Multispecies deep learning using citizen science data produces more informative plant community models.

In the age of big data, scientific progress is fundamentally limited by our capacity to extract critical information. Here, we map fine-grained spatiotemporal distributions for thousands of species, using deep neural networks (DNNs) and ubiquitous citizen science data. Based on 6.7 M observations, we jointly model the distributions of 2477 plant species and species aggregates across Switzerland with an ensemble of DNNs built with different cost functions. We find that, compared to commonly-used approaches, multispecies DNNs predict species distributions and especially community composition more accurately. Moreover, their design allows investigation of understudied aspects of ecology. Including seasonal variations of observation probability explicitly allows approximating flowering phenology; reweighting predictions to mirror cover-abundance allows mapping potentially canopy-dominant tree species nationwide; and projecting DNNs into the future allows assessing how distributions, phenology, and dominance may change. Given their skill and their versatility, multispecies DNNs can refine our understanding of the distribution of plants and well-sampled taxa in general.

Leaf metabolic traits reveal hidden dimensions of plant form and function.

The metabolome is the biochemical basis of plant form and function, but we know little about its macroecological variation across the plant kingdom. Here, we used the plant functional trait concept to interpret leaf metabolome variation among 457 tropical and 339 temperate plant species. Distilling metabolite chemistry into five metabolic functional traits reveals that plants vary on two major axes of leaf metabolic specialization-a leaf chemical defense spectrum and an expression of leaf longevity. Axes are similar for tropical and temperate species, with many trait combinations being viable. However, metabolic traits vary orthogonally to life-history strategies described by widely used functional traits. The metabolome thus expands the functional trait concept by providing additional axes of metabolic specialization for examining plant form and function.

ForestClim-Bioclimatic variables for microclimate temperatures of European forests.

Microclimate research gained renewed interest over the last decade and its importance for many ecological processes is increasingly being recognized. Consequently, the call for high-resolution microclimatic temperature grids across broad spatial extents is becoming more pressing to improve ecological models. Here, we provide a new set of open-access bioclimatic variables for microclimate temperatures of European forests at 25 × 25 m2 resolution.

DNA-based networks reveal the ecological determinants of plant-herbivore interactions along environmental gradients.

Understanding the ecological rules structuring the organization of species interactions is a prerequisite to predicting how ecosystems respond to environmental changes. While the ecological determinants of single networks have been documented, it remains unclear whether network ecological rules are conserved along spatial and environmental gradients. To address this gap, we reconstructed 48 plant-herbivore interaction networks along six elevation gradients in the Central European Alps in Switzerland, using DNA metabarcoding on orthoptera faeces. We developed hypotheses on the ecological mechanisms expected to structure interaction networks, based on plant phylogeny, plant abundance, leaf toughness, leaf nitrogen content and plant metabolomics. We show that plant phylogenetic relationships and species abundance have the greatest explanatory power regarding the structure of the ecological networks. Moreover, we found that leaf nitrogen content is a key determinant of interactions in warmer environments, while phenolic compounds and tannins are more important in colder environments, suggesting that determinants of species interactions can shift along environmental gradients. With this work, we propose an approach to study the mechanisms that structure the way species interact with each other between bioregions and ecosystems.

ForestTemp - Sub-canopy microclimate temperatures of European forests.

Ecological research heavily relies on coarse-gridded climate data based on standardized temperature measurements recorded at 2 m height in open landscapes. However, many organisms experience environmental conditions that differ substantially from those captured by these macroclimatic (i.e. free air) temperature grids. In forests, the tree canopy functions as a thermal insulator and buffers sub-canopy microclimatic conditions, thereby affecting biological and ecological processes. To improve the assessment of climatic conditions and climate-change-related impacts on forest-floor biodiversity and functioning, high-resolution temperature grids reflecting forest microclimates are thus urgently needed. Combining more than 1200 time series of in situ near-surface forest temperature with topographical, biological and macroclimatic variables in a machine learning model, we predicted the mean monthly offset between sub-canopy temperature at 15 cm above the surface and free-air temperature over the period 2000-2020 at a spatial resolution of 25 m across Europe. This offset was used to evaluate the difference between microclimate and macroclimate across space and seasons and finally enabled us to calculate mean annual and monthly temperatures for European forest understories. We found that sub-canopy air temperatures differ substantially from free-air temperatures, being on average 2.1°C (standard deviation ± 1.6°C) lower in summer and 2.0°C higher (±0.7°C) in winter across Europe. Additionally, our high-resolution maps expose considerable microclimatic variation within landscapes, not captured by the gridded macroclimatic products. The provided forest sub-canopy temperature maps will enable future research to model below-canopy biological processes and patterns, as well as species distributions more accurately.

Spatial and evolutionary predictability of phytochemical diversity.

To cope with environmental challenges, plants produce a wide diversity of phytochemicals, which are also the source of numerous medicines. Despite decades of research in chemical ecology, we still lack an understanding of the organization of plant chemical diversity across species and ecosystems. To address this challenge, we hypothesized that molecular diversity is not only related to species diversity, but also constrained by trophic, climatic, and topographical factors. We screened the metabolome of 416 vascular plant species encompassing the entire alpine elevation range and four alpine bioclimatic regions in order to characterize their phytochemical diversity. We show that by coupling phylogenetic information, topographic, edaphic, and climatic variables, we predict phytochemical diversity, and its inherent composition, of plant communities throughout landscape. Spatial mapping of phytochemical diversity further revealed that plant assemblages found in low to midelevation habitats, with more alkaline soils, possessed greater phytochemical diversity, whereas alpine habitats possessed higher phytochemical endemism. Altogether, we present a general tool that can be used for predicting hotspots of phytochemical diversity in the landscape, independently of plant species taxonomic identity. Such an approach offers promising perspectives in both drug discovery programs and conservation efforts worldwide.

Novel trophic interactions under climate change promote alpine plant coexistence.

Herbivory and plant defenses exhibit a coupled decline along elevation gradients. However, the current ecological equilibrium could be disrupted under climate change, with a faster upward range shift of animals than plants. Here, we experimentally simulated this upward herbivore range shift by translocating low-elevation herbivore insects to alpine grasslands. We report that the introduction of novel herbivores and increased herbivory disrupted the vertical functional organization of the plant canopy. By feeding preferentially on alpine plants with functional traits matching their low-elevation host plants, herbivores reduced the biomass of dominant alpine plant species and favored encroachment of herbivore-resistant small-stature plant species, inflating species richness. Supplementing a direct effect of temperature, novel biotic interactions represent a neglected but major driver of ecosystem modifications under climate change.

A landscape-scale assessment of the relationship between grassland functioning, community diversity, and functional traits.

Livestock farmers rely on a high and stable grassland productivity for fodder production to sustain their livelihoods. Future drought events related to climate change, however, threaten grassland functionality in many regions across the globe. The introduction of sustainable grassland management could buffer these negative effects. According to the biodiversity-productivity hypothesis, productivity positively associates with local biodiversity. The biodiversity-insurance hypothesis states that higher biodiversity enhances the temporal stability of productivity. To date, these hypotheses have mostly been tested through experimental studies under restricted environmental conditions, hereby neglecting climatic variations at a landscape-scale. Here, we provide a landscape-scale assessment of the contribution of species richness, functional composition, temperature, and precipitation on grassland productivity. We found that the variation in grassland productivity during the growing season was best explained by functional trait composition. The community mean of plant preference for nutrients explained 24.8% of the variation in productivity and the community mean of specific leaf area explained 18.6%, while species richness explained only 2.4%. Temperature and precipitation explained an additional 22.1% of the variation in productivity. Our results indicate that functional trait composition is an important predictor of landscape-scale grassland productivity.

Contrasting responses of above- and below-ground herbivore communities along elevation.

Above- and below-ground herbivory are key ecosystem processes that can be substantially altered by environmental changes. However, direct comparisons of the coupled variations of above- and below-ground herbivore communities along elevation gradients remain sparse. Here, we studied the variation in assemblages of two dominant groups of herbivores, namely, aboveground orthoptera and belowground nematodes, in grasslands along six elevation gradients in the Swiss Alps. By examining variations of community properties of herbivores and their food plants along montane clines, we sought to determine whether the structure and functional properties of these taxonomic groups change with elevation. We found that orthoptera decreased in both species richness and abundance with elevation. In contrast with aboveground herbivores, the taxonomic richness and the total abundance of nematode did not covary with elevation. We further found a stronger shift in above- than below-ground functional properties along elevation, where the mandibular strength of orthoptera matched a shift in leaf toughness. Nematodes showed a weaker pattern of declined sedentary behavior and increased mobility with elevation. In contrast to the direct exposal of aboveground organisms to the surface climate, conditions may be buffered belowground, which together with the influence of edaphic factors on the biodiversity of soil biota, may explain the differences between elevational patterns of above- and below-ground communities. Our study emphasizes the necessity to consider both the above- and below-ground compartments to understand the impact of current and future climatic variation on ecosystems, from a functional perspective of species interactions.

Ecological constraints coupled with deep-time habitat dynamics predict the latitudinal diversity gradient in reef fishes.

We develop a spatially explicit model of diversification based on palaeohabitat to explore the predictions of four major hypotheses potentially explaining the latitudinal diversity gradient (LDG), namely, the 'time-area', 'tropical niche conservatism', 'ecological limits' and 'evolutionary speed' hypotheses. We compare simulation outputs to observed diversity gradients in the global reef fish fauna. Our simulations show that these hypotheses are non-mutually exclusive and that their relative influence depends on the time scale considered. Simulations suggest that reef habitat dynamics produced the LDG during deep geological time, while ecological constraints shaped the modern LDG, with a strong influence of the reduction in the latitudinal extent of tropical reefs during the Neogene. Overall, this study illustrates how mechanistic models in ecology and evolution can provide a temporal and spatial understanding of the role of speciation, extinction and dispersal in generating biodiversity patterns.

Areas of high conservation value at risk by plant invaders in Georgia under climate change.

Invasive alien plants (IAP) are a threat to biodiversity worldwide. Understanding and anticipating invasions allow for more efficient management. In this regard, predicting potential invasion risks by IAPs is essential to support conservation planning into areas of high conservation value (AHCV) such as sites exhibiting exceptional botanical richness, assemblage of rare, and threatened and/or endemic plant species. Here, we identified AHCV in Georgia, a country showing high plant richness, and assessed the susceptibility of these areas to colonization by IAPs under present and future climatic conditions. We used actual protected areas and areas of high plant endemism (identified using occurrences of 114 Georgian endemic plant species) as proxies for AHCV. Then, we assessed present and future potential distribution of 27 IAPs using species distribution models under four climate change scenarios and stacked single-species potential distribution into a consensus map representing IAPs richness. We evaluated present and future invasion risks in AHCV using IAPs richness as a metric of susceptibility. We show that the actual protected areas cover only 9.4% of the areas of high plant endemism in Georgia. IAPs are presently located at lower elevations around the large urban centers and in western Georgia. We predict a shift of IAPs toward eastern Georgia and higher altitudes and an increased susceptibility of AHCV to IAPs under future climate change. Our study provides a good baseline for decision makers and stakeholders on where and how resources should be invested in the most efficient way to protect Georgia's high plant richness from IAPs.

Plant physical and chemical defence variation along elevation gradients: a functional trait-based approach.

Predicting variation in plant functional traits related to anti-herbivore defences remains a major challenge in ecological research, considering that multiple traits have evolved in response to both abiotic and biotic conditions. Therefore, understanding variation in plant anti-herbivore defence traits requires studying their expression along steep environmental gradients, such as along elevation, where multiple biotic and abiotic factors co-vary. We expand on plant defence theory and propose a novel conceptual framework to address the sources of variations of plant resistance traits at the community level. We analysed elevation patterns of within-community trait dissimilarity using the RaoQ index, and the community-weighted-mean (CWM) index, on several plant functional traits: plant height, specific leaf area (SLA), leaf-dry-matter-content (LDMC), silicium content, presence of trichomes, carbon-to-nitrogen ratio (CN) and total secondary metabolite richness. We found that at high elevation, where harsh environmental conditions persist, community functional convergence is dictated by traits relating to plant growth (plant height and SLA), while divergence arises for traits relating resource-use (LDMC). At low elevation, where greater biotic pressure occurs, we found a combination of random (plant height), convergence (metabolite richness) and divergence patterns (silicium content). This framework thus combines community assembly rules of ecological filtering and niche partition with plant defence hypotheses to unravel the relationship between environmental variations, biotic pressure and the average phenotype of plants within a community.

Comparing spatial diversification and meta-population models in the Indo-Australian Archipelago.

Reconstructing the processes that have shaped the emergence of biodiversity gradients is critical to understand the dynamics of diversification of life on Earth. Islands have traditionally been used as model systems to unravel the processes shaping biological diversity. MacArthur and Wilson's island biogeographic model predicts diversity to be based on dynamic interactions between colonization and extinction rates, while treating islands themselves as geologically static entities. The current spatial configuration of islands should influence meta-population dynamics, but long-term geological changes within archipelagos are also expected to have shaped island biodiversity, in part by driving diversification. Here, we compare two mechanistic models providing inferences on species richness at a biogeographic scale: a mechanistic spatial-temporal model of species diversification and a spatial meta-population model. While the meta-population model operates over a static landscape, the diversification model is driven by changes in the size and spatial configuration of islands through time. We compare the inferences of both models to floristic diversity patterns among land patches of the Indo-Australian Archipelago. Simulation results from the diversification model better matched observed diversity than a meta-population model constrained only by the contemporary landscape. The diversification model suggests that the dynamic re-positioning of islands promoting land disconnection and reconnection induced an accumulation of particularly high species diversity on Borneo, which is central within the island network. By contrast, the meta-population model predicts a higher diversity on the mainlands, which is less compatible with empirical data. Our analyses highlight that, by comparing models with contrasting assumptions, we can pinpoint the processes that are most compatible with extant biodiversity patterns.

Responses of coral reef fishes to past climate changes are related to life-history traits.

Coral reefs and their associated fauna are largely impacted by ongoing climate change. Unravelling species responses to past climatic variations might provide clues on the consequence of ongoing changes. Here, we tested the relationship between changes in sea surface temperature and sea levels during the Quaternary and present-day distributions of coral reef fish species. We investigated whether species-specific responses are associated with life-history traits. We collected a database of coral reef fish distribution together with life-history traits for the Indo-Pacific Ocean. We ran species distribution models (SDMs) on 3,725 tropical reef fish species using contemporary environmental factors together with a variable describing isolation from stable coral reef areas during the Quaternary. We quantified the variance explained independently by isolation from stable areas in the SDMs and related it to a set of species traits including body size and mobility. The variance purely explained by isolation from stable coral reef areas on the distribution of extant coral reef fish species largely varied across species. We observed a triangular relationship between the contribution of isolation from stable areas in the SDMs and body size. Species, whose distribution is more associated with historical changes, occurred predominantly in the Indo-Australian archipelago, where the mean size of fish assemblages is the lowest. Our results suggest that the legacy of habitat changes of the Quaternary is still detectable in the extant distribution of many fish species, especially those with small body size and the most sedentary. Because they were the least able to colonize distant habitats in the past, fish species with smaller body size might have the most pronounced lags in tracking ongoing climate change.

Plate tectonics drive tropical reef biodiversity dynamics.

The Cretaceous breakup of Gondwana strongly modified the global distribution of shallow tropical seas reshaping the geographic configuration of marine basins. However, the links between tropical reef availability, plate tectonic processes and marine biodiversity distribution patterns are still unknown. Here, we show that a spatial diversification model constrained by absolute plate motions for the past 140 million years predicts the emergence and movement of diversity hotspots on tropical reefs. The spatial dynamics of tropical reefs explains marine fauna diversification in the Tethyan Ocean during the Cretaceous and early Cenozoic, and identifies an eastward movement of ancestral marine lineages towards the Indo-Australian Archipelago in the Miocene. A mechanistic model based only on habitat-driven diversification and dispersal yields realistic predictions of current biodiversity patterns for both corals and fishes. As in terrestrial systems, we demonstrate that plate tectonics played a major role in driving tropical marine shallow reef biodiversity dynamics.

Forecasted coral reef decline in marine biodiversity hotspots under climate change.

Coral bleaching events threaten coral reef habitats globally and cause severe declines of local biodiversity and productivity. Related to high sea surface temperatures (SST), bleaching events are expected to increase as a consequence of future global warming. However, response to climate change is still uncertain as future low-latitude climatic conditions have no present-day analogue. Sea surface temperatures during the Eocene epoch were warmer than forecasted changes for the coming century, and distributions of corals during the Eocene may help to inform models forecasting the future of coral reefs. We coupled contemporary and Eocene coral occurrences with information on their respective climatic conditions to model the thermal niche of coral reefs and its potential response to projected climate change. We found that under the RCP8.5 climate change scenario, the global suitability for coral reefs may increase up to 16% by 2100, mostly due to improved suitability of higher latitudes. In contrast, in its current range, coral reef suitability may decrease up to 46% by 2100. Reduction in thermal suitability will be most severe in biodiversity hotspots, especially in the Indo-Australian Archipelago. Our results suggest that many contemporary hotspots for coral reefs, including those that have been refugia in the past, spatially mismatch with future suitable areas for coral reefs posing challenges to conservation actions under climate change.