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.

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.

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.

Global patterns of vascular plant alpha diversity.

Global patterns of regional (gamma) plant diversity are relatively well known, but whether these patterns hold for local communities, and the dependence on spatial grain, remain controversial. Using data on 170,272 georeferenced local plant assemblages, we created global maps of alpha diversity (local species richness) for vascular plants at three different spatial grains, for forests and non-forests. We show that alpha diversity is consistently high across grains in some regions (for example, Andean-Amazonian foothills), but regional 'scaling anomalies' (deviations from the positive correlation) exist elsewhere, particularly in Eurasian temperate forests with disproportionally higher fine-grained richness and many African tropical forests with disproportionally higher coarse-grained richness. The influence of different climatic, topographic and biogeographical variables on alpha diversity also varies across grains. Our multi-grain maps return a nuanced understanding of vascular plant biodiversity patterns that complements classic maps of biodiversity hotspots and will improve predictions of global change effects on biodiversity.

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.

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.

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.

Similar factors underlie tree abundance in forests in native and alien ranges.

AIM: Alien plant species can cause severe ecological and economic problems, and therefore attract a lot of research interest in biogeography and related fields. To identify potential future invasive species, we need to better understand the mechanisms underlying the abundances of invasive tree species in their new ranges, and whether these mechanisms differ between their native and alien ranges. Here, we test two hypotheses: that greater relative abundance is promoted by (a) functional difference from locally co-occurring trees, and (b) higher values than locally co-occurring trees for traits linked to competitive ability. LOCATION: Global. TIME PERIOD: Recent. MAJOR TAXA STUDIED: Trees. METHODS: We combined three global plant databases: sPlot vegetation-plot database, TRY plant trait database and Global Naturalized Alien Flora (GloNAF) database. We used a hierarchical Bayesian linear regression model to assess the factors associated with variation in local abundance, and how these relationships vary between native and alien ranges and depend on species' traits. RESULTS: In both ranges, species reach highest abundance if they are functionally similar to co-occurring species, yet are taller and have higher seed mass and wood density than co-occurring species. MAIN CONCLUSIONS: Our results suggest that light limitation leads to strong environmental and biotic filtering, and that it is advantageous to be taller and have denser wood. The striking similarities in abundance between native and alien ranges imply that information from tree species' native ranges can be used to predict in which habitats introduced species may become dominant.

Robinia pseudoacacia-dominated vegetation types of Southern Europe: Species composition, history, distribution and management.

Knowledge of the species composition of invaded vegetation helps to evaluate an ecological impact of aliens and design an optimal management strategy. We link a new vegetation analysis of a large dataset to the invasion history, ecology and management of Robinia pseudoacacia stands across Southern Europe and provide a map illustrating Robinia distribution. Finally, we compare detected relationships with Central Europe. We show that regional differences in Robinia invasion, distribution, habitats and management are driven both by local natural conditions (climate and soil properties, low competitive ability with native trees) and socioeconomic factors (traditional land-use). Based on the classification of 467 phytosociological relevés we distinguished five broad vegetation types reflecting an oceanity-continentality gradient. The stands were heterogeneous and included 824 taxa, with only 5.8% occurring in more than 10% of samples, representing mainly hemerobic generalists of mesophilous, nutrient-rich and semi-shady habitats. The most common were dry ruderal stands invading human-made habitats. Among native communities, disturbed mesic and alluvial forests were often invaded throughout the area, while dry forests and scrub dominated in Balkan countries. Continuous, long-term and large-scale cultivation represent a crucial factor driving Robinia invasions in natural habitats. Its invasion should be mitigated by suitable management taking into account adjacent habitats and changing cultivation practices to select for native species. Robinia invasion has a comparable pattern in Central and Southern Europe, but there is a substantial difference in management and utilization causing heterogeneity of many South-European stands.

Poleward migration of the destructive effects of tropical cyclones during the 20th century.

Determination of long-term tropical cyclone (TC) variability is of enormous importance to society; however, changes in TC activity are poorly understood owing to discrepancies among various datasets and limited span of instrumental records. While the increasing intensity and frequency of TCs have been previously documented on a long-term scale using various proxy records, determination of their poleward migration has been based mostly on short-term instrumental data. Here we present a unique tree-ring-based approach for determination of long-term variability in TC activity via forest disturbance rates in northeast Asia (33-45°N). Our results indicate significant long-term changes in TC activity, with increased rates of disturbances in the northern latitudes over the past century. The disturbance frequency was stable over time in the southern latitudes, however. Our findings of increasing disturbance frequency in the areas formerly situated at the edge of TC activity provide evidence supporting the broad relevance of poleward migration of TCs. Our results significantly enhance our understanding of the effects of climate change on TCs and emphasize the need for determination of long-term variation of past TC activity to improve future TC projections.

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.

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.

Life stage, not climate change, explains observed tree range shifts.

Ongoing climate change is expected to shift tree species distribution and therefore affect forest biodiversity and ecosystem services. To assess and project tree distributional shifts, researchers may compare the distribution of juvenile and adult trees under the assumption that differences between tree life stages reflect distributional shifts triggered by climate change. However, the distribution of tree life stages could differ within the lifespan of trees, therefore, we hypothesize that currently observed distributional differences could represent shifts over ontogeny as opposed to climatically driven changes. Here, we test this hypothesis with data from 1435 plots resurveyed after more than three decades across the Western Carpathians. We compared seedling, sapling and adult distribution of 12 tree species along elevation, temperature and precipitation gradients. We analyzed (i) temporal shifts between the surveys and (ii) distributional differences between tree life stages within both surveys. Despite climate warming, tree species distribution of any life stage did not shift directionally upward along elevation between the surveys. Temporal elevational shifts were species specific and an order of magnitude lower than differences among tree life stages within the surveys. Our results show that the observed range shifts among tree life stages are more consistent with ontogenetic differences in the species' environmental requirements than with responses to recent climate change. The distribution of seedlings substantially differed from saplings and adults, while the distribution of saplings did not differ from adults, indicating a critical transition between seedling and sapling tree life stages. Future research has to take ontogenetic differences among life stages into account as we found that distributional differences recently observed worldwide may not reflect climate change but rather the different environmental requirements of tree life stages.

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.

Plant movements and climate warming: intraspecific variation in growth responses to nonlocal soils.

Most range shift predictions focus on the dispersal phase of the colonization process. Because moving populations experience increasingly dissimilar nonclimatic environmental conditions as they track climate warming, it is also critical to test how individuals originating from contrasting thermal environments can establish in nonlocal sites. We assess the intraspecific variation in growth responses to nonlocal soils by planting a widespread grass of deciduous forests (Milium effusum) into an experimental common garden using combinations of seeds and soil sampled in 22 sites across its distributional range, and reflecting movement scenarios of up to 1600 km. Furthermore, to determine temperature and forest-structural effects, the plants and soils were experimentally warmed and shaded. We found significantly positive effects of the difference between the temperature of the sites of seed and soil collection on growth and seedling emergence rates. Migrant plants might thus encounter increasingly favourable soil conditions while tracking the isotherms towards currently 'colder' soils. These effects persisted under experimental warming. Rising temperatures and light availability generally enhanced plant performance. Our results suggest that abiotic and biotic soil characteristics can shape climate change-driven plant movements by affecting growth of nonlocal migrants, a mechanism which should be integrated into predictions of future range shifts.

Microclimate moderates plant responses to macroclimate warming.

Recent global warming is acting across marine, freshwater, and terrestrial ecosystems to favor species adapted to warmer conditions and/or reduce the abundance of cold-adapted organisms (i.e., "thermophilization" of communities). Lack of community responses to increased temperature, however, has also been reported for several taxa and regions, suggesting that "climatic lags" may be frequent. Here we show that microclimatic effects brought about by forest canopy closure can buffer biotic responses to macroclimate warming, thus explaining an apparent climatic lag. Using data from 1,409 vegetation plots in European and North American temperate forests, each surveyed at least twice over an interval of 12-67 y, we document significant thermophilization of ground-layer plant communities. These changes reflect concurrent declines in species adapted to cooler conditions and increases in species adapted to warmer conditions. However, thermophilization, particularly the increase of warm-adapted species, is attenuated in forests whose canopies have become denser, probably reflecting cooler growing-season ground temperatures via increased shading. As standing stocks of trees have increased in many temperate forests in recent decades, local microclimatic effects may commonly be moderating the impacts of macroclimate warming on forest understories. Conversely, increases in harvesting woody biomass--e.g., for bioenergy--may open forest canopies and accelerate thermophilization of temperate forest biodiversity.

Plant diversity changes during the postglacial in East Asia: insights from Forest Refugia on Halla Volcano, Jeju Island.

Understanding how past climate changes affected biodiversity is a key issue in contemporary ecology and conservation biology. These diversity changes are, however, difficult to reconstruct from paleoecological sources alone, because macrofossil and pollen records do not provide complete information about species assemblages. Ecologists therefore use information from modern analogues of past communities in order to get a better understanding of past diversity changes. Here we compare plant diversity, species traits and environment between late-glacial Abies, early-Holocene Quercus, and mid-Holocene warm-temperate Carpinus forest refugia on Jeju Island, Korea in order to provide insights into postglacial changes associated with their replacement. Based on detailed study of relict communities, we propose that the late-glacial open-canopy conifer forests in southern part of Korean Peninsula were rich in vascular plants, in particular of heliophilous herbs, whose dramatic decline was caused by the early Holocene invasion of dwarf bamboo into the understory of Quercus forests, followed by mid-Holocene expansion of strongly shading trees such as maple and hornbeam. This diversity loss was partly compensated in the Carpinus forests by an increase in shade-tolerant evergreen trees, shrubs and lianas. However, the pool of these species is much smaller than that of light-demanding herbs, and hence the total species richness is lower, both locally and in the whole area of the Carpinus and Quercus forests. The strongly shading tree species dominating in the hornbeam forests have higher leaf tissue N and P concentrations and smaller leaf dry matter content, which enhances litter decomposition and nutrient cycling and in turn favored the selection of highly competitive species in the shrub layer. This further reduced available light and caused almost complete disappearance of understory herbs, including dwarf bamboo.