Plant choice between arbuscular mycorrhizal fungal species results in increased plant P acquisition.

Arbuscular mycorrhizal fungi (AMF) are plant root symbionts that provide phosphorus (P) to plants in exchange for photosynthetically fixed carbon (C). Previous research has shown that plants-given a choice among AMF species-may preferentially allocate C to AMF species that provide more P. However, these investigations rested on a limited set of plant and AMF species, and it therefore remains unclear how general this phenomenon is. Here, we combined 4 plant and 6 AMF species in 24 distinct plant-AMF species compositions in split-root microcosms, manipulating the species identity of AMF in either side of the root system. Using 14C and 32P/33P radioisotope tracers, we tracked the transfer of C and P between plants and AMF, respectively. We found that when plants had a choice of AMF species, AMF species which transferred more P acquired more C. Evidence for preferential C allocation to more beneficial AMF species within individual plant roots was equivocal. However, AMF species which transferred more P to plants did so at lower C-to-P ratios, highlighting the importance both of absolute and relative costs of P acquisition from AMF. When plants had a choice of AMF species, their shoots contained a larger total amount of P at higher concentrations. Our results thus highlight the benefits of plant C choice among AMF for plant P acquisition.

Experimental erosion of microbial diversity decreases soil CH4 consumption rates.

Biodiversity-ecosystem functioning (BEF) experiments have predominantly focused on communities of higher organisms, in particular plants, with comparably little known to date about the relevance of biodiversity for microbially driven biogeochemical processes. Methanotrophic bacteria play a key role in Earth's methane (CH4 ) cycle by removing atmospheric CH4 and reducing emissions from methanogenesis in wetlands and landfills. Here, we used a dilution-to-extinction approach to simulate diversity loss in a methanotrophic landfill cover soil community. Replicate samples were diluted 101 -107 -fold, preincubated under a high CH4 atmosphere for microbial communities to recover to comparable size, and then incubated for 86 days at constant or diurnally cycling temperature. We hypothesize that (1) CH4 consumption decreases as methanotrophic diversity is lost, and (2) this effect is more pronounced under variable temperatures. Net CH4 consumption was determined by gas chromatography. Microbial community composition was determined by DNA extraction and sequencing of amplicons specific to methanotrophs and bacteria (pmoA and 16S gene fragments). The richness of operational taxonomic units (OTU) of methanotrophic and nonmethanotrophic bacteria decreased approximately linearly with log-dilution. CH4 consumption decreased with the number of OTUs lost, independent of community size. These effects were independent of temperature cycling. The diversity effects we found occured in relatively diverse communities, challenging the notion of high functional redundancy mediating high resistance to diversity erosion in natural microbial systems. The effects also resemble the ones for higher organisms, suggesting that BEF relationships are universal across taxa and spatial scales.

Single-gene resolution of diversity-driven overyielding in plant genotype mixtures.

In plant communities, diversity often increases productivity and functioning, but the specific underlying drivers are difficult to identify. Most ecological theories attribute positive diversity effects to complementary niches occupied by different species or genotypes. However, the specific nature of niche complementarity often remains unclear, including how it is expressed in terms of trait differences between plants. Here, we use a gene-centred approach to study positive diversity effects in mixtures of natural Arabidopsis thaliana genotypes. Using two orthogonal genetic mapping approaches, we find that between-plant allelic differences at the AtSUC8 locus are strongly associated with mixture overyielding. AtSUC8 encodes a proton-sucrose symporter and is expressed in root tissues. Genetic variation in AtSUC8 affects the biochemical activities of protein variants and natural variation at this locus is associated with different sensitivities of root growth to changes in substrate pH. We thus speculate that - in the particular case studied here - evolutionary divergence along an edaphic gradient resulted in the niche complementarity between genotypes that now drives overyielding in mixtures. Identifying genes important for ecosystem functioning may ultimately allow linking ecological processes to evolutionary drivers, help identify traits underlying positive diversity effects, and facilitate the development of high-performance crop variety mixtures.

A spatial fingerprint of land-water linkage of biodiversity uncovered by remote sensing and environmental DNA.

Aquatic and terrestrial ecosystems are tightly connected via spatial flows of organisms and resources. Such land-water linkages integrate biodiversity across ecosystems and suggest a spatial association of aquatic and terrestrial biodiversity. However, knowledge about the extent of this spatial association is limited. By combining satellite remote sensing (RS) and environmental DNA (eDNA) extraction from river water across a 740-km2 mountainous catchment, we identify a characteristic spatial land-water fingerprint. Specifically, we find a spatial association of riverine eDNA diversity with RS spectral diversity of terrestrial ecosystems upstream, peaking at a 400 m distance yet still detectable up to a 2.0 km radius. Our findings show that biodiversity patterns in rivers can be linked to the functional diversity of surrounding terrestrial ecosystems and provide a dominant scale at which these linkages are strongest. Such spatially explicit information is necessary for a functional understanding of land-water linkages.

From lab to field: biological control of the Japanese beetle with entomopathogenic fungi.

The Japanese beetle, Popillia japonica, is an invasive scarab and listed as quarantine organism in many countries worldwide. Native to Japan, it has invaded North America, the Azores, and recently mainland Europe. Adults are gregarious and cause agricultural and horticultural losses by feeding on leaves, fruits, and flowers of a wide range of crops and ornamental plants. Larvae feed belowground and damage grassland. To date, no efficient and environmentally friendly control measure is available. Larval populations of other scarab species such as Phyllopertha horticola and Melolontha melolontha are controlled by applying spores of the entomopathogenic fungi Metarhizium brunneum and Beauveria brongniartii to larval habitats. Here, we tested this control strategy against Japanese beetle larvae in grasslands, as well as spore spray applications against adults in crops. Using both, large-scale field experiments and inoculation experiments in the laboratory, we assess the efficacy of registered fungal strains against Japanese beetle larvae and adults. Metarhizium brunneum BIPESCO 5 established and persisted in the soil of larval habitats and on the leaves of adult's host plants after application. However, neither larval nor adult population sizes were reduced at the study sites. Laboratory experiments showed that larvae are not susceptible to M. brunneum ART 212, M. brunneum BIPESCO 5, and B. brongniartii BIPESCO 2. In contrast, adults were highly susceptible to all three strains. When blastospores were directly injected into the hemolymph, both adults and larvae showed elevated mortality rates, which suggests that the cuticle plays an important role in determining the difference in susceptibility of the two life stages. In conclusion, we do not see potential in adapting the state-of-the-art control strategy against native scarabs to Japanese beetle larvae. However, adults are susceptible to the tested entomopathogenic fungi in laboratory settings and BIPESCO 5 conidiospores survived for more than three weeks in the field despite UV-radiation and elevated temperatures. Hence, control of adults using fungi of the genera Beauveria or Metarhizium is more promising than larval control. Further research on efficient application methods and more virulent and locally adapted fungal strains will help to increase efficacy of fungal treatments for the control of P. japonica.

Increasing plant group productivity through latent genetic variation for cooperation.

Historic yield advances in the major crops have, to a large extent, been achieved by selection for improved productivity of groups of plant individuals such as high-density stands. Research suggests that such improved group productivity depends on "cooperative" traits (e.g., erect leaves, short stems) that-while beneficial to the group-decrease individual fitness under competition. This poses a problem for some traditional breeding approaches, especially when selection occurs at the level of individuals, because "selfish" traits will be selected for and reduce yield in high-density monocultures. One approach, therefore, has been to select individuals based on ideotypes with traits expected to promote group productivity. However, this approach is limited to architectural and physiological traits whose effects on growth and competition are relatively easy to anticipate. Here, we developed a general and simple method for the discovery of alleles promoting cooperation in plant stands. Our method is based on the game-theoretical premise that alleles increasing cooperation benefit the monoculture group but are disadvantageous to the individual when facing noncooperative neighbors. Testing the approach using the model plant Arabidopsis thaliana, we found a major effect locus where the rarer allele was associated with increased cooperation and productivity in high-density stands. The allele likely affects a pleiotropic gene, since we find that it is also associated with reduced root competition but higher resistance against disease. Thus, even though cooperation is considered evolutionarily unstable except under special circumstances, conflicting selective forces acting on a pleiotropic gene might maintain latent genetic variation for cooperation in nature. Such variation, once identified in a crop, could rapidly be leveraged in modern breeding programs and provide efficient routes to increase yields.

Effects of enemy exclusion on biodiversity-productivity relationships in a subtropical forest experiment.

Interspecific niche complementarity is a key mechanism posited to explain positive species richness-productivity relationships in plant communities. However, the exact nature of the niche dimensions that plant species partition remains poorly known.Species may partition abiotic resources that limit their growth, but species may also be specialized with respect to their set of biotic interactions with other trophic levels, in particular with enemies including pathogens and consumers. The lower host densities present in more species-diverse plant communities may therefore result in smaller populations of specialized enemies, and in a smaller associated negative feedback these enemies exert on plant productivity.To test whether such host density-dependent effects of enemies drive diversity-productivity relationships in young forest stands, we experimentally manipulated leaf fungal pathogens and insect herbivores in a large subtropical forest biodiversity-ecosystem functioning experiment in China (BEF-China).We found that fungicide spraying of tree canopies removed the positive tree-species richness-productivity relationship present in untreated control plots. The tree species that contributed the most to this effect were the ones with the highest fungicide-induced growth increase in monoculture. Insecticide application did not cause comparable effects. Synthesis. Our findings suggest that tree species diversity may not only promote productivity by interspecific resource-niche partitioning but also by trophic niche partitioning. Most likely, partitioning occurred with respect to enemies such as pathogenic fungi. Alternatively, similar effects on tree growth would have occurred if fungicide had eliminated positive effects of a higher diversity of beneficial fungi (e.g. mycorrhizal symbionts) that may have occurred in mixed tree species communities.

Remotely sensed between-individual functional trait variation in a temperate forest.

Trait-based ecology holds the promise to explain how plant communities work, for example, how functional diversity may support community productivity. However, so far it has been difficult to combine field-based approaches assessing traits at the level of plant individuals with limited spatial coverage and approaches using remote sensing (RS) with complete spatial coverage but assessing traits at the level of vegetation pixels rather than individuals. By delineating all individual-tree crowns within a temperate forest site and then assigning RS-derived trait measures to these trees, we combine the two approaches, allowing us to use general linear models to estimate the influence of taxonomic or environmental variation on between- and within-species variation across contiguous space.We used airborne imaging spectroscopy and laser scanning to collect individual-tree RS data from a mixed conifer-angiosperm forest on a mountain slope extending over 5.5 ha and covering large environmental gradients in elevation as well as light and soil conditions. We derived three biochemical (leaf chlorophyll, carotenoids, and water content) and three architectural traits (plant area index, foliage-height diversity, and canopy height), which had previously been used to characterize plant function, from the RS data. We then quantified the contributions of taxonomic and environmental variation and their interaction to trait variation and partitioned the remaining within-species trait variation into smaller-scale spatial and residual variation. We also investigated the correlation between functional trait and phylogenetic distances at the between-species level. The forest consisted of 13 tree species of which eight occurred in sufficient abundance for quantitative analysis.On average, taxonomic variation between species accounted for more than 15% of trait variation in biochemical traits but only around 5% (still highly significant) in architectural traits. Biochemical trait distances among species also showed a stronger correlation with phylogenetic distances than did architectural trait distances. Light and soil conditions together with elevation explained slightly more variation than taxonomy across all traits, but in particular increased plant area index (light) and reduced canopy height (elevation). Except for foliage-height diversity, all traits were affected by significant interactions between taxonomic and environmental variation, the different responses of the eight species to the within-site environmental gradients potentially contributing to the coexistence of the eight abundant species.We conclude that with high-resolution RS data it is possible to delineate individual-tree crowns within a forest and thus assess functional traits derived from RS data at individual level. With this precondition fulfilled, it is then possible to apply tools commonly used in field-based trait ecology to partition trait variation among individuals into taxonomic and potentially even genetic variation, environmental variation, and interactions between the two. The method proposed here presents a promising way of assessing individual-based trait information with complete spatial coverage and thus allowing analysis of functional diversity at different scales. This information can help to better understand processes shaping community structure, productivity, and stability of forests.

Ecological and evolutionary approaches to improving crop variety mixtures.

Variety mixtures can provide a range of benefits for both the crop and the environment. Their utility for the suppression of pathogens, especially in small grain crops, is well established and has seen some remarkable successes. However, despite decades of academic interest in the topic, commercial efforts to develop, release and promote variety mixtures remain peripheral to normal breeding activities. Here we argue that this is because simple but general design principles that allow for the optimization of multiple mixture benefits are currently lacking. We therefore review the practical and conceptual challenges inherent in the development of variety mixtures, and discuss common approaches to overcome these. We further consider three domains in which they might be particularly beneficial: pathogen resistance, yield stability and yield enhancement. We demonstrate that combining evolutionary and ecological concepts with data typically available from breeding and variety testing programmes could make mixture development easier and more economic. Identifying synergies between the breeding for monocultures and mixtures may even be key to the widespread adoption of mixtures-to the profit of breeders, farmers and society as a whole.

Plant traits alone are poor predictors of ecosystem properties and long-term ecosystem functioning.

Earth is home to over 350,000 vascular plant species that differ in their traits in innumerable ways. A key challenge is to predict how natural or anthropogenically driven changes in the identity, abundance and diversity of co-occurring plant species drive important ecosystem-level properties such as biomass production or carbon storage. Here, we analyse the extent to which 42 different ecosystem properties can be predicted by 41 plant traits in 78 experimentally manipulated grassland plots over 10 years. Despite the unprecedented number of traits analysed, the average percentage of variation in ecosystem properties jointly explained was only moderate (32.6%) within individual years, and even much lower (12.7%) across years. Most other studies linking ecosystem properties to plant traits analysed no more than six traits and, when including only six traits in our analysis, the average percentage of variation explained in across-year levels of ecosystem properties dropped to 4.8%. Furthermore, we found on average only 12.2% overlap in significant predictors among ecosystem properties, indicating that a small set of key traits able to explain multiple ecosystem properties does not exist. Our results therefore suggest that there are specific limits to the extent to which traits per se can predict the long-term functional consequences of biodiversity change, so that data on additional drivers, such as interacting abiotic factors, may be required to improve predictions of ecosystem property levels.

Local and landscape-level diversity effects on forest functioning.

Research of the past decades has shown that biodiversity is a fundamental driver of ecosystem functioning. However, most of this biodiversity-ecosystem functioning (BEF) research focused on experimental communities on small areas where environmental context was held constant. Whether the established BEF relationships also apply to natural or managed ecosystems that are embedded in variable landscape contexts remains unclear. In this study, we therefore investigated biodiversity effects on ecosystem functions in 36 forest stands that were located across a vast range of environmental conditions in managed landscapes of Central Europe (Switzerland). Specifically, we approximated forest productivity by leaf area index and forest phenology by growing-season length and tested effects of tree species richness and land-cover richness on these variables. We then examined the correlation and the confounding of these local and landscape-level diversity effects with environmental context variables related to forest stand structure (number of trees), landscape structure (land-cover edge density), climate (annual precipitation) and topography (mean altitude). We found that of all tested variables tree species richness was among the most important determinants of forest leaf area index and growing-season length. The positive effects of tree species richness on these two ecosystem variables were remarkably consistent across the different environmental conditions we investigated and we found little evidence of a context-dependent change in these biodiversity effects. Land-cover richness was not directly related to local forest functions but could nevertheless play a role via a positive effect on tree species richness.

Late-spring frost risk between 1959 and 2017 decreased in North America but increased in Europe and Asia.

Late-spring frosts (LSFs) affect the performance of plants and animals across the world's temperate and boreal zones, but despite their ecological and economic impact on agriculture and forestry, the geographic distribution and evolutionary impact of these frost events are poorly understood. Here, we analyze LSFs between 1959 and 2017 and the resistance strategies of Northern Hemisphere woody species to infer trees' adaptations for minimizing frost damage to their leaves and to forecast forest vulnerability under the ongoing changes in frost frequencies. Trait values on leaf-out and leaf-freezing resistance come from up to 1,500 temperate and boreal woody species cultivated in common gardens. We find that areas in which LSFs are common, such as eastern North America, harbor tree species with cautious (late-leafing) leaf-out strategies. Areas in which LSFs used to be unlikely, such as broad-leaved forests and shrublands in Europe and Asia, instead harbor opportunistic tree species (quickly reacting to warming air temperatures). LSFs in the latter regions are currently increasing, and given species' innate resistance strategies, we estimate that ∼35% of the European and ∼26% of the Asian temperate forest area, but only ∼10% of the North American, will experience increasing late-frost damage in the future. Our findings reveal region-specific changes in the spring-frost risk that can inform decision-making in land management, forestry, agriculture, and insurance policy.

Author Correction: Directed species loss reduces community productivity in a subtropical forest biodiversity experiment.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Directed species loss reduces community productivity in a subtropical forest biodiversity experiment.

Unprecedented species loss in diverse forests indicates the urgent need to test its consequences for ecosystem functioning. However, experimental evaluation based on realistic extinction scenarios is lacking. Using species interaction networks we introduce an approach to separate effects of node loss (reduced species number) from effects of link loss or compensation (reduced or increased interspecific interactions) on ecosystem functioning along directed extinction scenarios. By simulating random and non-random extinction scenarios in an experimental subtropical Chinese forest, we find that species loss is detrimental for stand volume in all scenarios, and that these effects strengthen with age. However, the magnitude of these effects depends on the type of attribute on which the directed species loss is based, with preferential loss of evolutionarily distinct species and those from small families having stronger effects than those that are regionally rare or have high specific leaf area. These impacts were due to both node loss and link loss or compensation. At high species richness (reductions from 16 to 8 species), strong stand-volume reduction only occurred in directed but not random extinction. Our results imply that directed species loss can severely hamper productivity in already diverse young forests.

Terrestrial land-cover type richness is positively linked to landscape-level functioning.

Biodiversity-ecosystem functioning (BEF) experiments have shown that local species richness promotes ecosystem functioning and stability. Whether this also applies under real-world conditions is still debated. Here, we focus on larger scales of space, time and ecological organization. We develop a quasi-experimental design in which we relate land-cover type richness as measure of landscape richness to 17-year time series of satellite-sensed functioning in 4974 landscape plots 6.25 or 25 ha in size. We choose plots so that landscape richness is orthogonal to land cover-type composition and environmental conditions across climatic gradients. Landscape-scale productivity and temporal stability increase with landscape richness, irrespective of landscape plot size. Peak season near-infrared surface albedo, which is relevant for surface energy budgets, is higher in mixed than in single land-cover type landscapes. Effect sizes are as large as those reported from BEF-experiments, suggesting that landscape richness promotes landscape functioning at spatial scales relevant for management.

Tree-species interactions increase light absorption and growth in Chinese subtropical mixed-species plantations.

Light-related interactions can increase productivity in tree-species mixtures compared with monocultures due to higher stand-level absorption of photosynthetically active radiation (APAR) or light-use efficiency (LUE). However, the effects of different light-related interactions, and their relative importance, have rarely been quantified. Here, measurements of vertical leaf-area distributions, tree sizes, and stand density were combined with a tree-level light model (Maestra) to examine how crown architecture and vertical or horizontal canopy structure influence the APAR of 16 monocultures and eight different two-species mixtures with 16 different species in a Chinese subtropical tree diversity experiment. A higher proportion of crown leaf area occurred in the upper crowns of species with higher specific leaf areas. Tree-level APAR depended largely on tree leaf area and also, but to a lesser extent, on relative height (i.e., tree dominance) and leaf-area index (LAI). Stand-level APAR depended on LAI and canopy volume, but not on the vertical stratification or canopy leaf-area density. The mixing effects, in terms of relative differences between mixtures and monocultures, on stand-level APAR were correlated with the mixing effects on basal area growth, indicating that light-related interactions may have been responsible for part of the mixing effects on basal area growth. While species identity influences the vertical distributions of leaf area within tree crowns, this can have a relatively small effect on tree and stand APAR compared with the size and vertical positioning of the crowns, or the LAI and canopy volume.

Globally consistent influences of seasonal precipitation limit grassland biomass response to elevated CO2.

Rising atmospheric carbon dioxide concentration should stimulate biomass production directly via biochemical stimulation of carbon assimilation, and indirectly via water savings caused by increased plant water-use efficiency. Because of these water savings, the CO2 fertilization effect (CFE) should be stronger at drier sites, yet large differences among experiments in grassland biomass response to elevated CO2 appear to be unrelated to annual precipitation, preventing useful generalizations. Here, we show that, as predicted, the impact of elevated CO2 on biomass production in 19 globally distributed temperate grassland experiments reduces as mean precipitation in seasons other than spring increases, but that it rises unexpectedly as mean spring precipitation increases. Moreover, because sites with high spring precipitation also tend to have high precipitation at other times, these effects of spring and non-spring precipitation on the CO2 response offset each other, constraining the response of ecosystem productivity to rising CO2. This explains why previous analyses were unable to discern a reliable trend between site dryness and the CFE. Thus, the CFE in temperate grasslands worldwide will be constrained by their natural rainfall seasonality such that the stimulation of biomass by rising CO2 could be substantially less than anticipated.

Response to Comment on "Impacts of species richness on productivity in a large-scale subtropical forest experiment".

Yang et al have raised criticism that the results reported by us would not be relevant for natural forests. We argue that productivity is positively related to species richness also in subtropical natural forests, and that both the species pools and the range of tree species richness used in our experiment are representative of many natural forests of this biome.

Effects of plant productivity and species richness on the drought response of soil respiration in temperate grasslands.

Soil respiration plays a crucial role in global carbon cycling. While the response of soil respiration to abiotic drivers like soil temperature and moisture is fairly well understood, less is known about the effects of biotic drivers, such as plant above- and belowground productivity or plant diversity, and their interactions with abiotic drivers on soil respiration. Thus, current predictions of soil respiration to summer droughts might miss relevant biological drivers and their interactions with abiotic drivers. Since drought events are expected to increase in Central Europe in the future, we simulated early summer drought using rainout shelters at 19 grassland sites, which differed in plant productivity and species richness in central Germany in 2002 and 2003. We tested the potentially interacting effects of drought with biotic drivers, i.e. annual above-ground productivity, species richness and root biomass, on the drought response of soil respiration in temperate grasslands. In both years, drought led to a significant reduction in soil respiration. The drought-induced reduction in soil respiration was largely driven by the reduction in above-ground productivity in response to drought. The extent of the drought response of soil respiration was dependent on the species richness level of the site and this interacting effect was explainable by the variation in root biomass (root biomass and species richness were positively correlated). Our findings highlight the importance of biotic drivers for the quantification of the drought response of soil respiration in grasslands.