Unpunctual in diversity: The effect of stand species richness on spring phenology of deciduous tree stands varies among species and years.

Climatic drivers alone do not adequately explain the regional variation in budburst timing in deciduous forests across Europe. Stand-level factors, such as tree species richness, might affect budburst timing by creating different microclimates under the same site macroclimate. We assessed different phases of the spring phenology (start, midpoint, end, and overall duration of the budburst period) of four important European tree species (Betula pendula, Fagus sylvatica, Quercus robur and Tilia cordata) in monocultures and four-species mixture stands of a common garden tree biodiversity experiment in Belgium (FORBIO) in 2021 and 2022. Microclimatic differences between the stands in terms of bud chilling, temperature forcing, and soil temperature were considerable, with four-species mixtures being generally colder than monocultures in spring, but not in winter. In the colder spring of 2021, at the stand level, the end of the budburst period was advanced, and its overall duration shortened, in the four-species mixtures. At species level, this response was significant for F. sylvatica. In the warmer spring of 2022, advances in spring phenology in four-species stands were observed again in F. sylvatica and, less markedly, in B. pendula but without a general response at the stand level. Q. robur showed specific patterns with delayed budburst start in 2021 in the four-species mixtures and very short budburst duration for all stands in 2022. Phenological differences between monocultures and four-species mixtures were linked to microclimatic differences in light availability rather than in temperature as even comparatively colder microclimates showed an advanced phenology. Compared to weather conditions, tree species richness had a lower impact on budburst timing, but this impact can be of importance for key species like F. sylvatica and colder springs. These results indicate that forest biodiversity can affect budburst phenology, with wider implications, especially for forest- and land surface models.

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.

Biochemical composition changes can be linked to the tolerance of four grassland species under more persistent precipitation regimes.

Climate models suggest that the persistence of summer precipitation regimes (PRs) is on the rise, characterized by both longer dry and longer wet durations. These PR changes may alter plant biochemical composition and thereby their economic and ecological characteristics. However, impacts of PR persistence have primarily been studied at the community level, largely ignoring the biochemistry of individual species. Here, we analyzed biochemical components of four grassland species with varying sensitivity to PR persistence (Holcus lanatus, Phleum pratense, Lychnis flos-cuculi, Plantago lanceolata) along a range of increasingly persistent PRs (longer consecutive dry and wet periods) in a mesocosm experiment. The more persistent PRs decreased nonstructural sugars, whereas they increased lignin in all species, possibly reducing plant quality. The most sensitive species Lychnis seemed less capable of altering its biochemical composition in response to altered PRs, which may partly explain its higher sensitivity. The more tolerant species may have a more robust and dynamic biochemical network, which buffers the effects of changes in individual biochemical components on biomass. We conclude that the biochemical composition changes are important determinants for plant performance under increasingly persistent precipitation regimes.

Dispersal network heterogeneity promotes species coexistence in hierarchical competitive communities.

Understanding the mechanisms of biodiversity maintenance is a fundamental issue in ecology. The possibility that species disperse within the landscape along differing paths presents a relatively unexplored mechanism by which diversity could emerge. By embedding a classical metapopulation model within a network framework, we explore how access to different dispersal networks can promote species coexistence. While it is clear that species with the same demography cannot coexist stably on shared dispersal networks, we find that coexistence is possible on unshared networks, as species can surprisingly form self-organised clusters of occupied patches with the most connected patches at the core. Furthermore, a unimodal biodiversity response to an increase in species colonisation rates or average patch connectivity emerges in unshared networks. Increasing network size also increases species richness monotonically, producing characteristic species-area curves. This suggests that, in contrast to previous predictions, many more species can co-occur than the number of limiting resources.

The role of arbuscular mycorrhizal fungi in nonnative plant invasion along mountain roads.

Plant associated mutualists can mediate invasion success by affecting the ecological niche of nonnative plant species. Anthropogenic disturbance is also key in facilitating invasion success through changes in biotic and abiotic conditions, but the combined effect of these two factors in natural environments is understudied. To better understand this interaction, we investigated how disturbance and its interaction with mycorrhizas could impact range dynamics of nonnative plant species in the mountains of Norway. Therefore, we studied the root colonisation and community composition of arbuscular mycorrhizal (AM) fungi in disturbed vs undisturbed plots along mountain roads. We found that roadside disturbance strongly increases fungal diversity and richness while also promoting AM fungal root colonisation in an otherwise ecto-mycorrhiza and ericoid-mycorrhiza dominated environment. Surprisingly, AM fungi associating with nonnative plant species were present across the whole elevation gradient, even above the highest elevational limit of nonnative plants, indicating that mycorrhizal fungi are not currently limiting the upward movement of nonnative plants. We conclude that roadside disturbance has a positive effect on AM fungal colonisation and richness, possibly supporting the spread of nonnative plants, but that there is no absolute limitation of belowground mutualists, even at high elevation.

Risk of short-term biodiversity loss under more persistent precipitation regimes.

Recent findings indicate that atmospheric warming increases the persistence of weather patterns in the mid-latitudes, resulting in sequences of longer dry and wet periods compared to historic averages. The alternation of progressively longer dry and wet extremes could increasingly select for species with a broad environmental tolerance. As a consequence, biodiversity may decline. Here we explore the relationship between the persistence of summer precipitation regimes and plant diversity by subjecting experimental grassland mesocosms to a gradient of dry-wet alternation frequencies whilst keeping the total precipitation constant. The gradient varied the duration of consecutive wet and dry periods, from 1 up to 60 days with or without precipitation, over a total of 120 days. An alternation of longer dry and wet spells led to a severe loss of species richness (up to -75% relative to the current rainfall pattern in W-Europe) and functional diversity (enhanced dominance of grasses relative to nitrogen (N)-fixers and non-N-fixing forbs). Loss of N-fixers and non-N-fixing forbs in severe treatments was linked to lower baseline competitive success and higher physiological sensitivity to changes in soil moisture compared to grasses. The extent of diversity losses also strongly depended on the timing of the dry and wet periods. Regimes in which long droughts (≥20 days) coincided with above-average temperatures showed significantly more physiological plant stress over the experimental period, greater plant mortality, and impoverished communities by the end of the season. Across all regimes, the duration of the longest period below permanent wilting point was an accurate predictor of mortality across the communities, indicating that increasingly persistent precipitation regimes may reduce opportunities for drought stress alleviation. We conclude that without recruitment, which was precluded in this experiment, summer precipitation regimes with longer dry and wet spells will likely diminish plant diversity, at least in the short term.

Ecotrons: Powerful and versatile ecosystem analysers for ecology, agronomy and environmental science.

Ecosystems integrity and services are threatened by anthropogenic global changes. Mitigating and adapting to these changes require knowledge of ecosystem functioning in the expected novel environments, informed in large part through experimentation and modelling. This paper describes 13 advanced controlled environment facilities for experimental ecosystem studies, herein termed ecotrons, open to the international community. Ecotrons enable simulation of a wide range of natural environmental conditions in replicated and independent experimental units while measuring various ecosystem processes. This capacity to realistically control ecosystem environments is used to emulate a variety of climatic scenarios and soil conditions, in natural sunlight or through broad-spectrum lighting. The use of large ecosystem samples, intact or reconstructed, minimizes border effects and increases biological and physical complexity. Measurements of concentrations of greenhouse trace gases as well as their net exchange between the ecosystem and the atmosphere are performed in most ecotrons, often quasi continuously. The flow of matter is often tracked with the use of stable isotope tracers of carbon and other elements. Equipment is available for measurements of soil water status as well as root and canopy growth. The experiments ran so far emphasize the diversity of the hosted research. Half of them concern global changes, often with a manipulation of more than one driver. About a quarter deal with the impact of biodiversity loss on ecosystem functioning and one quarter with ecosystem or plant physiology. We discuss how the methodology for environmental simulation and process measurements, especially in soil, can be improved and stress the need to establish stronger links with modelling in future projects. These developments will enable further improvements in mechanistic understanding and predictive capacity of ecotron research which will play, in complementarity with field experimentation and monitoring, a crucial role in exploring the ecosystem consequences of environmental changes.

Fertilized graminoids intensify negative drought effects on grassland productivity.

Droughts can strongly affect grassland productivity and biodiversity, but responses differ widely. Nutrient availability may be a critical factor explaining this variation, but is often ignored in analyses of drought responses. Here, we used a standardized nutrient addition experiment covering 10 European grasslands to test if full-factorial nitrogen, phosphorus, and potassium addition affected plant community responses to inter-annual variation in drought stress and to the extreme summer drought of 2018 in Europe. We found that nutrient addition amplified detrimental drought effects on community aboveground biomass production. Drought effects also differed between functional groups, with a negative effect on graminoid but not forb biomass production. Our results imply that eutrophication in grasslands, which promotes dominance of drought-sensitive graminoids over forbs, amplifies detrimental drought effects. In terms of climate change adaptation, agricultural management would benefit from taking into account differential drought impacts on fertilized versus unfertilized grasslands, which differ in ecosystem services they provide to society.

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.

Invader presence disrupts the stabilizing effect of species richness in plant community recovery after drought.

Higher biodiversity can stabilize the productivity and functioning of grassland communities when subjected to extreme climatic events. The positive biodiversity-stability relationship emerges via increased resistance and/or recovery to these events. However, invader presence might disrupt this diversity-stability relationship by altering biotic interactions. Investigating such disruptions is important given that invasion by non-native species and extreme climatic events are expected to increase in the future due to anthropogenic pressure. Here we present one of the first multisite invader × biodiversity × drought manipulation experiment to examine combined effects of biodiversity and invasion on drought resistance and recovery at three semi-natural grassland sites across Europe. The stability of biomass production to an extreme drought manipulation (100% rainfall reduction; BE: 88 days, BG: 85 days, DE: 76 days) was quantified in field mesocosms with a richness gradient of 1, 3, and 6 species and three invasion treatments (no invader, Lupinus polyphyllus, Senecio inaequidens). Our results suggest that biodiversity stabilized community productivity by increasing the ability of native species to recover from extreme drought events. However, invader presence turned the positive and stabilizing effects of diversity on native species recovery into a neutral relationship. This effect was independent of the two invader's own capacity to recover from an extreme drought event. In summary, we found that invader presence may disrupt how native community interactions lead to stability of ecosystems in response to extreme climatic events. Consequently, the interaction of three global change drivers, climate extremes, diversity decline, and invasive species, may exacerbate their effects on ecosystem functioning.

Disturbance is the key to plant invasions in cold environments.

Until now, nonnative plant species were rarely found at high elevations and latitudes. However, partly because of climate warming, biological invasions are now on the rise in these extremely cold environments. These plant invasions make it timely to undertake a thorough experimental assessment of what has previously been holding them back. This knowledge is key to developing efficient management of the increasing risks of cold-climate invasions. Here, we integrate human interventions (i.e., disturbance, nutrient addition, and propagule input) and climatic factors (i.e., temperature) into one seed-addition experiment across two continents: the subantarctic Andes and subarctic Scandinavian mountains (Scandes), to disentangle their roles in limiting or favoring plant invasions. Disturbance was found as the main determinant of plant invader success (i.e., establishment, growth, and flowering) along the entire cold-climate gradient, explaining 40-60% of the total variance in our models, with no indication of any facilitative effect from the native vegetation. Higher nutrient levels additionally stimulated biomass production and flowering. Establishment and flowering displayed a hump-shaped response with increasing elevation, suggesting that competition is the main limit on invader success at low elevations, as opposed to low-growing-season temperatures at high elevations. Our experiment showed, however, that nonnative plants can establish, grow, and flower well above their current elevational limits in high-latitude mountains. We thus argue that cold-climate ecosystems are likely to see rapid increases in plant invasions in the near future as a result of a synergistic interaction between increasing human-mediated disturbances and climate warming.

Dynamics of metabolic responses to periods of combined heat and drought in Arabidopsis thaliana under ambient and elevated atmospheric CO2.

As a consequence of global change processes, plants will increasingly be challenged by extreme climatic events, against a background of elevated atmospheric CO2. We analysed responses of Arabidopsis thaliana to periods of a combination of elevated heat and water deficit at ambient and elevated CO2 in order to gain mechanistic insights regarding changes in primary metabolism. Metabolic changes induced by extremes of climate are dynamic and specific to different classes of molecules. Concentrations of soluble sugars and amino acids increased transiently after short (4-d) exposure to heat and drought, and readjusted to control levels under prolonged (8-d) stress. In contrast, fatty acids showed persistent changes during the stress period. Elevated CO2 reduced the impact of stress on sugar and amino acid metabolism, but not on fatty acids. Integrating metabolite data with transcriptome results revealed that some of the metabolic changes were regulated at the transcriptional level. Multivariate analyses grouped metabolites on the basis of stress exposure time, indicating specificity in metabolic responses to short and prolonged stress. Taken together, the results indicate that dynamic metabolic reprograming plays an important role in plant acclimation to climatic extremes. The extent of such metabolic adjustments is less under high CO2, further pointing towards the role of high CO2 in stress mitigation.

Species richness effects on grassland recovery from drought depend on community productivity in a multisite experiment.

Biodiversity can buffer ecosystem functioning against extreme climatic events, but few experiments have explicitly tested this. Here, we present the first multisite biodiversity × drought manipulation experiment to examine drought resistance and recovery at five temperate and Mediterranean grassland sites. Aboveground biomass production declined by 30% due to experimental drought (standardised local extremity by rainfall exclusion for 72-98 consecutive days). Species richness did not affect resistance but promoted recovery. Recovery was only positively affected by species richness in low-productive communities, with most diverse communities even showing overcompensation. This positive diversity effect could be linked to asynchrony of species responses. Our results suggest that a more context-dependent view considering the nature of the climatic disturbance as well as the productivity of the studied system will help identify under which circumstances biodiversity promotes drought resistance or recovery. Stability of biomass production can generally be expected to decrease with biodiversity loss and climate change.

Robustness of metacommunities with omnivory to habitat destruction: disentangling patch fragmentation from patch loss.

Habitat destruction, characterized by patch loss and fragmentation, is a major driving force of species extinction, and understanding its mechanisms has become a central issue in biodiversity conservation. Numerous studies have explored the effect of patch loss on food web dynamics, but ignored the critical role of patch fragmentation. Here we develop an extended patch-dynamic model for a tri-trophic omnivory system with trophic-dependent dispersal in fragmented landscapes. We found that species display different vulnerabilities to both patch loss and fragmentation, depending on their dispersal range and trophic position. The resulting trophic structure varies depending on the degree of habitat loss and fragmentation, due to a tradeoff between bottom-up control on omnivores (dominated by patch loss) and dispersal limitation on intermediate consumers (dominated by patch fragmentation). Overall, we find that omnivory increases system robustness to habitat destruction relative to a simple food chain.

Coexistence of species with different dispersal across landscapes: a critical role of spatial correlation in disturbance.

Disturbance is key to maintaining species diversity in plant communities. Although the effects of disturbance frequency and extent on species diversity have been studied, we do not yet have a mechanistic understanding of how these aspects of disturbance interact with spatial structure of disturbance to influence species diversity. Here we derive a novel pair approximation model to explore competitive outcomes in a two-species system subject to spatially correlated disturbance. Generally, spatial correlation in disturbance favoured long-range dispersers, while distance-limited dispersers were greatly suppressed. Interestingly, high levels of spatial aggregation of disturbance promoted long-term species coexistence that is not possible in the absence of disturbance, but only when the local disperser was intrinsically competitively superior. However, spatial correlation in disturbance led to different competitive outcomes, depending on the disturbed area. Concerning ecological conservation and management, we theoretically demonstrate that introducing a spatially correlated disturbance to the system or altering an existing disturbance regime can be a useful strategy either to control species invasion or to promote species coexistence. Disturbance pattern analysis may therefore provide new insights into biodiversity conservation.

Three times greater weight of daytime than of night-time temperature on leaf unfolding phenology in temperate trees.

The phenology of spring leaf unfolding plays a key role in the structure and functioning of ecosystems. The classical concept of heat requirement (growing degree days) for leaf unfolding was developed hundreds of years ago, but this model does not include the recently reported greater importance of daytime than night-time temperature. A manipulative experiment on daytime vs night-time warming with saplings of three species of temperate deciduous trees was conducted and a Bayesian method was applied to explore the different effects of daytime and night-time temperatures on spring phenology. We found that both daytime and night-time warming significantly advanced leaf unfolding, but the sensitivities to increased daytime and night-time temperatures differed significantly. Trees were most sensitive to daytime warming (7.4 ± 0.9, 4.8 ± 0.3 and 4.8 ± 0.2 d advancement per degree Celsius warming (d °C-1 ) for birch, oak and beech, respectively) and least sensitive to night-time warming (5.5 ± 0.9, 3.3 ± 0.3 and 2.1 ± 0.9 d °C-1 ). Interestingly, a Bayesian analysis found that the impact of daytime temperature on leaf unfolding was approximately three times higher than that of night-time temperatures. Night-time global temperature is increasing faster than daytime temperature, so model projections of future spring phenology should incorporate the effects of these different temperatures.

Physiological, biochemical, and genome-wide transcriptional analysis reveals that elevated CO2 mitigates the impact of combined heat wave and drought stress in Arabidopsis thaliana at multiple organizational levels.

Climate changes increasingly threaten plant growth and productivity. Such changes are complex and involve multiple environmental factors, including rising CO2 levels and climate extreme events. As the molecular and physiological mechanisms underlying plant responses to realistic future climate extreme conditions are still poorly understood, a multiple organizational level analysis (i.e. eco-physiological, biochemical, and transcriptional) was performed, using Arabidopsis exposed to incremental heat wave and water deficit under ambient and elevated CO2 . The climate extreme resulted in biomass reduction, photosynthesis inhibition, and considerable increases in stress parameters. Photosynthesis was a major target as demonstrated at the physiological and transcriptional levels. In contrast, the climate extreme treatment induced a protective effect on oxidative membrane damage, most likely as a result of strongly increased lipophilic antioxidants and membrane-protecting enzymes. Elevated CO2 significantly mitigated the negative impact of a combined heat and drought, as apparent in biomass reduction, photosynthesis inhibition, chlorophyll fluorescence decline, H2 O2 production, and protein oxidation. Analysis of enzymatic and molecular antioxidants revealed that the stress-mitigating CO2 effect operates through up-regulation of antioxidant defense metabolism, as well as by reduced photorespiration resulting in lowered oxidative pressure. Therefore, exposure to future climate extreme episodes will negatively impact plant growth and production, but elevated CO2 is likely to mitigate this effect.

Can permanent grassland soils with elevated organic carbon buffer negative effects of more persistent precipitation regimes on forage grass performance?

Agricultural practices enhancing soil organic carbon (SOC) show potential to buffer negative effects of climate change on forage grass performance. We tested this by subjecting five forage grass varieties differing in fodder quality and drought/flooding resistance to increased persistence in summer precipitation regimes (PR) across sandy and sandy-loam soils from either permanent (high SOC) or temporary grasslands (low SOC) in adjacent parcels. Over the course of two consecutive summers, monoculture mesocosms were subjected to rainy/dry weather alternation either every 3 days or every 30 days, whilst keeping total precipitation equal. Increased PR persistence induced species-specific drought damage and productivity declines. Soils from permanent grasslands with elevated SOC buffered plant quality, but buffering effects of SOC on drought damage, nutrient availability and yield differed between texture classes. In the more persistent PR, Festuca arundinacea FERMINA was the most productive species but had the lowest quality under both ample water supply and mild soil drought, whilst under the most intense soil droughts, Festulolium FESTILO maintained the highest yields. The hybrid Lolium × boucheanum kunth MELCOMBI had intermediate productivity and both Lolium perenne varieties showed the lowest yields under soil drought, but the highest forage quality (especially the tetraploid variety MELFORCE). Performance varied with plant maturity stage and across seasons/years and was driven by altered water and nutrient availability and related nitrogen nutrition among species during drought and upon rewetting. Moreover, whilst permanent grassland soils showed the most consistent positive effects on plant performance, their available water capacity also declined under increased PR persistence. We conclude that permanent grassland soils with historically elevated SOC likely buffer negative effects of increasing summer weather persistence on forage grass performance, but may also be more sensitive to degradation under climate change.

Species persistence in landscapes with spatial variation in habitat quality: a pair approximation model.

Habitat degradation has become a major threat to species persistence. Although several models have explicitly integrated habitat quality into metapopulation dynamics, we still lack knowledge of the spatial variability of species persistence which may result from the clustering of habitat patches of differing quality. Here we construct both pair approximation (PA) and cellular automaton (CA) models for species persistence in homogeneous versus heterogeneous landscapes. Heterogeneous landscapes are generated by varying the orthogonal-neighbour correlation between two different-quality habitats. In our simulations, the PA model exhibits similar population dynamics to the CA model, though it overestimates species persistence due to the doublet approximation neglecting correlation beyond nearest neighbours. Generally, landscape heterogeneity enhances species persistence relative to landscape homogeneity, especially with enlarging habitat-quality difference. This indicates that models based on homogeneous landscapes may overestimate species extinction rate. In heterogeneous landscapes, habitat clumping does not influence global dispersers because of random establishment, although it does promote the persistence of local dispersers, especially under severe habitat degradation. However, habitat configurational fragmentation improves the persistence of global dispersers that are highly sensitive to local crowding, probably by reducing density dependence, but this positive fragmentation effect on local dispersers is overshadowed by the stronger negative border effect on impeding local extension. Furthermore, increasing density dependence promotes the extinction risk of local dispersers, while global dispersers are not influenced. For conservation and habitat management, our results suggest that minimising random anthropogenic disturbance should take priority over increasing the connectivity of good-quality habitat, as random habitat degradation poses a more serious threat to species persistence than clustered habitat degradation. Owing to species' diverse responses to habitat configurational fragmentation, landscapes with different properties may accommodate different species.