The effect of diversity on disease reverses from dilution to amplification in a 22-year biodiversity × N × CO2 experiment.

Plant disease often increases with N, decreases with CO2, and increases as biodiversity is lost (i.e., the dilution effect). Additionally, all these factors can indirectly alter disease by changing host biomass and hence density-dependent disease transmission. Yet over long periods of time as communities undergo compositional changes, these biomass-mediated pathways might fade, intensify, or even reverse in direction. Using a field experiment that has manipulated N, CO2, and species richness for over 20 years, we compared severity of a specialist rust fungus (Puccinia andropogonis) on its grass host (Andropogon gerardii) shortly after the experiment began (1999) and twenty years later (2019). Between these two sampling periods, two decades apart, we found that disease severity consistently increased with N and decreased with CO2. However, the relationship between diversity and disease reversed from a dilution effect in 1999 (more severe disease in monocultures) to an amplification effect in 2019 (more severe disease in mixtures). The best explanation for this reversal centered on host density (i.e., aboveground biomass), which was initially highest in monoculture, but became highest in mixtures two decades later. Thus, the diversity-disease pattern reversed, but disease consistently increased with host biomass. These results highlight the consistency of N and CO2 as drivers of plant disease in the Anthropocene and emphasize the critical role of host biomass-despite potentially variable effects of diversity-for relationships between biodiversity and disease.

ZooTraits: An R shiny app for exploring animal trait data for ecological and evolutionary research.

Animal trait data are scattered across several datasets, making it challenging to compile and compare trait information across different groups. For plants, the TRY database has been an unwavering success for those ecologists interested in addressing how plant traits influence a wide variety of processes and patterns, but the same is not true for most animal taxonomic groups. Here, we introduce ZooTraits, a Shiny app designed to help users explore and obtain animal trait data for research in ecology and evolution. ZooTraits was developed to tackle the challenge of finding in a single site information of multiple trait datasets and facilitating access to traits by providing an easy-to-use, open-source platform. This app combines datasets centralized in the Open Trait Network, raw data from the AnimalTraits database, and trait information for animals compiled by Gonçalves-Souza et al. (2023, Ecology and Evolution 13, e10016). Importantly, the ZooTraits app can be accessed freely and provides a user-friendly interface through three functionalities that will allow users to easily visualize, compare, download, and upload trait data across the animal tree of life-ExploreTrait, FeedTrait, and GetTrait. By using ExploreTrait and GetTrait, users can explore, compare, and extract 3954 trait records from 23,394 species centralized in the Open Traits Network, and trait data for ~2000 species from the AnimalTraits database. The app summarizes trait information for numerous taxonomic groups within the Animal Kingdom, encompassing data from diverse aquatic and terrestrial ecosystems and various geographic regions worldwide. Moreover, ZooTraits enables researchers to upload trait information, serving as a hub for a continually expanding global trait database. By promoting the centralization of trait datasets and offering a platform for data sharing, ZooTraits is facilitating advancements in trait-based ecological and evolutionary studies. We hope that other trait databases will evolve to mirror the approach we have outlined here.

Molecular-level carbon traits underlie the multidimensional fine root economics space.

Carbon influences the evolution and functioning of plants and their roots. Previous work examining a small number of commonly measured root traits has revealed a global multidimensionality of the resource economics traits in fine roots considering carbon as primary currency but without considering the diversity of carbon-related traits. To address this knowledge gap, we use data from 66 tree species from a tropical forest to illustrate that root economics space co-varies with a novel molecular-level traits space based on nuclear magnetic resonance. Thinner fine roots exhibit higher proportions of carbohydrates and lower diversity of molecular carbon than thicker roots. Mass-denser fine roots have more lignin and aromatic carbon compounds but less bioactive carbon compounds than lighter roots. Thus, the transition from thin to thick fine roots implies a shift in the root carbon economy from 'do-it-yourself' soil exploration to collaboration with mycorrhizal fungi, while the shift from light to dense fine roots emphasizes a shift from acquisitive to conservative root strategy. We reveal a previously undocumented role of molecular-level carbon traits that potentially undergird the multidimensional root economics space. This finding offers new molecular insight into the diversity of root form and function, which is fundamental to our understanding of plant evolution, species coexistence and adaptations to heterogeneous environments.

Linking fine root lifespan to root chemical and morphological traits-A global analysis.

Fine root lifespan is a critical trait associated with contrasting root strategies of resource acquisition and protection. Yet, its position within the multidimensional "root economics space" synthesizing global root economics strategies is largely uncertain, and it is rarely represented in frameworks integrating plant trait variations. Here, we compiled the most comprehensive dataset of absorptive median root lifespan (MRL) data including 98 observations from 79 woody species using (mini-)rhizotrons across 40 sites and linked MRL to other plant traits to address questions of the regulators of MRL at large spatial scales. We demonstrate that MRL not only decreases with plant investment in root nitrogen (associated with more metabolically active tissues) but also increases with construction of larger diameter roots which is often associated with greater plant reliance on mycorrhizal symbionts. Although theories linking organ structure and function suggest that root traits should play a role in modulating MRL, we found no correlation between root traits associated with structural defense (root tissue density and specific root length) and MRL. Moreover, fine root and leaf lifespan were globally unrelated, except among evergreen species, suggesting contrasting evolutionary selection between leaves and roots facing contrasting environmental influences above vs. belowground. At large geographic scales, MRL was typically longer at sites with lower mean annual temperature and higher mean annual precipitation. Overall, this synthesis uncovered several key ecophysiological covariates and environmental drivers of MRL, highlighting broad avenues for accurate parametrization of global biogeochemical models and the understanding of ecosystem response to global climate change.

Deforestation impacts soil biodiversity and ecosystem services worldwide.

Deforestation poses a global threat to biodiversity and its capacity to deliver ecosystem services. Yet, the impacts of deforestation on soil biodiversity and its associated ecosystem services remain virtually unknown. We generated a global dataset including 696 paired-site observations to investigate how native forest conversion to other land uses affects soil properties, biodiversity, and functions associated with the delivery of multiple ecosystem services. The conversion of native forests to plantations, grasslands, and croplands resulted in higher bacterial diversity and more homogeneous fungal communities dominated by pathogens and with a lower abundance of symbionts. Such conversions also resulted in significant reductions in carbon storage, nutrient cycling, and soil functional rates related to organic matter decomposition. Responses of the microbial community to deforestation, including bacterial and fungal diversity and fungal guilds, were predominantly regulated by changes in soil pH and total phosphorus. Moreover, we found that soil fungal diversity and functioning in warmer and wetter native forests is especially vulnerable to deforestation. Our work highlights that the loss of native forests to managed ecosystems poses a major global threat to the biodiversity and functioning of soils and their capacity to deliver ecosystem services.

Predators control pests and increase yield across crop types and climates: a meta-analysis.

Pesticides have well-documented negative consequences to control crop pests, and natural predators are alternatives and can provide an ecosystem service as biological control agents. However, there remains considerable uncertainty regarding whether such biological control can be a widely applicable solution, especially given ongoing climatic variation and climate change. Here, we performed a meta-analysis focused on field studies with natural predators to explore broadly whether and how predators might control pests and in turn increase yield. We also contrasted across studies pest suppression by a single and multiple predators and how climate influence biological control. Predators reduced pest populations by 73% on average, and increased crop yield by 25% on average. Surprisingly, the impact of predators did not depend on whether there were many or a single predator species. Precipitation seasonality was a key climatic influence on biological control: as seasonality increased, the impact of predators on pest populations increased. Taken together, the positive contribution of predators in controlling pests and increasing yield, and the consistency of such responses in the face of precipitation variability, suggest that biocontrol has the potential to be an important part of pest management and increasing food supplies as the planet precipitation patterns become increasingly variable.

Cumulative nitrogen enrichment alters the drivers of grassland overyielding.

Effects of plant diversity on grassland productivity, or overyielding, are found to be robust to nutrient enrichment. However, the impact of cumulative nitrogen (N) addition (total N added over time) on overyielding and its drivers are underexplored. Synthesizing data from 15 multi-year grassland biodiversity experiments with N addition, we found that N addition decreases complementarity effects and increases selection effects proportionately, resulting in no overall change in overyielding regardless of N addition rate. However, we observed a convex relationship between overyielding and cumulative N addition, driven by a shift from complementarity to selection effects. This shift suggests diminishing positive interactions and an increasing contribution of a few dominant species with increasing N accumulation. Recognizing the importance of cumulative N addition is vital for understanding its impacts on grassland overyielding, contributing essential insights for biodiversity conservation and ecosystem resilience in the face of increasing N deposition.

Effects of plant diversity on productivity strengthen over time due to trait-dependent shifts in species overyielding.

Plant diversity effects on community productivity often increase over time. Whether the strengthening of diversity effects is caused by temporal shifts in species-level overyielding (i.e., higher species-level productivity in diverse communities compared with monocultures) remains unclear. Here, using data from 65 grassland and forest biodiversity experiments, we show that the temporal strength of diversity effects at the community scale is underpinned by temporal changes in the species that yield. These temporal trends of species-level overyielding are shaped by plant ecological strategies, which can be quantitatively delimited by functional traits. In grasslands, the temporal strengthening of biodiversity effects on community productivity was associated with increasing biomass overyielding of resource-conservative species increasing over time, and with overyielding of species characterized by fast resource acquisition either decreasing or increasing. In forests, temporal trends in species overyielding differ when considering above- versus belowground resource acquisition strategies. Overyielding in stem growth decreased for species with high light capture capacity but increased for those with high soil resource acquisition capacity. Our results imply that a diversity of species with different, and potentially complementary, ecological strategies is beneficial for maintaining community productivity over time in both grassland and forest ecosystems.

Long-term warming increased carbon sequestration capacity in a humid subtropical forest.

Tropical and subtropical forests play a crucial role in global carbon (C) pools, and their responses to warming can significantly impact C-climate feedback and predictions of future global warming. Despite earth system models projecting reductions in land C storage with warming, the magnitude of this response varies greatly between models, particularly in tropical and subtropical regions. Here, we conducted a field ecosystem-level warming experiment in a subtropical forest in southern China, by translocating mesocosms (ecosystem composed of soils and plants) across 600 m elevation gradients with temperature gradients of 2.1°C (moderate warming), to explore the response of ecosystem C dynamics of the subtropical forest to continuous 6-year warming. Compared with the control, the ecosystem C stock decreased by 3.8% under the first year of 2.1°C warming; but increased by 13.4% by the sixth year of 2.1°C warming. The increased ecosystem C stock by the sixth year of warming was mainly attributed to a combination of sustained increased plant C stock due to the maintenance of a high plant growth rate and unchanged soil C stock. The unchanged soil C stock was driven by compensating and offsetting thermal adaptation of soil microorganisms (unresponsive soil respiration and enzyme activity, and more stable microbial community), increased plant C input, and inhibitory C loss (decreased C leaching and inhibited temperature sensitivity of soil respiration) from soil drying. These results suggest that the humid subtropical forest C pool would not necessarily diminish consistently under future long-term warming. We highlight that differential and asynchronous responses of plant and soil C processes over relatively long-term periods should be considered when predicting the effects of climate warming on ecosystem C dynamics of subtropical forests.

Reduced global plant respiration due to the acclimation of leaf dark respiration coupled with photosynthesis.

Leaf dark respiration (Rd ) acclimates to environmental changes. However, the magnitude, controls and time scales of acclimation remain unclear and are inconsistently treated in ecosystem models. We hypothesized that Rd and Rubisco carboxylation capacity (Vcmax ) at 25°C (Rd,25 , Vcmax,25 ) are coordinated so that Rd,25 variations support Vcmax,25 at a level allowing full light use, with Vcmax,25 reflecting daytime conditions (for photosynthesis), and Rd,25 /Vcmax,25 reflecting night-time conditions (for starch degradation and sucrose export). We tested this hypothesis temporally using a 5-yr warming experiment, and spatially using an extensive field-measurement data set. We compared the results to three published alternatives: Rd,25 declines linearly with daily average prior temperature; Rd at average prior night temperatures tends towards a constant value; and Rd,25 /Vcmax,25 is constant. Our hypothesis accounted for more variation in observed Rd,25 over time (R2 = 0.74) and space (R2 = 0.68) than the alternatives. Night-time temperature dominated the seasonal time-course of Rd , with an apparent response time scale of c. 2 wk. Vcmax dominated the spatial patterns. Our acclimation hypothesis results in a smaller increase in global Rd in response to rising CO2 and warming than is projected by the two of three alternative hypotheses, and by current models.

Rapid migration of Mongolian oak into the southern Asian boreal forest.

The migration of trees induced by climatic warming has been observed at many alpine treelines and boreal-tundra ecotones, but the migration of temperate trees into southern boreal forest remains less well documented. We conducted a field investigation across an ecotone of temperate and boreal forests in northern Greater Khingan Mountains of northeast China. Our analysis demonstrates that Mongolian oak (Quercus mongolica), an important temperate tree species, has migrated rapidly into southern boreal forest in synchrony with significant climatic warming over the past century. The average rate of migration is estimated to be 12.0 ± 1.0 km decade-1 , being slightly slower than the movement of isotherms (14.7 ± 6.4 km decade-1 ). The migration rate of Mongolian oak is the highest observed among migratory temperate trees (average rate 4.0 ± 1.0 km decade-1 ) and significantly higher than the rates of tree migration at boreal-tundra ecotones (0.9 ± 0.4 km decade-1 ) and alpine treelines (0.004 ± 0.003 km decade-1 ). Compared with the coexisting dominant boreal tree species, Dahurian larch (Larix gmelinii), temperate Mongolian oak is observed to have significantly lower capacity for light acquisition, comparable water-use efficiency but stronger capacity to utilize nutrients especially the most limiting nutrient, nitrogen. In the context of climatic warming, and in addition to a high seed dispersal capacity and potential thermal niche differences, the advantage of nutrient utilization, reflected by foliar elementomes and stable nitrogen isotope ratios, is also likely a key mechanism for Mongolian oak to coexist with Dahurian larch and facilitate its migration toward boreal forest. These findings highlight a rapid deborealization of southern Asian boreal forest in response to climatic warming.

Integrated global assessment of the natural forest carbon potential.

Forests are a substantial terrestrial carbon sink, but anthropogenic changes in land use and climate have considerably reduced the scale of this system1. Remote-sensing estimates to quantify carbon losses from global forests2-5 are characterized by considerable uncertainty and we lack a comprehensive ground-sourced evaluation to benchmark these estimates. Here we combine several ground-sourced6 and satellite-derived approaches2,7,8 to evaluate the scale of the global forest carbon potential outside agricultural and urban lands. Despite regional variation, the predictions demonstrated remarkable consistency at a global scale, with only a 12% difference between the ground-sourced and satellite-derived estimates. At present, global forest carbon storage is markedly under the natural potential, with a total deficit of 226 Gt (model range = 151-363 Gt) in areas with low human footprint. Most (61%, 139 Gt C) of this potential is in areas with existing forests, in which ecosystem protection can allow forests to recover to maturity. The remaining 39% (87 Gt C) of potential lies in regions in which forests have been removed or fragmented. Although forests cannot be a substitute for emissions reductions, our results support the idea2,3,9 that the conservation, restoration and sustainable management of diverse forests offer valuable contributions to meeting global climate and biodiversity targets.

Increasing atmospheric dryness reduces boreal forest tree growth.

Rising atmospheric vapour pressure deficit (VPD) associated with climate change affects boreal forest growth via stomatal closure and soil dryness. However, the relationship between VPD and forest growth depends on the climatic context. Here we assess Canadian boreal forest responses to VPD changes from 1951-2018 using a well-replicated tree-growth increment network with approximately 5,000 species-site combinations. Of the 3,559 successful growth models, we observed a relationship between growth and concurrent summer VPD in one-third of the species-site combinations, and between growth and prior summer VPD in almost half of those combinations. The relationship between previous year VPD and current year growth was almost exclusively negative, while current year VPD also tended to reduce growth. Tree species, age, annual temperature, and soil moisture primarily determined tree VPD responses. Younger trees and species like white spruce and Douglas fir exhibited higher VPD sensitivity, as did areas with high annual temperature and low soil moisture. Since 1951, summer VPD increases in Canada have paralleled tree growth decreases, particularly in spruce species. Accelerating atmospheric dryness in the decades ahead will impair carbon storage and societal-economic services.

The global biogeography of tree leaf form and habit.

Understanding what controls global leaf type variation in trees is crucial for comprehending their role in terrestrial ecosystems, including carbon, water and nutrient dynamics. Yet our understanding of the factors influencing forest leaf types remains incomplete, leaving us uncertain about the global proportions of needle-leaved, broadleaved, evergreen and deciduous trees. To address these gaps, we conducted a global, ground-sourced assessment of forest leaf-type variation by integrating forest inventory data with comprehensive leaf form (broadleaf vs needle-leaf) and habit (evergreen vs deciduous) records. We found that global variation in leaf habit is primarily driven by isothermality and soil characteristics, while leaf form is predominantly driven by temperature. Given these relationships, we estimate that 38% of global tree individuals are needle-leaved evergreen, 29% are broadleaved evergreen, 27% are broadleaved deciduous and 5% are needle-leaved deciduous. The aboveground biomass distribution among these tree types is approximately 21% (126.4 Gt), 54% (335.7 Gt), 22% (136.2 Gt) and 3% (18.7 Gt), respectively. We further project that, depending on future emissions pathways, 17-34% of forested areas will experience climate conditions by the end of the century that currently support a different forest type, highlighting the intensification of climatic stress on existing forests. By quantifying the distribution of tree leaf types and their corresponding biomass, and identifying regions where climate change will exert greatest pressure on current leaf types, our results can help improve predictions of future terrestrial ecosystem functioning and carbon cycling.

Native diversity buffers against severity of non-native tree invasions.

Determining the drivers of non-native plant invasions is critical for managing native ecosystems and limiting the spread of invasive species1,2. Tree invasions in particular have been relatively overlooked, even though they have the potential to transform ecosystems and economies3,4. Here, leveraging global tree databases5-7, we explore how the phylogenetic and functional diversity of native tree communities, human pressure and the environment influence the establishment of non-native tree species and the subsequent invasion severity. We find that anthropogenic factors are key to predicting whether a location is invaded, but that invasion severity is underpinned by native diversity, with higher diversity predicting lower invasion severity. Temperature and precipitation emerge as strong predictors of invasion strategy, with non-native species invading successfully when they are similar to the native community in cold or dry extremes. Yet, despite the influence of these ecological forces in determining invasion strategy, we find evidence that these patterns can be obscured by human activity, with lower ecological signal in areas with higher proximity to shipping ports. Our global perspective of non-native tree invasion highlights that human drivers influence non-native tree presence, and that native phylogenetic and functional diversity have a critical role in the establishment and spread of subsequent invasions.

Boreal conifers maintain carbon uptake with warming despite failure to track optimal temperatures.

Warming shifts the thermal optimum of net photosynthesis (ToptA) to higher temperatures. However, our knowledge of this shift is mainly derived from seedlings grown in greenhouses under ambient atmospheric carbon dioxide (CO2) conditions. It is unclear whether shifts in ToptA of field-grown trees will keep pace with the temperatures predicted for the 21st century under elevated atmospheric CO2 concentrations. Here, using a whole-ecosystem warming controlled experiment under either ambient or elevated CO2 levels, we show that ToptA of mature boreal conifers increased with warming. However, shifts in ToptA did not keep pace with warming as ToptA only increased by 0.26-0.35 °C per 1 °C of warming. Net photosynthetic rates estimated at the mean growth temperature increased with warming in elevated CO2 spruce, while remaining constant in ambient CO2 spruce and in both ambient CO2 and elevated CO2 tamarack with warming. Although shifts in ToptA of these two species are insufficient to keep pace with warming, these boreal conifers can thermally acclimate photosynthesis to maintain carbon uptake in future air temperatures.

Climate change-induced stress disrupts ectomycorrhizal interaction networks at the boreal-temperate ecotone.

The interaction networks formed by ectomycorrhizal fungi (EMF) and their tree hosts, which are important to both forest recruitment and ecosystem carbon and nutrient retention, may be particularly susceptible to climate change at the boreal-temperate forest ecotone where environmental conditions are changing rapidly. Here, we quantified the compositional and functional trait responses of EMF communities and their interaction networks with two boreal (Pinus banksiana and Betula papyrifera) and two temperate (Pinus strobus and Quercus macrocarpa) hosts to a factorial combination of experimentally elevated temperatures and reduced rainfall in a long-term open-air field experiment. The study was conducted at the B4WarmED (Boreal Forest Warming at an Ecotone in Danger) experiment in Minnesota, USA, where infrared lamps and buried heating cables elevate temperatures (ambient, +3.1 °C) and rain-out shelters reduce growing season precipitation (ambient, ~30% reduction). EMF communities were characterized and interaction networks inferred from metabarcoding of fungal-colonized root tips. Warming and rainfall reduction significantly altered EMF community composition, leading to an increase in the relative abundance of EMF with contact-short distance exploration types. These compositional changes, which likely limited the capacity for mycelial connections between trees, corresponded with shifts from highly redundant EMF interaction networks under ambient conditions to less redundant (more specialized) networks. Further, the observed changes in EMF communities and interaction networks were correlated with changes in soil moisture and host photosynthesis. Collectively, these results indicate that the projected changes in climate will likely lead to significant shifts in the traits, structure, and integrity of EMF communities as well as their interaction networks in forest ecosystems at the boreal-temperate ecotone.

Leaf-level coordination principles propagate to the ecosystem scale.

Fundamental axes of variation in plant traits result from trade-offs between costs and benefits of resource-use strategies at the leaf scale. However, it is unclear whether similar trade-offs propagate to the ecosystem level. Here, we test whether trait correlation patterns predicted by three well-known leaf- and plant-level coordination theories - the leaf economics spectrum, the global spectrum of plant form and function, and the least-cost hypothesis - are also observed between community mean traits and ecosystem processes. We combined ecosystem functional properties from FLUXNET sites, vegetation properties, and community mean plant traits into three corresponding principal component analyses. We find that the leaf economics spectrum (90 sites), the global spectrum of plant form and function (89 sites), and the least-cost hypothesis (82 sites) all propagate at the ecosystem level. However, we also find evidence of additional scale-emergent properties. Evaluating the coordination of ecosystem functional properties may aid the development of more realistic global dynamic vegetation models with critical empirical data, reducing the uncertainty of climate change projections.