Pollinator movement activity influences genetic diversity and differentiation of spatially isolated populations of clonal forest herbs

In agricultural landscapes, forest herbs live in small, spatially isolated forest patches. For their long-term survival, their populations depend on animals as genetic linkers that provide pollen- or seed-mediated gene flow among different forest patches. However, whether insect pollinators serve as genetic linkers among spatially isolated forest herb populations in agricultural landscapes remains to be shown. Here, we used population genetic methods to analyze: (A) the genetic diversity and genetic differentiation of populations of two common, slow-colonizing temperate forest herb species [Polygonatum multiflorum (L.) All. and Anemone nemorosa L.] in spatially isolated populations within three agricultural landscapes in Germany and Sweden and (B) the movement activity of their most relevant associated pollinator species, i.e., the bumblebee Bombus pascuorum (Scopoli, 1,763) and the hoverfly Melanostoma scalare (Fabricus, 1,794), respectively, which differ in their mobility. We tested whether the indicated pollinator movement activity affected the genetic diversity and genetic differentiation of the forest herb populations. Bumblebee movement indicators that solely indicated movement activity between the forest patches affected both genetic diversity and genetic differentiation of the associated forest herb P. multiflorum in a way that can be explained by pollen-mediated gene flow among the forest herb populations. In contrast, movement indicators reflecting the total movement activity at a forest patch (including within-forest patch movement activity) showed unexpected effects for both plant-pollinator pairs that might be explained by accelerated genetic drift due to enhanced sexual reproduction. Our integrated approach revealed that bumblebees serve as genetic linkers of associated forest herb populations, even if they are more than 2 km apart from each other. No such evidence was found for the forest associated hoverfly species which showed significant genetic differentiation among forest patches itself. Our approach also indicated that a higher within-forest patch movement activity of both pollinator species might enhance sexual recruitment and thus diminishes the temporal buffer that clonal growth provides against habitat fragmentation effects

Hedging against biodiversity loss : forest herbs’ performance in hedgerows across temperate Europe

Questions: How do contrasting environmental conditions among forests and hedgerows affect the vegetative and reproductive performance of understorey forest herbs in both habitats? Can hedgerows support reproductive source populations of forest herbs, thus potentially allowing progressive dispersal of successive generations along these linear habitats? Location: Hedgerows and deciduous forest patches in agricultural landscapes across the European temperate biome. Methods: First, we assessed differences in environmental conditions among forests and hedgerows. Next, we quantified plant performance based on a set of functional life‐history traits for four forest herbs (Anemone nemorosa, Ficaria verna, Geum urbanum, Poa nemoralis) with contrasting flowering phenology and colonisation capacity in paired combinations of forests and hedgerows, and compared these traits among both habitats. Finally, we assessed relationships between plant performance and environmental conditions in both habitats. Results: All study species showed a higher above‐ground biomass in hedgerows than in forests. For Poa nemoralis and Geum urbanum, we also found a higher reproductive output in hedgerows, which was mainly correlated to the higher sub‐canopy temperatures therein. The “ancient forest herb” Anemone nemorosa, however, appeared to have a lower reproductive output in hedgerows than in forests, while for Ficaria verna no reproductive differences were found between the two habitats. Conclusions: This is the first study on such a broad geographical scale to provide evidence of reproductive source populations of forest herbs in hedgerows. Our findings provide key information on strategies by which forest plants grow, reproduce and disperse in hedgerow environments, which is imperative to better understand the dispersal corridor function of these wooded linear structures. Finally, we highlight the urgent need to develop guidelines for preserving, managing and establishing hedgerows in intensive agricultural landscapes, given their potential to contribute to the long‐term conservation and migration of forest herbs in the face of global environmental change

Sensitivity to habitat fragmentation across European landscapes in three temperate forest herbs

Context Evidence for effects of habitat loss and fragmentation on the viability of temperate forest herb populations in agricultural landscapes is so far based on population genetic studies of single species in single landscapes. However, forest herbs differ in their life histories, and landscapes have different environments, structures and histories, making generalizations difficult. Objectives We compare the response of three slow-colonizing forest herbs to habitat loss and fragmentation and set this in relation to differences in life-history traits, in particular their mating system and associated pollinators. Methods We analysed the herbs' landscape-scale population genetic structure based on microsatellite markers from replicate forest fragments across seven European agricultural landscapes. Results All species responded to reductions in population size with a decrease in allelic richness and an increase in genetic differentiation among populations. Genetic differentiation also increased with enhanced spatial isolation. In addition, each species showed unique responses. Heterozygosity in the self-compatible Oxalis acetosella was reduced in smaller populations. The genetic diversity of Anemone nemorosa, whose main pollinators are less mobile, decreased with increasing spatial isolation, but not that of the bumblebee-pollinated Polygonatum multiflorum. Conclusions Our study indicates that habitat loss and fragmentation compromise the long-term viability of slow-colonizing forest herbs despite their ability to persist for many decades by clonal propagation. The distinct responses of the three species studied within the same landscapes confirm the need of multi-species approaches. The mobility of associated pollinators should be considered an important determinant of forest herbs' sensitivity to habitat loss and fragmentation

High ecosystem service delivery potential of small woodlands in agricultural landscapes

Global forest loss and fragmentation have strongly increased the frequency of forest patches smaller than a few hectares. Little is known about the biodiversity and ecosystem service supply potential of such small woodlands in comparison to larger forests. As it is widely recognized that high biodiversity levels increase ecosystem functionality and the delivery of multiple ecosystem services, small, isolated woodlands are expected to have a lower potential for ecosystem service delivery than large forests hosting more species. We collected data on the diversity of six taxonomic groups covering invertebrates, plants and fungi, and on the supply potential of five ecosystem services and one disservice within 224 woodlands distributed across temperate Europe. We related their ability to simultaneously provide multiple ecosystem services (multiservice delivery potential) at different performance levels to biodiversity of all studied taxonomic groups (multidiversity), forest patch size and age, as well as habitat availability and connectivity within the landscape, while accounting for macroclimate, soil properties and forest structure. Unexpectedly, despite their lower multidiversity, smaller woodlands had the potential to deliver multiple services at higher performance levels per area than larger woodlands of similar age, probably due to positive edge effects on the supply potential of several ecosystem services. Biodiversity only affected multiservice delivery potential at a low performance level as well as some individual ecosystem services. The importance of other drivers of ecosystem service supply potential by small woodlands in agricultural landscapes also depended on the level of performance and varied with the individual ecosystem service considered. Synthesis and applications. Large, ancient woodlands host high levels of biodiversity and can therefore deliver a number of ecosystem services. In contrast, smaller woodlands in agricultural landscapes, especially ancient woodlands, have a higher potential to deliver multiple ecosystem services on a per area basis. Despite their important contribution to agricultural landscape multifunctionality, small woodlands are not currently considered by public policies. There is thus an urgent need for targeted policy instruments to ensure their adequate management and future conservation in order to either achieve multiservice delivery at high levels or to maximize the delivery of specific ecosystem services

High ecosystem service delivery potential of small woodlands in agricultural landscapes

Global forest loss and fragmentation have strongly increased the frequency of forest patches smaller than a few hectares. Little is known about the biodiversity and ecosystem service supply potential of such small woodlands in comparison to larger forests. As it is widely recognized that high biodiversity levels increase ecosystem functionality and the delivery of multiple ecosystem services, small, isolated woodlands are expected to have a lower potential for ecosystem service delivery than large forests hosting more species. We collected data on the diversity of six taxonomic groups covering invertebrates, plants and fungi, and on the supply potential of five ecosystem services and one disservice within 224 woodlands distributed across temperate Europe. We related their ability to simultaneously provide multiple ecosystem services (multiservice delivery potential) at different performance levels to biodiversity of all studied taxonomic groups (multidiversity), forest patch size and age, as well as habitat availability and connectivity within the landscape, while accounting for macroclimate, soil properties and forest structure. Unexpectedly, despite their lower multidiversity, smaller woodlands had the potential to deliver multiple services at higher performance levels per area than larger woodlands of similar age, probably due to positive edge effects on the supply potential of several ecosystem services. Biodiversity only affected multiservice delivery potential at a low performance level as well as some individual ecosystem services. The importance of other drivers of ecosystem service supply potential by small woodlands in agricultural landscapes also depended on the level of performance and varied with the individual ecosystem service considered. Synthesis and applications. Large, ancient woodlands host high levels of biodiversity and can therefore deliver a number of ecosystem services. In contrast, smaller woodlands in agricultural landscapes, especially ancient woodlands, have a higher potential to deliver multiple ecosystem services on a per area basis. Despite their important contribution to agricultural landscape multifunctionality, small woodlands are not currently considered by public policies. There is thus an urgent need for targeted policy instruments to ensure their adequate management and future conservation in order to either achieve multiservice delivery at high levels or to maximize the delivery of specific ecosystem services

Responses of competitive understorey species to spatial environmental gradients inaccurately explain temporal changes

Understorey plant communities play a key role in the functioning of forest ecosystems. Under favourable environmental conditions, competitive understorey species may develop high abundances and influence important ecosystem processes such as tree regeneration. Thus, understanding and predicting the response of competitive understorey species as a function of changing environmental conditions is important for forest managers. In the absence of sufficient temporal data to quantify actual vegetation changes, space-for-time (SFT) substitution is often used, i.e. studies that use environmental gradients across space to infer vegetation responses to environmental change over time. Here we assess the validity of such SFT approaches and analysed 36 resurvey studies from ancient forests with low levels of recent disturbances across temperate Europe to assess how six competitive understorey plant species respond to gradients of overstorey cover, soil conditions, atmospheric N deposition and climatic conditions over space and time. The combination of historical and contemporary surveys allows (i) to test if observed contemporary patterns across space are consistent at the time of the historical survey, and, crucially, (ii) to assess whether changes in abundance over time given recorded environmental change match expectations from patterns recorded along environmental gradients in space. We found consistent spatial relationships at the two periods: local variation in soil variables and overstorey cover were the best predictors of individual species’ cover while interregional variation in coarse-scale variables, i.e. N deposition and climate, was less important. However, we found that our SFT approach could not accurately explain the large variation in abundance changes over time. We thus recommend to be cautious when using SFT substitution to infer species responses to temporal changes.</p

Forest microclimate dynamics drive plant responses to warming

Climate warming is causing a shift in biological communities in favor of warm-affinity species (i.e., thermophilization). Species responses often lag behind climate warming, but the reasons for such lags remain largely unknown. Here, we analyzed multidecadal understory microclimate dynamics in European forests and show that thermophilization and the climatic lag in forest plant communities are primarily controlled by microclimate. Increasing tree canopy cover reduces warming rates inside forests, but loss of canopy cover leads to increased local heat that exacerbates the disequilibrium between community responses and climate change. Reciprocal effects between plants and microclimates are key to understanding the response of forest biodiversity and functioning to climate and land-use changes

Combining biodiversity resurveys across regions to advance global change research

More and more ecologists have started to resurvey communities sampled in earlier decades to determine long-term shifts in community composition and infer the likely drivers of the ecological changes observed. However, to assess the relative importance of and interactions among multiple drivers, joint analyses of resurvey data from many regions spanning large environmental gradients are needed. In this article, we illustrate how combining resurvey data from multiple regions can increase the likelihood of driver orthogonality within the design and show that repeatedly surveying across multiple regions provides higher representativeness and comprehensiveness, allowing us to answer more completely a broader range of questions. We provide general guidelines to aid the implementation of multiregion resurvey databases. In so doing, we aim to encourage resurvey database development across other community types and biomes to advance global environmental change research

Replacements of small- by large-ranged species scale up to diversity loss in Europe’s temperate forest biome

The loss of biodiversity at the global scale has been difficult to reconcile with observations of no net loss at local scales. Vegetation surveys across European temperate forests show that this may be explained by the replacement of small-ranged species with large-ranged ones, driven by nitrogen deposition. Biodiversity time series reveal global losses and accelerated redistributions of species, but no net loss in local species richness. To better understand how these patterns are linked, we quantify how individual species trajectories scale up to diversity changes using data from 68 vegetation resurvey studies of seminatural forests in Europe. Herb-layer species with small geographic ranges are being replaced by more widely distributed species, and our results suggest that this is due less to species abundances than to species nitrogen niches. Nitrogen deposition accelerates the extinctions of small-ranged, nitrogen-efficient plants and colonization by broadly distributed, nitrogen-demanding plants (including non-natives). Despite no net change in species richness at the spatial scale of a study site, the losses of small-ranged species reduce biome-scale (gamma) diversity. These results provide one mechanism to explain the directional replacement of small-ranged species within sites and thus explain patterns of biodiversity change across spatial scales

Observer and relocation errors matter in resurveys of historical vegetation plots

Aim: Revisits of non-permanent, relocatable plots first surveyed several decades ago offer a direct way to observe vegetation change and form a unique and increasingly used source of information for global change research. Despite the important insights that can be obtained from resurveying these quasi-permanent vegetation plots, their use is prone to both observer and relocation errors. Studying the combined effects of both error types is important since they will play out together in practice and it is yet unknown to what extent observed vegetation changes are influenced by these errors. Methods: We designed a study that mimicked all steps in a resurvey study and that allowed determination of the magnitude of observer errors only vs the joint observer and relocation errors. Communities of vascular plants growing in the understorey of temperate forests were selected as study system. Ten regions in Europe were covered to explore generality across contexts and 50 observers were involved, which deliberately differed in their experience in making vegetation records. Results: The mean geographic distance between plots in the observer+relocation error data set was 24m. The mean relative difference in species richness in the observer error and the observer+relocation data set was 15% and 21%, respectively. The mean pseudo-turnover between the five records at a quasi-permanent plot location was on average 0.21 and 0.35 for the observer error and observer+relocation error data sets, respectively. More detailed analyses of the compositional variation showed that the nestedness and turnover components were of equal importance in the observer data set, whereas turnover was much more important than nestedness in the observer+relocation data set. Interestingly, the differences between the observer and the observer+relocation data sets largely disappeared when looking at temporal change: both the changes in species richness and species composition over time were very similar in these data sets. Conclusions: Our results demonstrate that observer and relocation errors are non-negligible when resurveying quasi-permanent plots. A careful interpretation of the results of resurvey studies is warranted, especially when changes are assessed based on a low number of plots. We conclude by listing measures that should be taken to maximally increase the precision and the strength of the inferences drawn from vegetation resurveys