Extent of intraspecific trait variability in ecologically central and marginal populations of a dominant alpine plant across European mountains.

BACKGROUND AND AIMS: Studying trait variability and restricted gene flow between populations of species can reveal species dynamics. Peripheral populations commonly exhibit lower genetic diversity and trait variability due to isolation and ecological marginality, unlike central populations experiencing gene flow and optimal conditions. This study focused on Carex curvula, the dominant species in alpine acidic meadows of European mountain regions. The species is sparser in dry areas such as the Pyrenees and Balkans, compared to the Central-Eastern Alps and Carpathians. We hypothesized that distinct population groups could be identified based on their mean functional trait values and their correlation with the environment; we predicted that ecologically marginal populations would have stronger trait correlations, lower within-population trait variability (intraspecific trait variability, ITV) and lower genetic diversity than populations of optimal habitats. METHODS: Sampling was conducted in 34 populations that spanned the entire distribution range of C. curvula. We used hierarchical clustering to identify emergent functional groups of populations, defined by combinations of multiple traits associated with nutrient economy and drought tolerance (e.g. specific leaf area, anatomy). We contrasted the geographical distribution of these groups in relation to environment and genetic structure. We compared pairwise trait relationships, within-population trait variation (ITV) and neutral genetic diversity between groups. KEY RESULTS: Our study identified emergent functional groups of populations. Those in the southernmost ranges, specifically the Pyrenees and Balkan region, showed drought-tolerant trait syndromes and correlated with indicators of limited water availability. While we noted a decline in population genetic diversity, we did not observe any significant changes in ITV in ecologically marginal (peripheral) populations. CONCLUSIONS: Our research exemplifies the relationship between ecological marginality and geographical peripherality, which in this case study is linked to genetic depauperation but not to reduced ITV. Understanding these relationships is crucial for understanding the biogeographical factors shaping trait variation.

Development of SSR markers for Carex curvula (Cyperaceae) and their importance in investigating the species genetic structure.

BACKGROUND: Microsatellite primers were developed and tested to genotype several populations of Carex curvula s. l. (Cyperaceae), in order to infer the phylogeographic relationships of the populations within species and the boundaries between the two described subspecies: C. curvula subsp. curvula and C. curvula subsp. rosae. METHODS AND RESULTS: Candidate microsatellite loci were isolated based on next-generation sequencing. We tested 18 markers for polymorphism and replicability in seven C. curvula s. l. populations and identified 13 polymorphic loci with dinucleotide repeats. Genotyping results showed the total number of alleles per locus varied from four to 23 (including both infrataxa), and the observed and expected heterozygosity ranged between 0.1 to 0.82 and 0.219 to 0.711, respectively. Furthermore, the NJ tree showed a clear separation between C. curvula subsp. curvula and C. curvula subsp. rosae. CONCLUSION: The development of these highly polymorphic markers proved to be very efficient not only in delineating between the two subspecies, but also in genetic discriminating at population level within each infrataxon. They are promising tools for evolutionary studies in Cariceae section, as well as in providing knowledge on patterns of the species phylogeography.

The tempo of greening in the European Alps: Spatial variations on a common theme.

The long-term increase in satellite-based proxies of vegetation cover is a well-documented response of seasonally snow-covered ecosystems to climate warming. However, observed greening trends are far from uniform, and substantial uncertainty remains concerning the underlying causes of this spatial variability. Here, we processed surface reflectance of the moderate resolution imaging spectroradiometer (MODIS) to investigate trends and drivers of changes in the annual peak values of the Normalized Difference Vegetation Index (NDVI). Our study focuses on above-treeline ecosystems in the European Alps. NDVI changes in these ecosystems are highly sensitive to land cover and biomass changes and are marginally affected by anthropogenic disturbances. We observed widespread greening for the 2000-2020 period, a pattern that is consistent with the overall increase in summer temperature. At the local scale, the spatial variability of greening was mainly due to the preferential response of north-facing slopes between 1900 and 2400 m. Using high-resolution imagery, we noticed that the presence of screes and outcrops locally magnified this response. At the regional scale, we identified hotspots of greening where vegetation cover is sparser than expected given the elevation and exposure. Most of these hotspots experienced delayed snow melt and green-up dates in recent years. We conclude that the ongoing greening in the Alps primarily reflects the high responsiveness of sparsely vegetated ecosystems that are able to benefit the most from temperature and water-related habitat amelioration above treeline.

Topsoil organic matter build-up in glacier forelands around the world.

Since the last glacial maximum, soil formation related to ice-cover shrinkage has been one major sink of carbon accumulating as soil organic matter (SOM), a phenomenon accelerated by the ongoing global warming. In recently deglacierized forelands, processes of SOM accumulation, including those that control carbon and nitrogen sequestration rates and biogeochemical stability of newly sequestered carbon, remain poorly understood. Here, we investigate the build-up of SOM during the initial stages (up to 410 years) of topsoil development in 10 glacier forelands distributed on four continents. We test whether the net accumulation of SOM on glacier forelands (i) depends on the time since deglacierization and local climatic conditions (temperature and precipitation); (ii) is accompanied by a decrease in its stability and (iii) is mostly due to an increasing contribution of organic matter from plant origin. We measured total SOM concentration (carbon, nitrogen), its relative hydrogen/oxygen enrichment, stable isotopic (13 C, 15 N) and carbon functional groups (C-H, C=O, C=C) compositions, and its distribution in carbon pools of different thermal stability. We show that SOM content increases with time and is faster on forelands experiencing warmer climates. The build-up of SOM pools shows consistent trends across the studied soil chronosequences. During the first decades of soil development, the low amount of SOM is dominated by a thermally stable carbon pool with a small and highly thermolabile pool. The stability of SOM decreases with soil age at all sites, indicating that SOM storage is dominated by the accumulation of labile SOM during the first centuries of soil development, and suggesting plant carbon inputs to soil (SOM depleted in nitrogen, enriched in hydrogen and in aromatic carbon). Our findings highlight the potential vulnerability of SOM stocks from proglacial areas to decomposition and suggest that their durability largely depends on the relative contribution of carbon inputs from plants.

Author Correction: A global database for metacommunity ecology, integrating species, traits, environment and space.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

A global database for metacommunity ecology, integrating species, traits, environment and space.

The use of functional information in the form of species traits plays an important role in explaining biodiversity patterns and responses to environmental changes. Although relationships between species composition, their traits, and the environment have been extensively studied on a case-by-case basis, results are variable, and it remains unclear how generalizable these relationships are across ecosystems, taxa and spatial scales. To address this gap, we collated 80 datasets from trait-based studies into a global database for metaCommunity Ecology: Species, Traits, Environment and Space; "CESTES". Each dataset includes four matrices: species community abundances or presences/absences across multiple sites, species trait information, environmental variables and spatial coordinates of the sampling sites. The CESTES database is a live database: it will be maintained and expanded in the future as new datasets become available. By its harmonized structure, and the diversity of ecosystem types, taxonomic groups, and spatial scales it covers, the CESTES database provides an important opportunity for synthetic trait-based research in community ecology.

Contrasting microbial biogeographical patterns between anthropogenic subalpine grasslands and natural alpine grasslands.

The effect of plant species composition on soil microbial communities was studied at the multiregional level. We compared the soil microbial communities of alpine natural grasslands dominated by Carex curvula and anthropogenic subalpine pastures dominated by Nardus stricta. We conducted paired sampling across the Carpathians and the Alps and used Illumina sequencing to reveal the molecular diversity of soil microbes. We found that bacterial and fungal communities exhibited contrasting regional distributions and that the distribution in each grassland is well discriminated. Beta diversity of microbial communities was much higher in C. curvula grasslands due to a marked regional effect. The composition of grassland-type core microbiomes suggest that C. curvula, and N. stricta to a lesser extent, tend to select a cohort of microbes related to antibiosis/exclusion, pathogenesis and endophytism. We discuss these findings in light of the postglacial history of the studied grasslands, the habitat connectivity and the disturbance regimes. Human-induced disturbance in the subalpine belt of European mountains has led to homogeneous soil microbial communities at large biogeographical scales. Our results confirm the overarching role of the dominant grassland plant species in the distribution of microbial communities and highlight the relevance of biogeographical history.

What it takes to invade grassland ecosystems: traits, introduction history and filtering processes.

Whether the success of alien species can be explained by their functional or phylogenetic characteristics remains unresolved because of data limitations, scale issues and weak quantifications of success. Using permanent grasslands across France (50 000 vegetation plots, 2000 species, 130 aliens) and building on the Rabinowitz's classification to quantify spread, we showed that phylogenetic and functional similarities to natives were the most important correlates of invasion success compared to intrinsic functional characteristics and introduction history. Results contrasted between spatial scales and components of invasion success. Widespread and common aliens were similar to co-occurring natives at coarse scales (indicating environmental filtering), but dissimilar at finer scales (indicating local competition). In contrast, regionally widespread but locally rare aliens showed patterns of competitive exclusion already at coarse scale. Quantifying trait differences between aliens and natives and distinguishing the components of invasion success improved our ability to understand and potentially predict alien spread at multiple scales.

Long-lasting modification of soil fungal diversity associated with the introduction of rabbits to a remote sub-Antarctic archipelago.

During the late nineteenth century, Europeans introduced rabbits to many of the sub-Antarctic islands, environments that prior to this had been devoid of mammalian herbivores. The impacts of rabbits on indigenous ecosystems are well studied; notably, they cause dramatic changes in plant communities and promote soil erosion. However, the responses of fungal communities to such biotic disturbances remain unexplored. We used metabarcoding of soil extracellular DNA to assess the diversity of plant and fungal communities at sites on the sub-Antarctic Kerguelen Islands with contrasting histories of disturbance by rabbits. Our results suggest that on these islands, the simplification of plant communities and increased erosion resulting from the introduction of rabbits have driven compositional changes, including diversity reductions, in indigenous soil fungal communities. Moreover, there is no indication of recovery at sites from which rabbits were removed 20 years ago. These results imply that introduced herbivores have long-lasting and multifaceted effects on fungal biodiversity as well as highlight the low resiliency of sub-Antarctic ecosystems.

Vegetation ecology meets ecosystem science: Permanent grasslands as a functional biogeography case study.

The effect of biodiversity on ecosystem functioning has been widely acknowledged, and the importance of the functional roles of species, as well as their diversity, in the control of ecosystem processes has been emphasised recently. However, bridging biodiversity and ecosystem science to address issues at a biogeographic scale is still in its infancy. Bridging this gap is the primary goal of the emerging field of functional biogeography. While the rise of Big Data has catalysed functional biogeography studies in recent years, comprehensive evidence remains scarce. Here, we present the rationale and the first results of a country-wide initiative focused on the C3 permanent grasslands. We aimed to collate, integrate and process large databases of vegetation relevés, plant traits and environmental layers to provide a country-wide assessment of ecosystem properties and services which can be used to improve regional models of climate and land use changes. We outline the theoretical background, data availability, and ecoinformatics challenges associated with the approach and its feasibility. We provide a case study of upscaling of leaf dry matter content averaged at ecosystem level and country-wide predictions of forage digestibility. Our framework sets milestones for further hypothesis testing in functional biogeography and earth system modelling.

Modelling snow cover duration improves predictions of functional and taxonomic diversity for alpine plant communities.

BACKGROUND AND AIMS: Quantifying relationships between snow cover duration and plant community properties remains an important challenge in alpine ecology. This study develops a method to estimate spatial variation in energy availability in the context of a topographically complex, high-elevation watershed, which was used to test the explanatory power of environmental gradients both with and without snow cover in relation to taxonomic and functional plant diversity. METHODS: Snow cover in the French Alps was mapped at 15-m resolution using Landsat imagery for five recent years, and a generalized additive model (GAM) was fitted for each year linking snow to time and topography. Predicted snow cover maps were combined with air temperature and solar radiation data at daily resolution, summed for each year and averaged across years. Equivalent growing season energy gradients were also estimated without accounting for snow cover duration. Relationships were tested between environmental gradients and diversity metrics measured for 100 plots, including species richness, community-weighted mean traits, functional diversity and hyperspectral estimates of canopy chlorophyll content. KEY RESULTS: Accounting for snow cover in environmental variables consistently led to improved predictive power as well as more ecologically meaningful characterizations of plant diversity. Model parameters differed significantly when fitted with and without snow cover. Filtering solar radiation with snow as compared without led to an average gain in R(2) of 0·26 and reversed slope direction to more intuitive relationships for several diversity metrics. CONCLUSIONS: The results show that in alpine environments high-resolution data on snow cover duration are pivotal for capturing the spatial heterogeneity of both taxonomic and functional diversity. The use of climate variables without consideration of snow cover can lead to erroneous predictions of plant diversity. The results further indicate that studies seeking to predict the response of alpine plant communities to climate change need to consider shifts in both temperature and nival regimes.

Reconstructing long-term human impacts on plant communities: an ecological approach based on lake sediment DNA.

Paleoenvironmental studies are essential to understand biodiversity changes over long timescales and to assess the relative importance of anthropogenic and environmental factors. Sedimentary ancient DNA (sedaDNA) is an emerging tool in the field of paleoecology and has proven to be a complementary approach to the use of pollen and macroremains for investigating past community changes. SedaDNA-based reconstructions of ancient environments often rely on indicator taxa or expert knowledge, but quantitative ecological analyses might provide more objective information. Here, we analysed sedaDNA to investigate plant community trajectories in the catchment of a high-elevation lake in the Alps over the last 6400 years. We combined data on past and present plant species assemblages along with sedimentological and geochemical records to assess the relative impact of human activities through pastoralism, and abiotic factors (temperature and soil evolution). Over the last 6400 years, we identified significant variation in plant communities, mostly related to soil evolution and pastoral activities. An abrupt vegetational change corresponding to the establishment of an agropastoral landscape was detected during the Late Holocene, approximately 4500 years ago, with the replacement of mountain forests and tall-herb communities by heathlands and grazed lands. Our results highlight the importance of anthropogenic activities in mountain areas for the long-term evolution of local plant assemblages. SedaDNA data, associated with other paleoenvironmental proxies and present plant assemblages, appear to be a relevant tool for reconstruction of plant cover history. Their integration, in conjunction with classical tools, offers interesting perspectives for a better understanding of long-term ecosystem dynamics under the influence of human-induced and environmental drivers.

Modelling plant species distribution in alpine grasslands using airborne imaging spectroscopy.

Remote sensing using airborne imaging spectroscopy (AIS) is known to retrieve fundamental optical properties of ecosystems. However, the value of these properties for predicting plant species distribution remains unclear. Here, we assess whether such data can add value to topographic variables for predicting plant distributions in French and Swiss alpine grasslands. We fitted statistical models with high spectral and spatial resolution reflectance data and tested four optical indices sensitive to leaf chlorophyll content, leaf water content and leaf area index. We found moderate added-value of AIS data for predicting alpine plant species distribution. Contrary to expectations, differences between species distribution models (SDMs) were not linked to their local abundance or phylogenetic/functional similarity. Moreover, spectral signatures of species were found to be partly site-specific. We discuss current limits of AIS-based SDMs, highlighting issues of scale and informational content of AIS data.

Long-term modeling of the forest-grassland ecotone in the French Alps: implications for land management and conservation.

Understanding decadal-scale land-cover changes has the potential to inform current conservation policies. European mountain landscapes that include numerous protected areas provide a unique opportunity to weigh the long-term influences of land-use practices and climate on forest-grassland ecotone dynamics. Aerial photographs from four dates (1948, 1978, 1993, and 2009) were used to quantify the extent of forest and grassland cover at 5-m resolution across a 150-km2 area in a protected area of the southwestern French Alps. The study area included a grazed zone and a nongrazed zone that was abandoned during the 1970s. We estimated time series of a forestation index (FI) and analyzed the effects of elevation and grazing on FI using a hierarchical linear mixed effect model. Forest extent (composed primarily of mountain pine, Pinus uncinata) expanded from 50.6 km2 in 1948 to 85.5 km2 in 2009, i.e., a 23% increase in relative cover at the expense of grassland communities. Over the sixty-year period, the treeline rose by 118 m, from 1564 to 1682 m. Rapid forest expansion within the nongrazed zone followed the cessation of logging activities and was likely accelerated by climate warming during the 1980s. Within the grazed zone, the maintained presence of sheep did not fully counteract mountain pine expansion and led to highly contrasting rates of land-cover change based on the location of shepherds' cabins and water sources. Projections of FI for 2030 showed remnant patches of intensively used grasslands interspersed in a densely forested matrix. Our analysis of mountain land-cover dynamics provided strong evidence for forest encroachment into grassland habitat despite consistent grazing pressure. This pattern may be attributed to the disappearance of traditional land-use practices such as shrub burning and removal. Our findings prompt land managers to reconsider their initial conservation priority (i.e., the protection of a renowned mountain pine forest) and to implement proactive management strategies in order to preserve landscape heterogeneity and biological diversity. Projecting historical trends in the forest-grassland ecotone to 2030 provides stakeholders with a policy relevant tool for near-term land management.

Combining the fourth-corner and the RLQ methods for assessing trait responses to environmental variation.

Assessing trait responses to environmental gradients requires the simultaneous analysis of the information contained in three tables: L (species distribution across samples), R (environmental characteristics of samples), and Q (species traits). Among the available methods, the so-called fourth-corner and RLQ methods are two appealing alternatives that provide a direct way to test and estimate trait-nvironment relationships. Both methods are based on the analysis of the fourth-corner matrix, which crosses traits and environmental variables weighted by species abundances. However, they differ greatly in their outputs: RLQ is a multivariate technique that provides ordination scores to summarize the joint structure among the three tables, whereas the fourth-corner method mainly tests for individual trait-environment relationships (i.e., one trait and one environmental variable at a time). Here, we illustrate how the complementarity between these two methods can be exploited to promote new ecological knowledge and to improve the study of trait-environment relationships. After a short description of each method, we apply them to real ecological data to present their different outputs and provide hints about the gain resulting from their combined use.

Long livestock farming history and human landscape shaping revealed by lake sediment DNA.

The reconstruction of human-driven, Earth-shaping dynamics is important for understanding past human/environment interactions and for helping human societies that currently face global changes. However, it is often challenging to distinguish the effects of the climate from human activities on environmental changes. Here we evaluate an approach based on DNA metabarcoding used on lake sediments to provide the first high-resolution reconstruction of plant cover and livestock farming history since the Neolithic Period. By comparing these data with a previous reconstruction of erosive event frequency, we show that the most intense erosion period was caused by deforestation and overgrazing by sheep and cowherds during the Late Iron Age and Roman Period. Tracking plants and domestic mammals using lake sediment DNA (lake sedDNA) is a new, promising method for tracing past human practices, and it provides a new outlook of the effects of anthropogenic factors on landscape-scale changes.

Working toward integrated models of alpine plant distribution.

Species distribution models (SDMs) have been frequently employed to forecast the response of alpine plants to global changes. Efforts to model alpine plant distribution have thus far been primarily based on a correlative approach, in which ecological processes are implicitly addressed through a statistical relationship between observed species occurrences and environmental predictors. Recent evidence, however, highlights the shortcomings of correlative SDMs, especially in alpine landscapes where plant species tend to be decoupled from atmospheric conditions in micro-topographic habitats and are particularly exposed to geomorphic disturbances. While alpine plants respond to the same limiting factors as plants found at lower elevations, alpine environments impose a particular set of scale-dependent and hierarchical drivers that shape the realized niche of species and that require explicit consideration in a modelling context. Several recent studies in the European Alps have successfully integrated both correlative and process-based elements into distribution models of alpine plants, but for the time being a single integrative modelling framework that includes all key drivers remains elusive. As a first step in working toward a comprehensive integrated model applicable to alpine plant communities, we propose a conceptual framework that structures the primary mechanisms affecting alpine plant distributions. We group processes into four categories, including multi-scalar abiotic drivers, gradient dependent species interactions, dispersal and spatial-temporal plant responses to disturbance. Finally, we propose a methodological framework aimed at developing an integrated model to better predict alpine plant distribution.

Genetic diversity in widespread species is not congruent with species richness in alpine plant communities.

The Convention on Biological Diversity (CBD) aims at the conservation of all three levels of biodiversity, that is, ecosystems, species and genes. Genetic diversity represents evolutionary potential and is important for ecosystem functioning. Unfortunately, genetic diversity in natural populations is hardly considered in conservation strategies because it is difficult to measure and has been hypothesised to co-vary with species richness. This means that species richness is taken as a surrogate of genetic diversity in conservation planning, though their relationship has not been properly evaluated. We tested whether the genetic and species levels of biodiversity co-vary, using a large-scale and multi-species approach. We chose the high-mountain flora of the Alps and the Carpathians as study systems and demonstrate that species richness and genetic diversity are not correlated. Species richness thus cannot act as a surrogate for genetic diversity. Our results have important consequences for implementing the CBD when designing conservation strategies.

Relationship between reproductive allocation and relative abundance among 32 species of a Tibetan alpine meadow: effects of fertilization and grazing.

BACKGROUND: Understanding the relationship between species traits and species abundance is an important goal in ecology and biodiversity science. Although theoretical studies predict that traits related to performance (e.g. reproductive allocation) are most directly linked to species abundance within a community, empirical investigations have rarely been done. It also remains unclear how environmental factors such as grazing or fertilizer application affect the predicted relationship. METHODOLOGY: We conducted a 3-year field experiment in a Tibetan alpine meadow to assess the relationship between plant reproductive allocation (RA) and species relative abundance (SRA) on control, grazed and fertilized plots. Overall, the studied plant community contained 32 common species. PRINCIPAL FINDINGS: At the treatment level, (i) RA was negatively correlated with SRA on control plots and during the first year on fertilized plots. (ii) No negative RA-SRA correlations were observed on grazed plots and during the second and third year on fertilized plots. (iii) Seed size was positively correlated with SRA on control plots. At the plot level, the correlation between SRA and RA were not affected by treatment, year or species composition. CONCLUSIONS/SIGNIFICANCE: Our study shows that the performance-related trait RA can negatively affect SRA within communities, which is possibly due to the tradeoffs between clonal growth (for space occupancy) and sexual reproduction. We propose that if different species occupy different positions along these tradeoffs it will contribute to biodiversity maintenance in local communities or even at lager scale.

Soil sampling and isolation of extracellular DNA from large amount of starting material suitable for metabarcoding studies.

DNA metabarcoding refers to the DNA-based identification of multiple species from a single complex and degraded environmental sample. We developed new sampling and extraction protocols suitable for DNA metabarcoding analyses targeting soil extracellular DNA. The proposed sampling protocol has been designed to reduce, as much as possible, the influence of local heterogeneity by processing a large amount of soil resulting from the mixing of many different cores. The DNA extraction is based on the use of saturated phosphate buffer. The sampling and extraction protocols were validated first by analysing plant DNA from a set of 12 plots corresponding to four plant communities in alpine meadows, and, second, by conducting pilot experiments on fungi and earthworms. The results of the validation experiments clearly demonstrated that sound biological information can be retrieved when following these sampling and extraction procedures. Such a protocol can be implemented at any time of the year without any preliminary knowledge of specific types of organisms during the sampling. It offers the opportunity to analyse all groups of organisms using a single sampling/extraction procedure and opens the possibility to fully standardize biodiversity surveys.