Evolutionary dynamics of Euphorbia carniolica suggest a complex Plio-Pleistocene history of understorey species of deciduous forest in southeastern Europe.

Deciduous forests form the dominant natural vegetation of Europe today, but were restricted to small refugia during Pleistocene cold stages, implying an evolutionary past shaped by recurrent range contractions and expansions. Cold-stage forest refugia were probably widespread in southern and central Europe, with the northwestern Balkan Peninsula being of particular importance. However, the actual number and location of deciduous forest refugia, as well as the connections between them, remain disputed. Here, we address the evolutionary dynamics of the deciduous forest understorey species Euphorbia carniolica as a proxy for past forest dynamics. To do so, we obtained genomic and morphometric data from populations representing the species' entire range, investigated phylogenetic position and intraspecific genetic variation, tested explicit demographic scenarios and applied species distribution models. Our data support two disjoint groups linked to separate refugia on the northwestern and central Balkan Peninsula. We find that genetic differentiation between groups started in the early Pleistocene via vicariance, suggesting a larger distribution in the past. Both refugia acted as sources for founder events to the southeastern Alps and the Carpathians; the latter were likely colonised before the last cold stage. In line with traditional views on the pre-Pleistocene origin of many southeastern European deciduous forest species, the origin of E. carniolica was dated to the late Pliocene. The fact that E. carniolica evolved at a time when a period of continuous forestation was ending in much of Eurasia provides an interesting biogeographical perspective on the past links between Eurasian deciduous forests and their biota.

Post-glacial range formation of temperate forest understorey herbs - Insights from a spatio-temporally explicit modelling approach.

Aim: Our knowledge of Pleistocene refugia and post-glacial recolonization routes of forest understorey plants is still very limited. The geographical ranges of these species are often rather narrow and show highly idiosyncratic, often fragmented patterns indicating either narrow and species-specific ecological tolerances or strong dispersal limitations. However, the relative roles of these factors are inherently difficult to disentangle. Location: Central and south-eastern Europe. Time period: 17,100 BP - present. Major taxa studied: Five understorey herbs of European beech forests: Aposeris foetida, Cardamine trifolia, Euphorbia carniolica, Hacquetia epipactis and Helleborus niger. Methods: We used spatio-temporally explicit modelling to reconstruct the post-glacial range dynamics of the five forest understorey herbs. We varied niche requirements, demographic rates and dispersal abilities across plausible ranges and simulated the spread of species from potential Pleistocene refugia identified by phylogeographical analyses. Then we identified the parameter settings allowing for the most accurate reconstruction of their current geographical ranges. Results: We found a largely homogenous pattern of optimal parameter settings among species. Broad ecological niches had to be combined with very low but non-zero rates of long-distance dispersal via chance events and low rates of seed dispersal over moderate distances by standard dispersal vectors. However, long-distance dispersal events, although rare, led to high variation among replicated simulation runs. Main conclusions: Small and fragmented ranges of many forest understorey species are best explained by a combination of broad ecological niches and rare medium- and long-distance dispersal events. Stochasticity is thus an important determinant of current species ranges, explaining the idiosyncratic distribution patterns of the study species despite strong similarities in refugia, ecological tolerances and dispersal abilities.

Range dynamics of mountain plants decrease with elevation.

Many studies report that mountain plant species are shifting upward in elevation. However, the majority of these reports focus on shifts of upper limits. Here, we expand the focus and simultaneously analyze changes of both range limits, optima, and abundances of 183 mountain plant species. We therefore resurveyed 1,576 vegetation plots first recorded before 1970 in the European Alps. We found that both range limits and optima shifted upward in elevation, but the most pronounced trend was a mean increase in species abundance. Despite huge species-specific variation, range dynamics showed a consistent trend along the elevational gradient: Both range limits and optima shifted upslope faster the lower they were situated historically, and species' abundance increased more for species from lower elevations. Traits affecting the species' dispersal and persistence capacity were not related to their range dynamics. Using indicator values to stratify species by their thermal and nutrient demands revealed that elevational ranges of thermophilic species tended to expand, while those of cold-adapted species tended to contract. Abundance increases were strongest for nutriphilous species. These results suggest that recent climate warming interacted with airborne nitrogen deposition in driving the observed dynamics. So far, the majority of species appear as "winners" of recent changes, yet "losers" are overrepresented among high-elevation, cold-adapted species with low nutrient demands. In the decades to come, high-alpine species may hence face the double pressure of climatic changes and novel, superior competitors that move up faster than they themselves can escape to even higher elevations.

An explicit test of Pleistocene survival in peripheral versus nunatak refugia in two high mountain plant species.

Pleistocene climate fluctuations had profound influence on the biogeographical history of many biota. As large areas in high mountain ranges were covered by glaciers, biota were forced either to peripheral refugia (and possibly beyond to lowland refugia) or to interior refugia (nunataks). However, nunatak survival remains controversial as it relies solely on correlative genetic evidence. Here, we test hypotheses of glacial survival using two high alpine plant species (the insect-pollinated Pedicularis asplenifolia and wind-pollinated Carex fuliginosa) in the European Alps. Employing the iDDC (integrative Distributional, Demographic and Coalescent) approach, which couples species distribution modelling, spatial and temporal demographic simulation and Approximate Bayesian Computation, we explicitly test three hypotheses of glacial survival: (a) peripheral survival only, (b) nunatak survival only and (c) peripheral plus nunatak survival. In P. asplenifolia the peripheral plus nunatak survival hypothesis was supported by Bayes factors (BF> 100), whereas in C. fuliginosa the peripheral survival only hypothesis, although best supported, could not be unambiguously distinguished from the peripheral plus nunatak survival hypothesis (BF = 5.58). These results are consistent with current habitat preferences (P. asplenifolia extends to higher elevations) and the potential for genetic swamping (i.e., replacement of local genotypes via hybridization with immigrating genotypes [expected to be higher in the wind-pollinated C. fuliginosa]). Although the persistence of plants on nunataks during glacial periods has been debated and studied over decades, this is one of the first studies to explicitly test the hypothesis instead of solely using correlative evidence.

A socio-ecological model for predicting impacts of land-use and climate change on regional plant diversity in the Austrian Alps.

Climate and land-use change jointly affect the future of biodiversity. Yet, biodiversity scenarios have so far concentrated on climatic effects because forecasts of land use are rarely available at appropriate spatial and thematic scales. Agent-based models (ABMs) represent a potentially powerful but little explored tool for establishing thematically and spatially fine-grained land-use scenarios. Here, we use an ABM parameterized for 1,329 agents, mostly farmers, in a Central European model region, and simulate the changes to land-use patterns resulting from their response to three scenarios of changing socio-economic conditions and three scenarios of climate change until the mid of the century. Subsequently, we use species distribution models to, first, analyse relationships between the realized niches of 832 plant species and climatic gradients or land-use types, respectively, and, second, to project consequent changes in potential regional ranges of these species as triggered by changes in both the altered land-use patterns and the changing climate. We find that both drivers determine the realized niches of the studied plants, with land use having a stronger effect than any single climatic variable in the model. Nevertheless, the plants' future distributions appear much more responsive to climate than to land-use changes because alternative future socio-economic backgrounds have only modest impact on land-use decisions in the model region. However, relative effects of climate and land-use changes on biodiversity may differ drastically in other regions, especially where landscapes are still dominated by natural or semi-natural habitat. We conclude that agent-based modelling of land use is able to provide scenarios at scales relevant to individual species distribution and suggest that coupling ABMs with models of species' range change should be intensified to provide more realistic biodiversity forecasts.

Reconstructing geographical parthenogenesis: effects of niche differentiation and reproductive mode on Holocene range expansion of an alpine plant.

Asexual taxa often have larger ranges than their sexual progenitors, particularly in areas affected by Pleistocene glaciations. The reasons given for this 'geographical parthenogenesis' are contentious, with expansion of the ecological niche or colonisation advantages of uniparental reproduction assumed most important in case of plants. Here, we parameterized a spread model for the alpine buttercup Ranunculus kuepferi and reconstructed the joint Holocene range expansion of its sexual and apomictic cytotype across the European Alps under different simulation settings. We found that, rather than niche broadening or a higher migration rate, a shift of the apomict's niche towards colder conditions per se was crucial as it facilitated overcoming of topographical barriers, a factor likely relevant for many alpine apomicts. More generally, our simulations suggest potentially strong interacting effects of niche differentiation and reproductive modes on range formation of related sexual and asexual taxa arising from their differential sensitivity to minority cytotype disadvantage.

A higher-level classification of the Pannonian and western Pontic steppe grasslands (Central and Eastern Europe).

QUESTIONS: What are the main floristic patterns in the Pannonian and western Pontic steppe grasslands? What are the diagnostic species of the major subdivisions of the class Festuco-Brometea (temperate Euro-Siberian dry and semi-dry grasslands)? LOCATION: Carpathian Basin (E Austria, SE Czech Republic, Slovakia, Hungary, Romania, Slovenia, N Croatia and N Serbia), Ukraine, S Poland and the Bryansk region of W Russia. METHODS: We applied a geographically stratified resampling to a large set of relevés containing at least one indicator species of steppe grasslands. The resulting data set of 17 993 relevés was classified using the TWINSPAN algorithm. We identified groups of clusters that corresponded to the class Festuco-Brometea. After excluding relevés not belonging to our target class, we applied a consensus of three fidelity measures, also taking into account external knowledge, to establish the diagnostic species of the orders of the class. The original TWINSPAN divisions were revised on the basis of these diagnostic species. RESULTS: The TWINSPAN classification revealed soil moisture as the most important environmental factor. Eight out of 16 TWINSPAN groups corresponded to Festuco-Brometea. A total of 80, 32 and 58 species were accepted as diagnostic for the orders Brometalia erecti, Festucetalia valesiacae and Stipo-Festucetalia pallentis, respectively. In the further subdivision of the orders, soil conditions, geographic distribution and altitude could be identified as factors driving the major floristic patterns. CONCLUSIONS: We propose the following classification of the Festuco-Brometea in our study area: (1) Brometalia erecti (semi-dry grasslands) with Scabioso ochroleucae-Poion angustifoliae (steppe meadows of the forest zone of E Europe) and Cirsio-Brachypodion pinnati (meadow steppes on deep soils in the forest-steppe zone of E Central and E Europe); (2) Festucetalia valesiacae (grass steppes) with Festucion valesiacae (grass steppes on less developed soils in the forest-steppe zone of E Central and E Europe) and Stipion lessingianae (grass steppes in the steppe zone); (3) Stipo-Festucetalia pallentis (rocky steppes) with Asplenio septentrionalis-Festucion pallentis (rocky steppes on siliceous and intermediate soils), Bromo-Festucion pallentis (thermophilous rocky steppes on calcareous soils), Diantho-Seslerion (dealpine Sesleria caerulea grasslands of the Western Carpathians) and Seslerion rigidae (dealpine Sesleria rigida grasslands of the Romanian Carpathians).

Uncertainty in predicting range dynamics of endemic alpine plants under climate warming.

Correlative species distribution models have long been the predominant approach to predict species' range responses to climate change. Recently, the use of dynamic models is increasingly advocated for because these models better represent the main processes involved in range shifts and also simulate transient dynamics. A well-known problem with the application of these models is the lack of data for estimating necessary parameters of demographic and dispersal processes. However, what has been hardly considered so far is the fact that simulating transient dynamics potentially implies additional uncertainty arising from our ignorance of short-term climate variability in future climatic trends. Here, we use endemic mountain plants of Austria as a case study to assess how the integration of decadal variability in future climate affects outcomes of dynamic range models as compared to projected long-term trends and uncertainty in demographic and dispersal parameters. We do so by contrasting simulations of a so-called hybrid model run under fluctuating climatic conditions with those based on a linear interpolation of climatic conditions between current values and those predicted for the end of the 21st century. We find that accounting for short-term climate variability modifies model results nearly as differences in projected long-term trends and much more than uncertainty in demographic/dispersal parameters. In particular, range loss and extinction rates are much higher when simulations are run under fluctuating conditions. These results highlight the importance of considering the appropriate temporal resolution when parameterizing and applying range-dynamic models, and hybrid models in particular. In case of our endemic mountain plants, we hypothesize that smoothed linear time series deliver more reliable results because these long-lived species are primarily responsive to long-term climate averages.

Tree cover at fine and coarse spatial grains interacts with shade tolerance to shape plant species distributions across the Alps.

The role of competition for light among plants has long been recognised at local scales, but its importance for plant species distributions at larger spatial scales has generally been ignored. Tree cover modifies the local abiotic conditions below the canopy, notably by reducing light availability, and thus, also the performance of species that are not adapted to low-light conditions. However, this local effect may propagate to coarser spatial grains, by affecting colonisation probabilities and local extinction risks of herbs and shrubs. To assess the effect of tree cover at both the plot- and landscape-grain sizes (approximately 10-m and 1-km), we fit Generalised Linear Models (GLMs) for the plot-level distributions of 960 species of herbs and shrubs using 6,935 vegetation plots across the European Alps. We ran four models with different combinations of variables (climate, soil and tree cover) at both spatial grains for each species. We used partial regressions to evaluate the independent effects of plot- and landscape-grain tree cover on plot-level plant communities. Finally, the effects on species-specific elevational range limits were assessed by simulating a removal experiment comparing the species distributions under high and low tree cover. Accounting for tree cover improved the model performance, with the probability of the presence of shade-tolerant species increasing with increasing tree cover, whereas shade-intolerant species showed the opposite pattern. The tree cover effect occurred consistently at both the plot and landscape spatial grains, albeit most strongly at the former. Importantly, tree cover at the two grain sizes had partially independent effects on plot-level plant communities. With high tree cover, shade-intolerant species exhibited narrower elevational ranges than with low tree cover whereas shade-tolerant species showed wider elevational ranges at both limits. These findings suggest that forecasts of climate-related range shifts for herb and shrub species may be modified by tree cover dynamics.

Scale decisions can reverse conclusions on community assembly processes.

AIM: Phylogenetic diversity patterns are increasingly being used to better understand the role of ecological and evolutionary processes in community assembly. Here, we quantify how these patterns are influenced by scale choices in terms of spatial and environmental extent and organismic scales. LOCATION: European Alps. METHODS: We applied 42 sampling strategies differing in their combination of focal scales. For each resulting sub-dataset, we estimated the phylogenetic diversity of the species pools, phylogenetic α-diversities of local communities, and statistics commonly used together with null models in order to infer non-random diversity patterns (i.e. phylogenetic clustering versus over-dispersion). Finally, we studied the effects of scale choices on these measures using regression analyses. RESULTS: Scale choices were decisive for revealing signals in diversity patterns. Notably, changes in focal scales sometimes reversed a pattern of over-dispersion into clustering. Organismic scale had a stronger effect than spatial and environmental extent. However, we did not find general rules for the direction of change from over-dispersion to clustering with changing scales. Importantly, these scale issues had only a weak influence when focusing on regional diversity patterns that change along abiotic gradients. MAIN CONCLUSIONS: Our results call for caution when combining phylogenetic data with distributional data to study how and why communities differ from random expectations of phylogenetic relatedness. These analyses seem to be robust when the focus is on relating community diversity patterns to variation in habitat conditions, such as abiotic gradients. However, if the focus is on identifying relevant assembly rules for local communities, the uncertainty arising from a certain scale choice can be immense. In the latter case, it becomes necessary to test whether emerging patterns are robust to alternative scale choices.

Evidence for Glacial Refugia of the Forest Understorey Species Helleborus niger (Ranunculaceae) in the Southern as Well as in the Northern Limestone Alps.

Glacial refugia of alpine and subnival biota have been intensively studied in the European Alps but the fate of forests and their understory species in that area remains largely unclear. In order to fill this gap, we aimed at disentangling the spatiotemporal diversification of disjunctly distributed black hellebore Helleborus niger (Ranunculaceae). We applied a set of phylogeographic analyses based on restriction-site associated DNA sequencing (RADseq) data and plastid DNA sequences to a range-wide sampling of populations. These analyses were supplemented with species distribution models generated for the present and the Last Glacial Maximum (LGM). We used exploratory analyses to delimit genomically coherent groups and then employed demographic modeling to reconstruct the history of these groups. We uncovered a deep split between two major genetic groups with western and eastern distribution within the Southern Limestone Alps, likely reflecting divergent evolution since the mid-Pleistocene in two glacial refugia situated along the unglaciated southern margin of the Alps. Long-term presence in the Southern Limestone Alps is also supported by high numbers of private alleles, elevated levels of nucleotide diversity and the species' modeled distribution at the LGM. The deep genetic divergence, however, is not reflected in leaf shape variation, suggesting that the morphological discrimination of genetically divergent entities within H. niger is questionable. At a shallower level, populations from the Northern Limestone Alps are differentiated from those in the Southern Limestone Alps in both RADseq and plastid DNA data sets, reflecting the North-South disjunction within the Eastern Alps. The underlying split was dated to ca. 0.1 mya, which is well before the LGM. In the same line, explicit tests of demographic models consistently rejected the hypothesis that the partial distribution area in the Northern Limestone Alps is the result of postglacial colonization. Taken together, our results strongly support that forest understory species such as H. niger have survived the LGM in refugia situated along the southern, but also along the northern or northeastern periphery of the Alps. Being a slow migrator, the species has likely survived repeated glacial-interglacial circles in distributional stasis while the composition of the tree canopy changed in the meanwhile.

Extinction debts and colonization credits of non-forest plants in the European Alps.

Mountain plant species shift their elevational ranges in response to climate change. However, to what degree these shifts lag behind current climate change, and to what extent delayed extinctions and colonizations contribute to these shifts, are under debate. Here, we calculate extinction debt and colonization credit of 135 species from the European Alps by comparing species distribution models with 1576 re-surveyed plots. We find extinction debt in 60% and colonization credit in 38% of the species, and at least one of the two in 93%. This suggests that the realized niche of very few of the 135 species fully tracks climate change. As expected, extinction debts occur below and colonization credits occur above the optimum elevation of species. Colonization credits are more frequent in warmth-demanding species from lower elevations with lower dispersal capability, and extinction debts are more frequent in cold-adapted species from the highest elevations. Local extinctions hence appear to be already pending for those species which have the least opportunity to escape climate warming.

Habitat Structure, Quality and Landscape Predict Species Richness and Communities of Collembola in Dry Grasslands in Austria.

We assessed the relationships between site size, habitat quality, landscape factors (fragmentation, landscape diversity) and species richness in communities of Collembola in 50 small dry grassland habitat patches in an agricultural landscape of eastern Austria. Grasslands in that region were once widespread and extensive, but have become increasingly fragmented and isolated. We hypothesized that dry grassland springtails species richness is significantly correlated with site variables (soil properties, habitat quality) and that the size of grassland sites is positively correlated with species richness. We used pitfall traps in 50 dry grasslands in differently structured agricultural landscapes and tested total abundance and three species richness measures: (1) the number of dry grassland specialist species, (2) total number of dry grassland species and (3) overall species richness. In the multivariate correlation models, we found that all species richness measures were significantly related to the plant species richness, a shape parameter of the sites, soil properties such as humus, temperature, sand and gravel content and the landscape variable reflecting isolation (distance to the nearest large dry grassland area). This landscape variable indicates that neighbouring grasslands are influencing the species richness of the sites. This may be a result of passive wind dispersal across the landscape or historic connection of the small sites with much larger dry grasslands. The size of the site did not show any significant correlation with total, dry grassland specialist, dry grassland generalist or generalist species richness. The small size of Collembola might explain these findings, because they have high population densities even in small patches.

History and environment shape species pools and community diversity in European beech forests.

A central hypothesis of ecology states that regional diversity influences local diversity through species-pool effects. Species pools are supposedly shaped by large-scale factors and then filtered into ecological communities, but understanding these processes requires the analysis of large datasets across several regions. Here, we use a framework of community assembly at a continental scale to test the relative influence of historical and environmental drivers, in combination with regional or local species pools, on community species richness and community completeness. Using 42,173 vegetation plots sampled across European beech forests, we found that large-scale factors largely accounted for species pool sizes. At the regional scale, main predictors reflected historical contingencies related to post-glacial dispersal routes, whereas at the local scale, the influence of environmental filters was predominant. Proximity to Quaternary refugia and high precipitation were the main factors supporting community species richness, especially among beech forest specialist plants. Models for community completeness indicate the influence of large-scale factors, further suggesting community saturation as a result of dispersal limitation or biotic interactions. Our results empirically demonstrate how historical factors complement environmental gradients to provide a better understanding of biodiversity patterns across multiple regions.

A matter of scale: apparent niche differentiation of diploid and tetraploid plants may depend on extent and grain of analysis.

AIM: Emerging polyploids may depend on environmental niche shifts for successful establishment. Using the alpine plant Ranunculus kuepferi as a model system, we explore the niche shift hypothesis at different spatial resolutions and in contrasting parts of the species range. LOCATION: European Alps. METHODS: We sampled 12 individuals from each of 102 populations of R. kuepferi across the Alps, determined their ploidy levels, derived coarse-grain (100 × 100 m) environmental descriptors for all sampling sites by downscaling WorldClim maps, and calculated fine-scale environmental descriptors (2 × 2 m) from indicator values of the vegetation accompanying the sampled individuals. Both coarse and fine-scale variables were further computed for 8239 vegetation plots from across the Alps. Subsequently, we compared niche optima and breadths of diploid and tetraploid cytotypes by combining principal components analysis and kernel smoothing procedures. Comparisons were done separately for coarse and fine-grain data sets and for sympatric, allopatric and the total set of populations. RESULTS: All comparisons indicate that the niches of the two cytotypes differ in optima and/or breadths, but results vary in important details. The whole-range analysis suggests differentiation along the temperature gradient to be most important. However, sympatric comparisons indicate that this climatic shift was not a direct response to competition with diploid ancestors. Moreover, fine-grained analyses demonstrate niche contraction of tetraploids, especially in the sympatric range, that goes undetected with coarse-grained data. MAIN CONCLUSIONS: Although the niche optima of the two cytotypes differ, separation along ecological gradients was probably less decisive for polyploid establishment than a shift towards facultative apomixis, a particularly effective strategy to avoid minority cytotype exclusion. In addition, our results suggest that coarse-grained analyses overestimate niche breadths of widely distributed taxa. Niche comparison analyses should hence be conducted at environmental data resolutions appropriate for the organism and question under study.

Cross-scale analysis of the region effect on vascular plant species diversity in southern and northern European mountain ranges.

BACKGROUND: The divergent glacial histories of southern and northern Europe affect present-day species diversity at coarse-grained scales in these two regions, but do these effects also penetrate to the more fine-grained scales of local communities? METHODOLOGY/PRINCIPAL FINDINGS: We carried out a cross-scale analysis to address this question for vascular plants in two mountain regions, the Alps in southern Europe and the Scandes in northern Europe, using environmentally paired vegetation plots in the two regions (n = 403 in each region) to quantify four diversity components: (i) total number of species occurring in a region (total γ-diversity), (ii) number of species that could occur in a target plot after environmental filtering (habitat-specific γ-diversity), (iii) pair-wise species compositional turnover between plots (plot-to-plot ß-diversity) and (iv) number of species present per plot (plot α-diversity). We found strong region effects on total γ-diversity, habitat-specific γ-diversity and plot-to-plot ß-diversity, with a greater diversity in the Alps even towards distances smaller than 50 m between plots. In contrast, there was a slightly greater plot α-diversity in the Scandes, but with a tendency towards contrasting region effects on high and low soil-acidity plots. CONCLUSIONS/SIGNIFICANCE: We conclude that there are strong regional differences between coarse-grained (landscape- to regional-scale) diversity components of the flora in the Alps and the Scandes mountain ranges, but that these differences do not necessarily penetrate to the finest-grained (plot-scale) diversity component, at least not on acidic soils. Our findings are consistent with the contrasting regional Quaternary histories, but we also consider alternative explanatory models. Notably, ecological sorting and habitat connectivity may play a role in the unexpected limited or reversed region effect on plot α-diversity, and may also affect the larger-scale diversity components. For instance, plot connectivity and/or selection for high dispersal ability may increase plot α-diversity and compensate for low total γ-diversity.