Clarifying the effect of biodiversity on productivity in natural ecosystems with longitudinal data and methods for causal inference.

Causal effects of biodiversity on ecosystem functions can be estimated using experimental or observational designs - designs that pose a tradeoff between drawing credible causal inferences from correlations and drawing generalizable inferences. Here, we develop a design that reduces this tradeoff and revisits the question of how plant species diversity affects productivity. Our design leverages longitudinal data from 43 grasslands in 11 countries and approaches borrowed from fields outside of ecology to draw causal inferences from observational data. Contrary to many prior studies, we estimate that increases in plot-level species richness caused productivity to decline: a 10% increase in richness decreased productivity by 2.4%, 95% CI [-4.1, -0.74]. This contradiction stems from two sources. First, prior observational studies incompletely control for confounding factors. Second, most experiments plant fewer rare and non-native species than exist in nature. Although increases in native, dominant species increased productivity, increases in rare and non-native species decreased productivity, making the average effect negative in our study. By reducing the tradeoff between experimental and observational designs, our study demonstrates how observational studies can complement prior ecological experiments and inform future ones.

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.

Water availability modifies productivity response to biodiversity and nitrogen in long-term grassland experiments.

Diversity and nitrogen addition have positive relationships with plant productivity, yet climate-induced changes in water availability threaten to upend these established relationships. Using long-term data from three experiments in a mesic grassland (ranging from 17 to 34 yr of data), we tested how the effects of species richness and nitrogen addition on community-level plant productivity changed as a function of annual fluctuations in water availability using growing season precipitation and the Standardized Precipitation-Evapotranspiration Index (SPEI). While results varied across experiments, our findings demonstrate that water availability can magnify the positive effects of both biodiversity and nitrogen addition on productivity. These results suggest that productivity responses to anthropogenic species diversity loss and increasing nitrogen deposition could depend on precipitation regimes, highlighting the importance of testing interactions between multiple global change drivers.

Community diversity outweighs effect of warming on plant colonization.

Abiotic environmental change, local species extinctions and colonization of new species often co-occur. Whether species colonization is driven by changes in abiotic conditions or reduced biotic resistance will affect community functional composition and ecosystem management. We use a grassland experiment to disentangle effects of climate warming and community diversity on plant species colonization. Community diversity had dramatic impacts on the biomass, richness and traits of plant colonists. Three times as many species colonized the monocultures than the high diversity 17 species communities (~30 vs. 10 species), and colonists collectively produced 10 times as much biomass in the monocultures than the high diversity communities (~30 vs. 3 g/m2 ). Colonists with resource-acquisitive strategies (high specific leaf area, light seeds, short heights) accrued more biomass in low diversity communities, whereas species with conservative strategies accrued most biomass in high diversity communities. Communities with higher biomass of resident C4 grasses were more resistant to colonization by legume, nonlegume forb and C3 grass colonists, but not by C4 grass colonists. Compared with effects of diversity, 6 years of 3°C-above-ambient temperatures had little impact on plant colonization. Warmed subplots had ~3 fewer colonist species than ambient subplots and selected for heavier seeded colonists. They also showed diversity-dependent changes in biomass of C3 grass colonists, which decreased under low diversity and increased under high diversity. Our findings suggest that species colonization is more strongly affected by biotic resistance from residents than 3°C of climate warming. If these results were extended to invasive species management, preserving community diversity should help limit plant invasion, even under climate warming.

When Do Ecosystem Services Depend on Rare Species?

Conservation aims to preserve species and ecosystem services. If rare species contribute little to ecosystem services, yet are those most in need of preservation, tradeoffs may exist for these contrasting objectives. However, little attention has focused on identifying how, when, and where rare species contribute to ecosystem services and at what scales. Here, we review distinct ways that ecosystem services can positively depend on the presence, abundance, disproportionate contribution or, counterintuitively, the scarcity of rare species. By contrast, ecosystem services are less likely to depend on rare species that do not have a unique role in any service or become abundant enough to contribute substantially. We propose a research agenda to identify when rare species may contribute significantly to services.

Effects of increased temperature on plant communities depend on landscape location and precipitation.

Global climate change is affecting and will continue to affect ecosystems worldwide. Specifically, temperature and precipitation are both expected to shift globally, and their separate and interactive effects will likely affect ecosystems differentially depending on current temperature, precipitation regimes, and other biotic and environmental factors. It is not currently understood how the effects of increasing temperature on plant communities may depend on either precipitation or where communities lie on soil moisture gradients. Such knowledge would play a crucial role in increasing our predictive ability for future effects of climate change in different systems. To this end, we conducted a multi-factor global change experiment at two locations, differing in temperature, moisture, aspect, and plant community composition, on the same slope in the northern Mongolian steppe. The natural differences in temperature and moisture between locations served as a point of comparison for the experimental manipulations of temperature and precipitation. We conducted two separate experiments, one examining the effect of climate manipulation via open-top chambers (OTCs) across the two different slope locations, the other a factorial OTC by watering experiment at one of the two locations. By combining these experiments, we were able to assess how OTCs impact plant productivity and diversity across a natural and manipulated range of soil moisture. We found that warming effects were context dependent, with the greatest negative impacts of warming on diversity in the warmer, drier upper slope location and in the unwatered plots. Our study is an important step in understanding how global change will affect ecosystems across multiple scales and locations.

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.

Climate warming promotes species diversity, but with greater taxonomic redundancy, in complex environments.

Climate warming is predicted to alter species interactions, which could potentially lead to extinction events. However, there is an ongoing debate whether the effects of warming on biodiversity may be moderated by biodiversity itself. We tested warming effects on soil nematodes, one of the most diverse and abundant metazoans in terrestrial ecosystems, along a gradient of environmental complexity created by a gradient of plant species richness. Warming increased nematode species diversity in complex (16-species mixtures) plant communities (by ~36%) but decreased it in simple (monocultures) plant communities (by ~39%) compared to ambient temperature. Further, warming led to higher levels of taxonomic relatedness in nematode communities across all levels of plant species richness. Our results highlight both the need for maintaining species-rich plant communities to help offset detrimental warming effects and the inability of species-rich plant communities to maintain nematode taxonomic distinctness when warming occur.

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.

Shifting grassland plant community structure drives positive interactive effects of warming and diversity on aboveground net primary productivity.

Ecosystems worldwide are increasingly impacted by multiple drivers of environmental change, including climate warming and loss of biodiversity. We show, using a long-term factorial experiment, that plant diversity loss alters the effects of warming on productivity. Aboveground primary productivity was increased by both high plant diversity and warming, and, in concert, warming (≈1.5 °C average above and belowground warming over the growing season) and diversity caused a greater than additive increase in aboveground productivity. The aboveground warming effects increased over time, particularly at higher levels of diversity, perhaps because of warming-induced increases in legume and C4 bunch grass abundances, and facilitative feedbacks of these species on productivity. Moreover, higher plant diversity was associated with the amelioration of warming-induced environmental conditions. This led to cooler temperatures, decreased vapor pressure deficit, and increased surface soil moisture in higher diversity communities. Root biomass (0-30 cm) was likewise consistently greater at higher plant diversity and was greater with warming in monocultures and at intermediate diversity, but at high diversity warming had no detectable effect. This may be because warming increased the abundance of legumes, which have lower root : shoot ratios than the other types of plants. In addition, legumes increase soil nitrogen (N) supply, which could make N less limiting to other species and potentially decrease their investment in roots. The negative warming × diversity interaction on root mass led to an overall negative interactive effect of these two global change factors on the sum of above and belowground biomass, and thus likely on total plant carbon stores. In total, plant diversity increased the effect of warming on aboveground net productivity and moderated the effect on root mass. These divergent effects suggest that warming and changes in plant diversity are likely to have both interactive and divergent impacts on various aspects of ecosystem functioning.

Spatial convergent cross mapping to detect causal relationships from short time series.

Recent developments in complex systems analysis have led to new techniques for detecting causal relationships using relatively short time series, on the order of 30 sequential observations. Although many ecological observation series are even shorter, perhaps fewer than ten sequential observations, these shorter time series are often highly replicated in space (i.e., plot replication). Here, we combine the existing techniques of convergent cross mapping (CCM) and dewdrop regression to build a novel test of causal relations that leverages spatial replication, which we call multispatial CCM. Using examples from simulated and real-world ecological data, we test the ability of multispatial CCM to detect causal relationships between processes. We find that multispatial CCM successfully detects causal relationships with as few as five sequential observations, even in the presence of process noise and observation error. Our results suggest that this technique may constitute a useful test for causality in systems where experiments are difficult to perform and long time series are not available. This new technique is available in the multispatialCCM package for the R programming language.

Plant diversity effects on soil microbial functions and enzymes are stronger than warming in a grassland experiment.

Anthropogenic changes in biodiversity and atmospheric temperature significantly influence ecosystem processes. However, little is known about potential interactive effects of plant diversity and warming on essential ecosystem properties, such as soil microbial functions and element cycling. We studied the effects of orthogonal manipulations of plant diversity (one, four, and 16 species) and warming (ambient, +1.5 degrees C, and +3 degrees C) on soil microbial biomass, respiration, growth after nutrient additions, and activities of extracellular enzymes in 2011 and 2012 in the BAC (biodiversity and climate) perennial grassland experiment site at Cedar Creek, Minnesota, USA. Focal enzymes are involved in essential biogeochemical processes of the carbon, nitrogen, and phosphorus cycles. Soil microbial biomass and some enzyme activities involved in the C and N cycle increased significantly with increasing plant diversity in both years. In addition, 16-species mixtures buffered warming induced reductions in topsoil water content. We found no interactive effects of plant diversity and warming on soil microbial biomass and growth rates. However, the activity of several enzymes (1,4-beta-glucosidase, 1,4-beta-N-acetylglucosaminidase, phosphatase, peroxidase) depended on interactions between plant diversity and warming with elevated activities of enzymes involved in the C, N, and P cycles at both high plant diversity and high warming levels. Increasing plant diversity consistently decreased microbial biomass-specific enzyme activities and altered soil microbial growth responses to nutrient additions, indicating that plant diversity changed nutrient limitations and/or microbial community composition. In contrast to our expectations, higher plant diversity only buffered temperature effects on soil water content, but not on microbial functions. Temperature effects on some soil enzymes were greatest at high plant diversity. In total, our results suggest that the fundamental temperature ranges of soil microbial communities may be sufficiently broad to buffer their functioning against changes in temperature and that plant diversity may be a dominant control of soil microbial processes in a changing world.