levels of configurational heterogeneity (meaning that only the habitat structure was changed, not its composition). Our results indicate that environmental heterogeneity can affect community diversity in the same way as fragmentation at the landscape level. Although generalist species might not be seriously affected by microfragmentation, the persistence of specialist species can be seriously disturbed by small-scale patchiness. The microfragmentation concept provides new insight into community level diversity dynamics and can influence conservation and management strategies.

The magnetic signal from trunk bark of urban trees catches the variation in particulate matter exposure within and across six European cities.

Biomagnetic monitoring increasingly is applied to assess particulate matter (PM) concentrations, mainly using plant leaves sampled in small geographical area and from a limited number of species. Here, the potential of magnetic analysis of urban tree trunk bark to discriminate between PM exposure levels was evaluated and bark magnetic variation was investigated at different spatial scales. Trunk bark was sampled from 684 urban trees of 39 genera in 173 urban green areas across six European cities. Samples were analysed magnetically for the Saturation isothermal remanent magnetisation (SIRM). The bark SIRM reflected well the PM exposure level at city and local scale, as the bark SIRM (i) differed between the cities in accordance with the mean atmospheric PM concentrations and (ii) increased with the cover of roads and industrial area around the trees. Furthermore, with increasing tree circumferences, the SIRM values increased, as a reflection of a tree age effect related to PM accumulation over time. Moreover, bark SIRM was higher at the side of the trunk facing the prevailing wind direction. Significant relationships between SIRM of different genera validate the possibility to combine bark SIRM from different genera to improve sampling resolution and coverage in biomagnetic studies. Thus, the SIRM signal of trunk bark from urban trees is a reliable proxy for atmospheric coarse to fine PM exposure in areas dominated by one PM source, as long as variation caused by genus, circumference and trunk side is taken into account.

The positive effect of plant diversity on soil carbon depends on climate.

Little is currently known about how climate modulates the relationship between plant diversity and soil organic carbon and the mechanisms involved. Yet, this knowledge is of crucial importance in times of climate change and biodiversity loss. Here, we show that plant diversity is positively correlated with soil carbon content and soil carbon-to-nitrogen ratio across 84 grasslands on six continents that span wide climate gradients. The relationships between plant diversity and soil carbon as well as plant diversity and soil organic matter quality (carbon-to-nitrogen ratio) are particularly strong in warm and arid climates. While plant biomass is positively correlated with soil carbon, plant biomass is not significantly correlated with plant diversity. Our results indicate that plant diversity influences soil carbon storage not via the quantity of organic matter (plant biomass) inputs to soil, but through the quality of organic matter. The study implies that ecosystem management that restores plant diversity likely enhances soil carbon sequestration, particularly in warm and arid climates.

Phenotypic dissimilarity index: Correcting for intra- and interindividual variability when quantifying phenotypic variation.

In trait-based ecology, phenotypic variation (PVar) is often quantified with measures expressing average differences between populations standardized in the range 0-1. However, these measures disregard the within-population trait variability. In addition, some of them cannot be partitioned between populations. These aspects can either alter their interpretation or limit their applicability. To overcome these problems, we propose a new measure, the phenotypic dissimilarity (PhD) index, to quantify PVar between populations in scenarios of varying within-population interindividual trait variability. PhD can also quantify within-population PVar while accounting for intraindividual trait variability. Using simulated and real data, we show that using the PhD index becomes important when the within-population trait variability is not negligible, as in all ecological studies. By accounting for within-population trait variability, the PhD index does not overestimate PVar across an environmental gradient compared to other estimators. Traits inherently vary within species. Accounting for such variability is essential to understanding species' phenotypic responses to environmental cues. The proposed PhD index will provide ecologists with a tool for quantifying PVar within species and compare it between species at different levels of biological organization. We provide an R function to calculate the PhD index.

Wild bee larval food composition in five European cities.

Urbanization poses threats and opportunities for the biodiversity of wild bees. At the same time, cities can harbor diverse wild bee assemblages, partly due to the unique plant assemblages that provide resources. While bee dietary preferences have been investigated in various studies, bee dietary studies have been conducted mostly in nonurban ecosystems and data based on plant visitation observations or palynological techniques. This data set describes the larval food preferences of four wild bee species (i.e., Chelostoma florisomne, Hylaeus communis, Osmia bicornis, and O. cornuta) common in urban areas in five different European cities (i.e., Antwerp, Belgium; Paris, France; Poznan, Poland; Tartu, Estonia; and Zurich, Switzerland). In addition, the data set describes the larval food preferences of individuals from three wild bee genera (i.e., Chelostoma sp., Hylaeus sp., and Osmia sp.) that could not be identified to the species level. These data were obtained from a Europe-level study aimed at understanding the effects of urbanization on biodiversity across different cities and cityscapes and a Swiss project aimed at understanding the effects of urban ecosystems in wild bee feeding behavior. Wild bees were sampled using standardized trap nests at 80 sites (32 in Zurich and 12 in each of the remaining cities), selected following a double gradient of available habitat at local and landscape scales. Larval pollen was obtained from the bee nests and identified using DNA metabarcoding. The data provide the plant composition at the species or genus level preferred by each bee. These unique data can be used for a wide array of research questions, including urban ecology (e.g., diversity of food sources along urban gradients), bee ecology (characterization of bee feeding preferences), or comparative studies on the urban evolution of behavioral traits between urban and nonurban sites. In addition, the data can be used to inform urban planning and conservation strategies, particularly concerning flower resources (e.g., importance of exotic species and, thus, management activities). This data set can be freely used for noncommercial purposes, and this data paper should be cited if the data is used; we request that collaboration with the data set contact person to be considered if this data set represents an important part of the data analyzed in a study.

Modelling the response of urban lichens to broad-scale changes in air pollution and climate.

To create more resilient cities, it is important that we understand the effects of the global change drivers in cities. Biodiversity-based ecological indicators (EIs) can be used for this, as biodiversity is the basis of ecosystem structure, composition, and function. In previous studies, lichens have been used as EIs to monitor the effects of global change drivers in an urban context, but only in single-city studies. Thus, we currently do not understand how lichens are affected by drivers that work on a broader scale. Therefore, our aim was to quantify the variance in lichen biodiversity-based metrics (taxonomic and trait-based) that can be explained by environmental drivers working on a broad spatial scale, in an urban context where local drivers are superimposed. To this end, we performed an unprecedented effort to sample epiphytic lichens in 219 green spaces across a continental gradient from Portugal to Estonia. Twenty-six broad-scale drivers were retrieved, including air pollution and bio-climatic variables, and their dimensionality reduced by means of a principal component analysis (PCA). Thirty-eight lichen metrics were then modelled against the scores of the first two axes of each PCA, and their variance partitioned into pollution and climate components. For the first time, we determined that 15% of the metric variance was explained by broad-scale drivers, with broad-scale air pollution showing more importance than climate across the majority of metrics. Taxonomic metrics were better explained by air pollution, as expected, while climate did not surpass air pollution in any of the trait-based metric groups. Consequently, 85% of the metric variance was shown to occur at the local scale. This suggests that further work is necessary to decipher the effects of climate change. Furthermore, although drivers working within cities are prevailing, both spatial scales must be considered simultaneously if we are to use lichens as EIs in cities at continental to global scales.