High CO2 dampens then amplifies N-induced diversity loss over 24 years.

Rising levels of atmospheric carbon dioxide (CO2) and nitrogen (N) deposition affect plant communities in numerous ways1-11. Nitrogen deposition causes local biodiversity loss globally12-14, but whether, and if so how, rising CO2 concentrations amplify or dampen those losses remains unclear and is almost entirely unstudied. We addressed this knowledge gap with an open-air experiment in which 108 grassland plots were grown for 24 years under different CO2 and N regimes. We initially found that adding N reduced plant species richness less at elevated than at ambient CO2. Over time, however, this interaction reversed, and elevated CO2 amplified losses in diversity from enriched N, tripling reductions in species richness from N addition over the last eight years of the study. These interactions resulted from temporal changes in the drivers of diversity, especially light availability, that were in turn driven by CO2 and N inputs and associated changes in plant biomass. This mechanism is likely to be similar in many grasslands, because additions of the plant resources CO2 and N are likely to increase the abundance of the dominant species. If rising CO2 generally exacerbates the widespread negative impacts of N deposition on plant diversity, this bodes poorly for the conservation of grassland biodiversity worldwide.

Biodiversity: Net primary productivity relationships are eliminated by invasive species dominance.

Experiments often find that net primary productivity (NPP) increases with species richness when native species are considered. However, relationships may be altered by exotic (non-native) species, which are hypothesized to reduce richness but increase productivity (i.e., 'invasion-diversity-productivity paradox'). We compared richness-NPP relationships using a comparison of exotic versus native-dominated sites across the central USA, and two experiments under common environments. Aboveground NPP was measured using peak biomass clipping in all three studies, and belowground NPP was measured in one study with root ingrowth cores using root-free soil. In all studies, there was a significantly positive relationship between NPP and richness across native species-dominated sites and plots, but no relationship across exotic-dominated ones. These results indicate that relationships between NPP and richness depend on whether native or exotic species are dominant, and that exotic species are 'breaking the rules', altering richness-productivity and richness-C stock relationships after invasion.

Species interactions amplify functional group responses to elevated CO2 and N enrichment in a 24-year grassland experiment.

Plant functional groups (FGs) differ in their response to global changes, although species within those groups also vary in such responses. Both species and FG responses to global change are likely influenced by species interactions such as inter-specific competition and facilitation, which are prevalent in species mixtures but not monocultures. As most studies focus on responses of plants growing in either monocultures or mixtures, but rarely both, it remains unclear how interspecific interactions in diverse ecological communities, especially among species in different FGs, modify FG responses to global changes. To address these issues, we leveraged data from a 16-species, 24-year perennial grassland experiment to examine plant FG biomass responses to atmospheric CO2, and N inputs at different planted diversity. FGs differed in their responses to N and CO2 treatments in monocultures. Such differences were amplified in mixtures, where N enrichment strongly increased C3 grass success at ambient CO2 and C4 grass success at elevated CO2. Legumes declined with N enrichment in mixtures at both CO2 levels and increased with elevated CO2 in the initial years of the experiment. Our results suggest that previous studies that considered responses to global changes in monocultures may underestimate biomass changes in diverse communities where interspecific interactions can amplify responses. Such effects of interspecific interactions on responses of FGs to global change may impact community composition over time and consequently influence ecosystem functions.

Nitrogen-Induced Hysteresis in Grassland Biodiversity: A Theoretical Test of Litter-Mediated Mechanisms.

AbstractThe global rise in anthropogenic reactive nitrogen and the negative impacts of N deposition on terrestrial plant diversity are well documented. The R* theory of resource competition predicts reversible decreases in plant diversity in response to N loading. However, empirical evidence for the reversibility of N-induced biodiversity loss is mixed. In a long-term N-enrichment experiment in Minnesota, a low-diversity state that emerged during N addition has persisted for decades after additions ceased. Hypothesized mechanisms preventing recovery of biodiversity include nutrient recycling, insufficient external seed supply, and litter inhibition of plant growth. Here, we present an ordinary differential equation model that unifies these mechanisms, produces bistability at intermediate N inputs, and qualitatively matches the observed hysteresis at Cedar Creek. Key features of the model, including native species' growth advantage in low-N conditions and limitation by litter accumulation, generalize from Cedar Creek to North American grasslands. Our results suggest that effective biodiversity restoration in these systems may require management beyond reducing N inputs, such as burning, grazing, haying, and seed additions. By coupling resource competition with an additional interspecific inhibitory process, the model also illustrates a general mechanism for bistability and hysteresis that may occur in multiple ecosystem types.

Linking the influence and dependence of people on biodiversity across scales.

Biodiversity enhances many of nature's benefits to people, including the regulation of climate and the production of wood in forests, livestock forage in grasslands and fish in aquatic ecosystems. Yet people are now driving the sixth mass extinction event in Earth's history. Human dependence and influence on biodiversity have mainly been studied separately and at contrasting scales of space and time, but new multiscale knowledge is beginning to link these relationships. Biodiversity loss substantially diminishes several ecosystem services by altering ecosystem functioning and stability, especially at the large temporal and spatial scales that are most relevant for policy and conservation.

A Conceptual Framework to Integrate Biodiversity, Ecosystem Function, and Ecosystem Service Models.

Global biodiversity and ecosystem service models typically operate independently. Ecosystem service projections may therefore be overly optimistic because they do not always account for the role of biodiversity in maintaining ecological functions. We review models used in recent global model intercomparison projects and develop a novel model integration framework to more fully account for the role of biodiversity in ecosystem function, a key gap for linking biodiversity changes to ecosystem services. We propose two integration pathways. The first uses empirical data on biodiversity-ecosystem function relationships to bridge biodiversity and ecosystem function models and could currently be implemented globally for systems and taxa with sufficient data. We also propose a trait-based approach involving greater incorporation of biodiversity into ecosystem function models. Pursuing both approaches will provide greater insight into biodiversity and ecosystem services projections. Integrating biodiversity, ecosystem function, and ecosystem service modeling will enhance policy development to meet global sustainability goals.

Diversifying livestock promotes multidiversity and multifunctionality in managed grasslands.

Increasing plant diversity can increase ecosystem functioning, stability, and services in both natural and managed grasslands, but the effects of herbivore diversity, and especially of livestock diversity, remain underexplored. Given that managed grazing is the most extensive land use worldwide, and that land managers can readily change livestock diversity, we experimentally tested how livestock diversification (sheep, cattle, or both) influenced multidiversity (the diversity of plants, insects, soil microbes, and nematodes) and ecosystem multifunctionality (including plant biomass production, plant leaf N and P, above-ground insect abundance, nutrient cycling, soil C stocks, water regulation, and plant-microbe symbiosis) in the world's largest remaining grassland. We also considered the potential dependence of ecosystem multifunctionality on multidiversity. We found that livestock diversification substantially increased ecosystem multifunctionality by increasing multidiversity. The link between multidiversity and ecosystem multifunctionality was always stronger than the link between single diversity components and functions. Our work provides insights into the importance of multitrophic diversity to maintain multifunctionality in managed ecosystems and suggests that diversifying livestock could promote both multidiversity and ecosystem multifunctionality in an increasingly managed world.

Global change effects on plant communities are magnified by time and the number of global change factors imposed.

Global change drivers (GCDs) are expected to alter community structure and consequently, the services that ecosystems provide. Yet, few experimental investigations have examined effects of GCDs on plant community structure across multiple ecosystem types, and those that do exist present conflicting patterns. In an unprecedented global synthesis of over 100 experiments that manipulated factors linked to GCDs, we show that herbaceous plant community responses depend on experimental manipulation length and number of factors manipulated. We found that plant communities are fairly resistant to experimentally manipulated GCDs in the short term (<10 y). In contrast, long-term (≥10 y) experiments show increasing community divergence of treatments from control conditions. Surprisingly, these community responses occurred with similar frequency across the GCD types manipulated in our database. However, community responses were more common when 3 or more GCDs were simultaneously manipulated, suggesting the emergence of additive or synergistic effects of multiple drivers, particularly over long time periods. In half of the cases, GCD manipulations caused a difference in community composition without a corresponding species richness difference, indicating that species reordering or replacement is an important mechanism of community responses to GCDs and should be given greater consideration when examining consequences of GCDs for the biodiversity-ecosystem function relationship. Human activities are currently driving unparalleled global changes worldwide. Our analyses provide the most comprehensive evidence to date that these human activities may have widespread impacts on plant community composition globally, which will increase in frequency over time and be greater in areas where communities face multiple GCDs simultaneously.

Determinants of community compositional change are equally affected by global change.

Global change is impacting plant community composition, but the mechanisms underlying these changes are unclear. Using a dataset of 58 global change experiments, we tested the five fundamental mechanisms of community change: changes in evenness and richness, reordering, species gains and losses. We found 71% of communities were impacted by global change treatments, and 88% of communities that were exposed to two or more global change drivers were impacted. Further, all mechanisms of change were equally likely to be affected by global change treatments-species losses and changes in richness were just as common as species gains and reordering. We also found no evidence of a progression of community changes, for example, reordering and changes in evenness did not precede species gains and losses. We demonstrate that all processes underlying plant community composition changes are equally affected by treatments and often occur simultaneously, necessitating a wholistic approach to quantifying community changes.

Grand challenges in biodiversity-ecosystem functioning research in the era of science-policy platforms require explicit consideration of feedbacks.

Feedbacks are an essential feature of resilient socio-economic systems, yet the feedbacks between biodiversity, ecosystem services and human wellbeing are not fully accounted for in global policy efforts that consider future scenarios for human activities and their consequences for nature. Failure to integrate feedbacks in our knowledge frameworks exacerbates uncertainty in future projections and potentially prevents us from realizing the full benefits of actions we can take to enhance sustainability. We identify six scientific research challenges that, if addressed, could allow future policy, conservation and monitoring efforts to quantitatively account for ecosystem and societal consequences of biodiversity change. Placing feedbacks prominently in our frameworks would lead to (i) coordinated observation of biodiversity change, ecosystem functions and human actions, (ii) joint experiment and observation programmes, (iii) more effective use of emerging technologies in biodiversity science and policy, and (iv) a more inclusive and integrated global community of biodiversity observers. To meet these challenges, we outline a five-point action plan for collaboration and connection among scientists and policymakers that emphasizes diversity, inclusion and open access. Efforts to protect biodiversity require the best possible scientific understanding of human activities, biodiversity trends, ecosystem functions and-critically-the feedbacks among them.

Disturbance type and species life history predict mammal responses to humans.

Human activity and land use change impact every landscape on Earth, driving declines in many animal species while benefiting others. Species ecological and life history traits may predict success in human-dominated landscapes such that only species with "winning" combinations of traits will persist in disturbed environments. However, this link between species traits and successful coexistence with humans remains obscured by the complexity of anthropogenic disturbances and variability among study systems. We compiled detection data for 24 mammal species from 61 populations across North America to quantify the effects of (1) the direct presence of people and (2) the human footprint (landscape modification) on mammal occurrence and activity levels. Thirty-three percent of mammal species exhibited a net negative response (i.e., reduced occurrence or activity) to increasing human presence and/or footprint across populations, whereas 58% of species were positively associated with increasing disturbance. However, apparent benefits of human presence and footprint tended to decrease or disappear at higher disturbance levels, indicative of thresholds in mammal species' capacity to tolerate disturbance or exploit human-dominated landscapes. Species ecological and life history traits were strong predictors of their responses to human footprint, with increasing footprint favoring smaller, less carnivorous, faster-reproducing species. The positive and negative effects of human presence were distributed more randomly with respect to species trait values, with apparent winners and losers across a range of body sizes and dietary guilds. Differential responses by some species to human presence and human footprint highlight the importance of considering these two forms of human disturbance separately when estimating anthropogenic impacts on wildlife. Our approach provides insights into the complex mechanisms through which human activities shape mammal communities globally, revealing the drivers of the loss of larger predators in human-modified landscapes.

Behaviorally-mediated trophic cascade attenuated by prey use of risky places at safe times.

The mere threat of predation may incite behavioral changes in prey that lead to community-wide impacts on productivity, biodiversity, and nutrient cycling. The paucity of experimental manipulations, however, has contributed to controversy over the strength of this pathway in wide-ranging vertebrate systems. We investigated whether simulated gray wolf (Canis lupus) presence can induce behaviorally-mediated trophic cascades, specifically, whether the 'fear' of wolf olfactory cues alone can change deer foraging behavior in ways that affect plants and soils. Wolves were recently removed from the Cedar Creek Ecosystem Science Reserve (Minnesota, USA), such that consumptively mediated predator effects were negligible. At 32 experimental plots, we crossed two nested treatments: wolf urine application and herbivore exclosures. We deployed camera traps to quantify how white-tailed deer (Odocoileus virginianus) adjusted their spatiotemporal habitat use, foraging, and vigilance in response to wolf cues and how these behavioral changes affected plant productivity, plant communities, and soil nutrients. Weekly applications of wolf urine significantly altered deer behavior, but deer responses did not cascade to affect plant or soil properties. Deer substantially reduced crepuscular activity at wolf-simulated sites compared to control locations. As wolves in this area predominantly hunted during mornings and evenings, this response potentially allows deer to maximize landscape use by accessing dangerous areas when temporal threat is low. Our experiment suggests that prey may be sensitive to 'dynamic' predation risk that is structured across both space and time and, consequentially, prey use of risky areas during safe times may attenuate behaviorally-mediated trophic cascades at the predator-prey interface.

Biodiversity increases the resistance of ecosystem productivity to climate extremes.

It remains unclear whether biodiversity buffers ecosystems against climate extremes, which are becoming increasingly frequent worldwide. Early results suggested that the ecosystem productivity of diverse grassland plant communities was more resistant, changing less during drought, and more resilient, recovering more quickly after drought, than that of depauperate communities. However, subsequent experimental tests produced mixed results. Here we use data from 46 experiments that manipulated grassland plant diversity to test whether biodiversity provides resistance during and resilience after climate events. We show that biodiversity increased ecosystem resistance for a broad range of climate events, including wet or dry, moderate or extreme, and brief or prolonged events. Across all studies and climate events, the productivity of low-diversity communities with one or two species changed by approximately 50% during climate events, whereas that of high-diversity communities with 16-32 species was more resistant, changing by only approximately 25%. By a year after each climate event, ecosystem productivity had often fully recovered, or overshot, normal levels of productivity in both high- and low-diversity communities, leading to no detectable dependence of ecosystem resilience on biodiversity. Our results suggest that biodiversity mainly stabilizes ecosystem productivity, and productivity-dependent ecosystem services, by increasing resistance to climate events. Anthropogenic environmental changes that drive biodiversity loss thus seem likely to decrease ecosystem stability, and restoration of biodiversity to increase it, mainly by changing the resistance of ecosystem productivity to climate events.

Grassland biodiversity can pay.

The biodiversity-ecosystem functioning (BEF) literature provides strong evidence of the biophysical basis for the potential profitability of greater diversity but does not address questions of optimal management. BEF studies typically focus on the ecosystem outputs produced by randomly assembled communities that only differ in their biodiversity levels, measured by indices such as species richness. Landholders, however, do not randomly select species to plant; they choose particular species that collectively maximize profits. As such, their interest is not in comparing the average performance of randomly assembled communities at each level of biodiversity but rather comparing the best-performing communities at each diversity level. Assessing the best-performing mixture requires detailed accounting of species' identities and relative abundances. It also requires accounting for the financial cost of individual species' seeds, and the economic value of changes in the quality, quantity, and variability of the species' collective output-something that existing multifunctionality indices fail to do. This study presents an assessment approach that integrates the relevant factors into a single, coherent framework. It uses ecological production functions to inform an economic model consistent with the utility-maximizing decisions of a potentially risk-averse private landowner. We demonstrate the salience and applicability of the framework using data from an experimental grassland to estimate production relationships for hay and carbon storage. For that case, our results suggest that even a risk-neutral, profit-maximizing landowner would favor a highly diverse mix of species, with optimal species richness falling between the low levels currently found in commercial grasslands and the high levels found in natural grasslands.

Scaling-up biodiversity-ecosystem functioning research.

A rich body of knowledge links biodiversity to ecosystem functioning (BEF), but it is primarily focused on small scales. We review the current theory and identify six expectations for scale dependence in the BEF relationship: (1) a nonlinear change in the slope of the BEF relationship with spatial scale; (2) a scale-dependent relationship between ecosystem stability and spatial extent; (3) coexistence within and among sites will result in a positive BEF relationship at larger scales; (4) temporal autocorrelation in environmental variability affects species turnover and thus the change in BEF slope with scale; (5) connectivity in metacommunities generates nonlinear BEF and stability relationships by affecting population  synchrony at local and regional scales; (6) spatial scaling in food web structure and diversity will generate scale dependence in ecosystem functioning. We suggest directions for synthesis that combine approaches in metaecosystem and metacommunity ecology and integrate cross-scale feedbacks. Tests of this theory may combine remote sensing with a generation of networked experiments that assess effects at multiple scales. We also show how anthropogenic land cover change may alter the scaling of the BEF relationship. New research on the role of scale in BEF will guide policy linking the goals of managing biodiversity and ecosystems.

Diversity-dependent soil acidification under nitrogen enrichment constrains biomass productivity.

In most plant communities, the net effect of nitrogen enrichment is an increase in plant productivity. However, nitrogen enrichment also has been shown to decrease species richness and to acidify soils, each of which may diminish the long-term impact of nutrient enrichment on productivity. Here we use a long-term (20 year) grassland plant diversity by nitrogen enrichment experiment in Minnesota, United States (a subexperiment within the BioCON experiment) to quantify the net impacts of nitrogen enrichment on productivity, including its potential indirect effects on productivity via changes in species richness and soil pH over an experimental diversity gradient. Overall, we found that nitrogen enrichment led to an immediate positive increment in productivity, but that this effect became nonsignificant over later years of the experiment, with the difference in productivity between fertilized and unfertilized plots decreasing in proportion to nitrogen addition-dependent declines in soil pH and losses of plant diversity. The net effect of nitrogen enrichment on productivity could have been 14.5% more on average over 20 years in monocultures if not for nitrogen-induced decreases in pH and about 28.5% more on average over 20 years in 16 species communities if not for nitrogen-induced species richness losses. Together, these results suggest that the positive effects of nutrient enrichment on biomass production can diminish in their magnitude over time, especially because of soil acidification in low diversity communities and especially because of plant diversity loss in initially high diversity communities.

Temporal variability in production is not consistently affected by global change drivers across herbaceous-dominated ecosystems.

Understanding how global change drivers (GCDs) affect aboveground net primary production (ANPP) through time is essential to predicting the reliability and maintenance of ecosystem function and services in the future. While GCDs, such as drought, warming and elevated nutrients, are known to affect mean ANPP, less is known about how they affect inter-annual variability in ANPP. We examined 27 global change experiments located in 11 different herbaceous ecosystems that varied in both abiotic and biotic conditions, to investigate changes in the mean and temporal variability of ANPP (measured as the coefficient of variation) in response to different GCD manipulations, including resource additions, warming, and irrigation. From this comprehensive data synthesis, we found that GCD treatments increased mean ANPP. However, GCD manipulations both increased and decreased temporal variability of ANPP (24% of comparisons), with no net effect overall. These inconsistent effects on temporal variation in ANPP can, in part, be attributed to site characteristics, such as mean annual precipitation and temperature as well as plant community evenness. For example, decreases in temporal variability in ANPP with the GCD treatments occurred in wetter and warmer sites with lower plant community evenness. Further, the addition of several nutrients simultaneously increased the sensitivity of ANPP to interannual variation in precipitation. Based on this analysis, we expect that GCDs will likely affect the magnitude more than the reliability over time of ecosystem production in the future.

Quantifying effects of biodiversity on ecosystem functioning across times and places.

Biodiversity loss decreases ecosystem functioning at the local scales at which species interact, but it remains unclear how biodiversity loss affects ecosystem functioning at the larger scales of space and time that are most relevant to biodiversity conservation and policy. Theory predicts that additional insurance effects of biodiversity on ecosystem functioning could emerge across time and space if species respond asynchronously to environmental variation and if species become increasingly dominant when and where they are most productive. Even if only a few dominant species maintain ecosystem functioning within a particular time and place, ecosystem functioning may be enhanced by many different species across many times and places (ß-diversity). Here, we develop and apply a new approach to estimate these previously unquantified insurance effects of biodiversity on ecosystem functioning that arise due to species turnover across times and places. In a long-term (18-year) grassland plant diversity experiment, we find that total insurance effects are positive in sign and substantial in magnitude, amounting to 19% of the net biodiversity effect, mostly due to temporal insurance effects. Species loss can therefore reduce ecosystem functioning both locally and by eliminating species that would otherwise enhance ecosystem functioning across temporally fluctuating and spatially heterogeneous environments.

Integrating community assembly and biodiversity to better understand ecosystem function: the Community Assembly and the Functioning of Ecosystems (CAFE) approach.

The research of a generation of ecologists was catalysed by the recognition that the number and identity of species in communities influences the functioning of ecosystems. The relationship between biodiversity and ecosystem functioning (BEF) is most often examined by controlling species richness and randomising community composition. In natural systems, biodiversity changes are often part of a bigger community assembly dynamic. Therefore, focusing on community assembly and the functioning of ecosystems (CAFE), by integrating both species richness and composition through species gains, losses and changes in abundance, will better reveal how community changes affect ecosystem function. We synthesise the BEF and CAFE perspectives using an ecological application of the Price equation, which partitions the contributions of richness and composition to function. Using empirical examples, we show how the CAFE approach reveals important contributions of composition to function. These examples show how changes in species richness and composition driven by environmental perturbations can work in concert or antagonistically to influence ecosystem function. Considering how communities change in an integrative fashion, rather than focusing on one axis of community structure at a time, will improve our ability to anticipate and predict changes in ecosystem function.