Long-term shift towards shady and nutrient-rich habitats in Central European temperate forests.

Biodiversity world-wide has been under increasing anthropogenic pressure in the past century. The long-term response of biotic communities has been tackled primarily by focusing on species richness, community composition and functionality. Equally important are shifts between entire communities and habitat types, which remain an unexplored level of biodiversity change. We have resurveyed > 2000 vegetation plots in temperate forests in central Europe to capture changes over an average of five decades. The plots were assigned to eight broad forest habitat types using an algorithmic classification system. We analysed transitions between the habitat types and interpreted the trend in terms of changes in environmental conditions. We identified a directional shift along the combined gradients of canopy openness and soil nutrients. Nutrient-poor open-canopy forest habitats have declined strongly in favour of fertile closed-canopy habitats. However, the shift was not uniform across the whole gradients. We conclude that the shifts in habitat types represent a century-long successional trend with significant consequences for forest biodiversity. Open forest habitats should be urgently targeted for plant diversity restoration through the implementation of active management. The approach presented here can be applied to other habitat types and at different spatio-temporal scales.

Evaluating plant lineage losses and gains in temperate forest understories: a phylogenetic perspective on climate change and nitrogen deposition.

Global change has accelerated local species extinctions and colonizations, often resulting in losses and gains of evolutionary lineages with unique features. Do these losses and gains occur randomly across the phylogeny? We quantified: temporal changes in plant phylogenetic diversity (PD); and the phylogenetic relatedness (PR) of lost and gained species in 2672 semi-permanent vegetation plots in European temperate forest understories resurveyed over an average period of 40 yr. Controlling for differences in species richness, PD increased slightly over time and across plots. Moreover, lost species within plots exhibited a higher degree of PR than gained species. This implies that gained species originated from a more diverse set of evolutionary lineages than lost species. Certain lineages also lost and gained more species than expected by chance, with Ericaceae, Fabaceae, and Orchidaceae experiencing losses and Amaranthaceae, Cyperaceae, and Rosaceae showing gains. Species losses and gains displayed no significant phylogenetic signal in response to changes in macroclimatic conditions and nitrogen deposition. As anthropogenic global change intensifies, temperate forest understories experience losses and gains in specific phylogenetic branches and ecological strategies, while the overall mean PD remains relatively stable.

Les changements globaux accélèrent les processus de colonisation et d'extinction locales d'espèces, aboutissant à des gains ou à des pertes de lignées évolutives uniques. Ces gains et pertes se produisent-ils de manière aléatoire dans l'arbre phylogénétique ? Nous avons mesuré: les changements de diversité phylogénétique; et la parenté phylogénétique des espèces végétales gagnées ou perdues dans 2672 placettes semi-permanentes disposées dans le sous-bois de forêts tempérées d'Europe sur une période moyenne de 40 ans. Une fois corrigée par la richesse spécifique, la diversité phylogénétique a légèrement augmenté au cours du temps dans les différentes placettes. Les espèces perdues ont une plus grande parenté phylogénétique que les espèces gagnées. Les espèces gagnées sont donc issues d'un plus grand nombre de lignées évolutives que les espèces perdues. Certaines lignées ont gagné ou perdu davantage d'espèces que ce qui est prédit par le hasard : les Ericaceae, les Fabaceae et les Orchidaceae ayant davantage perdu, tandis que les Amaranthaceae, les Cyperaceae, et les Rosaceae ont plus gagné. Il n'y a pas de signal phylogénétique des gains ou pertes d'espèces en réponse aux changements de conditions macroclimatiques ou des dépôts atmosphériques d'azote. Alors que les changements globaux d'origine anthropique s'intensifient, les sous-bois des forêts tempérées connaissent des gains et des pertes de certaines lignées évolutives et de certaines stratégies écologiques, sans que la diversité phylogénétique moyenne ne s'en trouve véritablement affectée.

El cambio global ha acelerado las extinciones y colonizaciones a escala local, lo que a menudo ha supuesto pérdidas y ganancias de linajes evolutivos con características únicas. Ahora bien, ¿estas pérdidas y ganancias ocurren aleatoriamente a lo largo de la filogenia? Cuantificamos: los cambios temporales en la diversidad filogenética de las plantas; y la relación filogenética de las especies perdidas y ganadas en 2.672 parcelas de vegetación semipermanente en sotobosques templados europeos y re-muestreadas durante un período promedio de 40 años. Al controlar por las diferencias en la riqueza de especies, la diversidad filogenética aumentó ligeramente con el tiempo y entre parcelas. Además, las especies perdidas dentro de las parcelas exhibieron un mayor grado de relación filogenética que las especies ganadas. Esto implica que las especies ganadas se originaron en un conjunto de linajes evolutivos más diversos que las especies perdidas. Ciertos linajes también perdieron y ganaron más especies de las esperadas aleatoriamente: Ericaceae, Fabaceae y Orchidaceae experimentaron pérdidas y Amaranthaceae, Cyperaceae y Rosaceae mostraron ganancias. Las pérdidas y ganancias de especies no mostraron ninguna señal filogenética significativa en respuesta a los cambios en las condiciones macro-climáticas y la deposición de nitrógeno. A medida que se intensifica el cambio global antropogénico, los sotobosques temperados experimentan pérdidas y ganancias en ramas filogenéticas y estrategias ecológicas específicas, mientras que la diversidad filogenética media general permanece relativamente estable.

Combining multiple investigative approaches to unravel functional responses to global change in the understorey of temperate forests.

Plant communities are being exposed to changing environmental conditions all around the globe, leading to alterations in plant diversity, community composition, and ecosystem functioning. For herbaceous understorey communities in temperate forests, responses to global change are postulated to be complex, due to the presence of a tree layer that modulates understorey responses to external pressures such as climate change and changes in atmospheric nitrogen deposition rates. Multiple investigative approaches have been put forward as tools to detect, quantify and predict understorey responses to these global-change drivers, including, among others, distributed resurvey studies and manipulative experiments. These investigative approaches are generally designed and reported upon in isolation, while integration across investigative approaches is rarely considered. In this study, we integrate three investigative approaches (two complementary resurvey approaches and one experimental approach) to investigate how climate warming and changes in nitrogen deposition affect the functional composition of the understorey and how functional responses in the understorey are modulated by canopy disturbance, that is, changes in overstorey canopy openness over time. Our resurvey data reveal that most changes in understorey functional characteristics represent responses to changes in canopy openness with shifts in macroclimate temperature and aerial nitrogen deposition playing secondary roles. Contrary to expectations, we found little evidence that these drivers interact. In addition, experimental findings deviated from the observational findings, suggesting that the forces driving understorey change at the regional scale differ from those driving change at the forest floor (i.e., the experimental treatments). Our study demonstrates that different approaches need to be integrated to acquire a full picture of how understorey communities respond to global change.

Global environmental change effects on plant community composition trajectories depend upon management legacies.

The contemporary state of functional traits and species richness in plant communities depends on legacy effects of past disturbances. Whether temporal responses of community properties to current environmental changes are altered by such legacies is, however, unknown. We expect global environmental changes to interact with land-use legacies given different community trajectories initiated by prior management, and subsequent responses to altered resources and conditions. We tested this expectation for species richness and functional traits using 1814 survey-resurvey plot pairs of understorey communities from 40 European temperate forest datasets, syntheses of management transitions since the year 1800, and a trait database. We also examined how plant community indicators of resources and conditions changed in response to management legacies and environmental change. Community trajectories were clearly influenced by interactions between management legacies from over 200 years ago and environmental change. Importantly, higher rates of nitrogen deposition led to increased species richness and plant height in forests managed less intensively in 1800 (i.e., high forests), and to decreases in forests with a more intensive historical management in 1800 (i.e., coppiced forests). There was evidence that these declines in community variables in formerly coppiced forests were ameliorated by increased rates of temperature change between surveys. Responses were generally apparent regardless of sites' contemporary management classifications, although sometimes the management transition itself, rather than historic or contemporary management types, better explained understorey responses. Main effects of environmental change were rare, although higher rates of precipitation change increased plant height, accompanied by increases in fertility indicator values. Analysis of indicator values suggested the importance of directly characterising resources and conditions to better understand legacy and environmental change effects. Accounting for legacies of past disturbance can reconcile contradictory literature results and appears crucial to anticipating future responses to global environmental change.

Habitat requirements of endangered species in a former coppice of high conservation value.

Transformation of coppices to high forests has caused fundamental changes in site conditions and a decline of many species across Central Europe. Nevertheless, some formerly coppiced forests still harbour a number of the declining species and have become biodiversity hotspots in the changing landscape. We focused on the best preserved remnant of formerly grazed and coppiced subcontinental oak forest in the Czech Republic - Dúbrava forest near Hodonín. To improve our understanding of the ecology of the declining species, we studied local habitat requirements of vascular plants most endangered at the national level. We recorded vegetation composition and sampled important site variables in plots with the largest populations of endangered species and in additional plots placed randomly across all major forest habitats. We demonstrated that sites with endangered species have a highly uneven distribution in ecological space and their species composition is often similar to open-canopy oak forests. Within this habitat, the endangered species are concentrated in places with a high light availability and high soil pH. Light-demanding species characteristic of subcontinental oak forests are the best indicators of these sites, while broadly distributed shade-tolerant and nutrient-demanding species avoid them. These results support the view that the occurrence of many endangered species in Dúbrava forest is a legacy of the long history of traditional management that kept the canopies open. The light-demanding species are now threatened by ongoing successional changes. Therefore, active conservation measures are recommended, including opening up the canopies, early thinning of young stands, control of expansive and invasive species and understorey grazing or mowing.

The paradox of long-term ungulate impact: increase of plant species richness in a temperate forest.

QUESTIONS: Did high densities of wild ungulates cause a decline in plant species richness in a temperate oakwood? How did species composition change after nearly five decades? Did ungulates facilitate the spread of ruderal species and supress endangered species? Did dispersal strategies play a role in these processes? LOCATION: Krumlov Wood, SE Czech Republic. METHODS: In 2012, we resampled 58 quasi-permanent vegetation plots first surveyed in 1960s. Between the surveys, 36 plots were enclosed in a game preserve with artificially high density of ungulates (mostly deer, mouflon and wild boar; ca. 55 animals per square km). We analysed the differences in temporal changes between plots inside and outside the game preserve, focusing on species diversity and composition. We assessed species characteristics relevant to grazing to understand compositional changes. RESULTS: Ungulates significantly increased alpha and gamma diversity and caused significant vegetation homogenization inside the game preserve. Vegetation homogenization and the increase in species richness resulted from massive enrichment by ruderal species. However, richness of endangered species decreased. Species dispersed by animals internally (endozoochory) increased, while species dispersed externally (epizoochory) or by wind (anemochory) decreased. CONCLUSIONS: Contrary to our expectations, our long-term data showed that artificially high ungulate densities substantially increased plant species richness. Apparently, the establishment of ruderal herbs was supported by frequent disturbances and ungulate-mediated dispersal. At the same time, species richness of non-ruderal plants did not change, probably because ungulates hindered the regeneration of woody species and maintained an open forest canopy. In conclusion, high ungulate density led to the spread of ruderal species, which in turn strongly contributed to the observed shift towards nutrient-richer conditions and taxonomically more homogenous communities.

Combining community resurvey data 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 paper 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 implementation of multi-region resurvey databases. In so doing, we aim to encourage resurvey database development across other community types and biomes to advance global environmental change research.

Drivers of temporal changes in temperate forest plant diversity vary across spatial scales.

Global biodiversity is affected by numerous environmental drivers. Yet, the extent to which global environmental changes contribute to changes in local diversity is poorly understood. We investigated biodiversity changes in a meta-analysis of 39 resurvey studies in European temperate forests (3988 vegetation records in total, 17-75 years between the two surveys) by assessing the importance of (i) coarse-resolution (i.e., among sites) vs. fine-resolution (i.e., within sites) environmental differences and (ii) changing environmental conditions between surveys. Our results clarify the mechanisms underlying the direction and magnitude of local-scale biodiversity changes. While not detecting any net local diversity loss, we observed considerable among-site variation, partly explained by temporal changes in light availability (a local driver) and density of large herbivores (a regional driver). Furthermore, strong evidence was found that presurvey levels of nitrogen deposition determined subsequent diversity changes. We conclude that models forecasting future biodiversity changes should consider coarse-resolution environmental changes, account for differences in baseline environmental conditions and for local changes in fine-resolution environmental conditions.

Effects of simulated historical tree litter raking on the understorey vegetation in a central European forest.

QUESTION: What is the impact of simulated historical tree litter removal on understorey plants and soil properties in a temperate deciduous forest? What is the role of seasonal timing of tree litter removal on understorey plants? LOCATION: Podyjí National Park, Czech Republic. METHODS: We conducted an experiment in a randomized complete block design of 45 plots (5 × 5 m). Each block (N = 15) consisted of one plot for each of the three treatments. Treatments consisted of (i) tree litter removal during spring, (ii) tree litter removal during autumn, or (iii) no litter removal as control treatment. These treatments were repeated for a duration of four years. In each plot we recorded the understorey plant species composition and collected soil samples prior to treatment (year 0) and in each subsequent year (years 1-4). Temporal trends in species richness were analysed using repeated measures ANOVAs. The impact of the treatments on vegetation composition over time was analysed using Principal Response Curves. RESULTS: Total species richness per plot significantly changed over time, but this was not related to treatment. Annual species richness increased significantly, but only for the autumn treatment. Annual species also showed the highest inter-annual variation. Endangered species were not affected. When compared to the control treatment, the effect of autumn raking on species composition was stronger than the effect of spring raking. Although the amount of removed nutrients substantially exceeded ambient nitrogen input, no changes in soil conditions were detected. CONCLUSIONS: The season in which tree litter removal took place had a small but significant impact on the understorey vegetation, in particular affecting the germination and establishment of annual species. The large inter-annual variation in species richness calls for a long-term field experiment. The removal of nutrients via litter raking greatly exceeds atmospheric nutrient deposition, warranting a further investigation of litter raking as a potential tool for forest conservation.

Long-term nitrogen deposition reduces the diversity of nitrogen-fixing plants.

Biological nitrogen fixation is a fundamental part of ecosystem functioning. Anthropogenic nitrogen deposition and climate change may, however, limit the competitive advantage of nitrogen-fixing plants, leading to reduced relative diversity of nitrogen-fixing plants. Yet, assessments of changes of nitrogen-fixing plant long-term community diversity are rare. Here, we examine temporal trends in the diversity of nitrogen-fixing plants and their relationships with anthropogenic nitrogen deposition while accounting for changes in temperature and aridity. We used forest-floor vegetation resurveys of temperate forests in Europe and the United States spanning multiple decades. Nitrogen-fixer richness declined as nitrogen deposition increased over time but did not respond to changes in climate. Phylogenetic diversity also declined, as distinct lineages of N-fixers were lost between surveys, but the "winners" and "losers" among nitrogen-fixing lineages varied among study sites, suggesting that losses are context dependent. Anthropogenic nitrogen deposition reduces nitrogen-fixing plant diversity in ways that may strongly affect natural nitrogen fixation.

Unexpected westward range shifts in European forest plants link to nitrogen deposition.

Climate change is commonly assumed to induce species' range shifts toward the poles. Yet, other environmental changes may affect the geographical distribution of species in unexpected ways. Here, we quantify multidecadal shifts in the distribution of European forest plants and link these shifts to key drivers of forest biodiversity change: climate change, atmospheric deposition (nitrogen and sulfur), and forest canopy dynamics. Surprisingly, westward distribution shifts were 2.6 times more likely than northward ones. Not climate change, but nitrogen-mediated colonization events, possibly facilitated by the recovery from past acidifying deposition, best explain westward movements. Biodiversity redistribution patterns appear complex and are more likely driven by the interplay among several environmental changes than due to the exclusive effects of climate change alone.

Experimental restoration of coppice-with-standards: Response of understorey vegetation from the conservation perspective.

A substantial part of European lowland woodlands was managed as coppices or wood pastures for millennia. However, traditional management forms were almost completely abandoned in Central Europe by the middle of the 20th century. Combined with the effects of nitrogen deposition and herbivore pressure, shifts in management resulted in biodiversity loss affecting particularly light-demanding oligotrophic plant species. Experimental thinning was applied in a former oak coppice-with-standards in an attempt to restore vanishing understorey plant communities. Two levels of thinning intensity and zero management as control were used on 90 plots. Ten years after the treatment, significant changes in species composition and diversity were observed in heavily thinned plots, while moderate thinning had mostly insignificant effects. Light-demanding oligotrophic species significantly increased, indicating positive consequences of restoration. However, heavy thinning also brought about the expansion of native ruderal species. Alien species remained unchanged. We conclude that the restoration of coppice-with-standards can be an efficient tool to support vanishing light-demanding woodland species. Combined with biodiversity benefits, the increasing demand for biofuel may contribute to the renaissance of traditional management forms in forestry.

Spatial scaling of pollen-plant diversity relationship in landscapes with contrasting diversity patterns.

Mitigating the effects of global change on biodiversity requires its understanding in the past. The main proxy of plant diversity, fossil pollen record, has a complex relationship to surrounding vegetation and unknown spatial scale. We explored both using modern pollen spectra in species-rich and species-poor regions in temperate Central Europe. We also considered the biasing effects of the trees by using sites in forests and open habitats in each region. Pollen samples were collected from moss polsters at 60 sites and plant species were recorded along two 1 km-transects at each site. We found a significant positive correlation between pollen and plant richness (alpha diversity) in both complete datasets and for both subsets from open habitats. Pollen richness in forest datasets is not significantly related to floristic data due to canopy interception of pollen rather than to pollen productivity. Variances (beta diversity) of the six pollen and floristic datasets are strongly correlated. The source area of pollen richness is determined by the number of species appearing with increasing distance, which aggregates information on diversity of individual patches within the landscape mosaic and on their compositional similarity. Our results validate pollen as a reconstruction tool for plant diversity in the past.

Divergent roles of herbivory in eutrophying forests.

Ungulate populations are increasing across Europe with important implications for forest plant communities. Concurrently, atmospheric nitrogen (N) deposition continues to eutrophicate forests, threatening many rare, often more nutrient-efficient, plant species. These pressures may critically interact to shape biodiversity as in grassland and tundra systems, yet any potential interactions in forests remain poorly understood. Here, we combined vegetation resurveys from 52 sites across 13 European countries to test how changes in ungulate herbivory and eutrophication drive long-term changes in forest understorey communities. Increases in herbivory were associated with elevated temporal species turnover, however, identities of winner and loser species depended on N levels. Under low levels of N-deposition, herbivory favored threatened and small-ranged species while reducing the proportion of non-native and nutrient-demanding species. Yet all these trends were reversed under high levels of N-deposition. Herbivores also reduced shrub cover, likely exacerbating N effects by increasing light levels in the understorey. Eutrophication levels may therefore determine whether herbivory acts as a catalyst for the "N time bomb" or as a conservation tool in temperate forests.

Response to Comment on "Forest microclimate dynamics drive plant responses to warming".

Bertrand et al question our interpretation about warming effects on the thermophilization in forest plant communities and propose an alternative way to analyze climatic debt. We show that microclimate warming is a better predictor than macroclimate warming for studying forest plant community responses to warming. Their additional analyses do not affect or change our interpretations and conclusions.

Response to Comment on "Forest microclimate dynamics drive plant responses to warming".

Schall and Heinrichs question our interpretation that the climatic debt in understory plant communities is locally modulated by canopy buffering. However, our results clearly show that the discrepancy between microclimate warming rates and thermophilization rates is highest in forests where canopy cover was reduced, which suggests that the need for communities to respond to warming is highest in those forests.

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.

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

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.

Understanding context dependency in the response of forest understorey plant communities to nitrogen deposition.

Understorey communities can dominate forest plant diversity and strongly affect forest ecosystem structure and function. Understoreys often respond sensitively but inconsistently to drivers of ecological change, including nitrogen (N) deposition. Nitrogen deposition effects, reflected in the concept of critical loads, vary greatly not only among species and guilds, but also among forest types. Here, we characterize such context dependency as driven by differences in the amounts and forms of deposited N, cumulative deposition, the filtering of N by overstoreys, and available plant species pools. Nitrogen effects on understorey trajectories can also vary due to differences in surrounding landscape conditions; ambient browsing pressure; soils and geology; other environmental factors controlling plant growth; and, historical and current disturbance/management regimes. The number of these factors and their potentially complex interactions complicate our efforts to make simple predictions about how N deposition affects forest understoreys. We review the literature to examine evidence for context dependency in N deposition effects on forest understoreys. We also use data from 1814 European temperate forest plots to test the ability of multi-level models to characterize context-dependent understorey responses across sites that differ in levels of N deposition, community composition, local conditions and management history. This analysis demonstrated that historical management, and plot location on light and pH-fertility gradients, significantly affect how understorey communities respond to N deposition. We conclude that species' and communities' responses to N deposition, and thus the determination of critical loads, vary greatly depending on environmental contexts. This complicates our efforts to predict how N deposition will affect forest understoreys and thus how best to conserve and restore understorey biodiversity. To reduce uncertainty and incorporate context dependency in critical load setting, we should assemble data on underlying environmental conditions, conduct globally distributed field experiments, and analyse a wider range of habitat types.