Mechanistic Models of Trophic Interactions: Opportunities for Species Richness and Challenges for Modern Coexistence Theory.

AbstractMany potential mechanisms promote species coexistence, but we know little about their relative importance. To compare multiple mechanisms, we modeled a two-trophic planktonic food web based on mechanistic species interactions and empirically measured species traits. We simulated thousands of possible communities under realistic and altered interaction strengths to assess the relative importance of three potential drivers of phytoplankton and zooplankton species richness: resource-mediated coexistence mechanisms, predator-prey interactions, and trait trade-offs. Next, we computed niche and fitness differences of competing zooplankton to obtain a deeper understanding of how these mechanisms determine species richness. We found that predator-prey interactions were the most important driver of phytoplankton and zooplankton species richness and that large zooplankton fitness differences were associated with low species richness, but zooplankton niche differences were not associated with species richness. However, for many communities we could not apply modern coexistence theory to compute niche and fitness differences of zooplankton because of conceptual issues with the invasion growth rates arising from trophic interactions. We therefore need to expand modern coexistence theory to fully investigate multitrophic-level communities.

Beyond pairwise mechanisms of species coexistence in complex communities.

The tremendous diversity of species in ecological communities has motivated a century of research into the mechanisms that maintain biodiversity. However, much of this work examines the coexistence of just pairs of competitors. This approach ignores those mechanisms of coexistence that emerge only in diverse competitive networks. Despite the potential for these mechanisms to create conditions under which the loss of one competitor triggers the loss of others, we lack the knowledge needed to judge their importance for coexistence in nature. Progress requires borrowing insight from the study of multitrophic interaction networks, and coupling empirical data to models of competition.

Synchrony matters more than species richness in plant community stability at a global scale.

The stability of ecological communities is critical for the stable provisioning of ecosystem services, such as food and forage production, carbon sequestration, and soil fertility. Greater biodiversity is expected to enhance stability across years by decreasing synchrony among species, but the drivers of stability in nature remain poorly resolved. Our analysis of time series from 79 datasets across the world showed that stability was associated more strongly with the degree of synchrony among dominant species than with species richness. The relatively weak influence of species richness is consistent with theory predicting that the effect of richness on stability weakens when synchrony is higher than expected under random fluctuations, which was the case in most communities. Land management, nutrient addition, and climate change treatments had relatively weak and varying effects on stability, modifying how species richness, synchrony, and stability interact. Our results demonstrate the prevalence of biotic drivers on ecosystem stability, with the potential for environmental drivers to alter the intricate relationship among richness, synchrony, and stability.

Climate disequilibrium dominates uncertainty in long-term projections of primary productivity.

Rapid climate change may exceed ecosystems' capacities to respond through processes including phenotypic plasticity, compositional turnover and evolutionary adaption. However, consequences of the resulting climate disequilibria for ecosystem functioning are rarely considered in projections of climate change impacts. Combining statistical models fit to historical climate data and remotely-sensed estimates of herbaceous net primary productivity with an ensemble of climate models, we demonstrate that assumptions concerning the magnitude of climate disequilibrium are a dominant source of uncertainty: models assuming maximum disequilibrium project widespread decreases in productivity in the western US by 2100, while models assuming minimal disequilibrium project productivity increases. Uncertainty related to climate disequilibrium is larger than uncertainties from variation among climate models or emissions pathways. A better understanding of processes that regulate climate disequilibria is essential for improving long-term projections of ecological responses and informing management to maintain ecosystem functioning at historical baselines.

Nutrient identity modifies the destabilising effects of eutrophication in grasslands.

Nutrient enrichment can simultaneously increase and destabilise plant biomass production, with co-limitation by multiple nutrients potentially intensifying these effects. Here, we test how factorial additions of nitrogen (N), phosphorus (P) and potassium with essential nutrients (K+) affect the stability (mean/standard deviation) of aboveground biomass in 34 grasslands over 7 years. Destabilisation with fertilisation was prevalent but was driven by single nutrients, not synergistic nutrient interactions. On average, N-based treatments increased mean biomass production by 21-51% but increased its standard deviation by 40-68% and so consistently reduced stability. Adding P increased interannual variability and reduced stability without altering mean biomass, while K+ had no general effects. Declines in stability were largest in the most nutrient-limited grasslands, or where nutrients reduced species richness or intensified species synchrony. We show that nutrients can differentially impact the stability of biomass production, with N and P in particular disproportionately increasing its interannual variability.

Integrative modelling reveals mechanisms linking productivity and plant species richness.

How ecosystem productivity and species richness are interrelated is one of the most debated subjects in the history of ecology. Decades of intensive study have yet to discern the actual mechanisms behind observed global patterns. Here, by integrating the predictions from multiple theories into a single model and using data from 1,126 grassland plots spanning five continents, we detect the clear signals of numerous underlying mechanisms linking productivity and richness. We find that an integrative model has substantially higher explanatory power than traditional bivariate analyses. In addition, the specific results unveil several surprising findings that conflict with classical models. These include the isolation of a strong and consistent enhancement of productivity by richness, an effect in striking contrast with superficial data patterns. Also revealed is a consistent importance of competition across the full range of productivity values, in direct conflict with some (but not all) proposed models. The promotion of local richness by macroecological gradients in climatic favourability, generally seen as a competing hypothesis, is also found to be important in our analysis. The results demonstrate that an integrative modelling approach leads to a major advance in our ability to discern the underlying processes operating in ecological systems.

Addition of multiple limiting resources reduces grassland diversity.

Niche dimensionality provides a general theoretical explanation for biodiversity-more niches, defined by more limiting factors, allow for more ways that species can coexist. Because plant species compete for the same set of limiting resources, theory predicts that addition of a limiting resource eliminates potential trade-offs, reducing the number of species that can coexist. Multiple nutrient limitation of plant production is common and therefore fertilization may reduce diversity by reducing the number or dimensionality of belowground limiting factors. At the same time, nutrient addition, by increasing biomass, should ultimately shift competition from belowground nutrients towards a one-dimensional competitive trade-off for light. Here we show that plant species diversity decreased when a greater number of limiting nutrients were added across 45 grassland sites from a multi-continent experimental network. The number of added nutrients predicted diversity loss, even after controlling for effects of plant biomass, and even where biomass production was not nutrient-limited. We found that elevated resource supply reduced niche dimensionality and diversity and increased both productivity and compositional turnover. Our results point to the importance of understanding dimensionality in ecological systems that are undergoing diversity loss in response to multiple global change factors.

Species loss due to nutrient addition increases with spatial scale in global grasslands.

The effects of altered nutrient supplies and herbivore density on species diversity vary with spatial scale, because coexistence mechanisms are scale dependent. This scale dependence may alter the shape of the species-area relationship (SAR), which can be described by changes in species richness (S) as a power function of the sample area (A): S = cAz , where c and z are constants. We analysed the effects of experimental manipulations of nutrient supply and herbivore density on species richness across a range of scales (0.01-75 m2 ) at 30 grasslands in 10 countries. We found that nutrient addition reduced the number of species that could co-occur locally, indicated by the SAR intercepts (log c), but did not affect the SAR slopes (z). As a result, proportional species loss due to nutrient enrichment was largely unchanged across sampling scales, whereas total species loss increased over threefold across our range of sampling scales.

Biotic vs abiotic controls on temporal sensitivity of primary production to precipitation across North American drylands.

Dryland net primary productivity (NPP) is sensitive to temporal variation in precipitation (PPT), but the magnitude of this 'temporal sensitivity' varies spatially. Hypotheses for spatial variation in temporal sensitivity have often emphasized abiotic factors, such as moisture limitation, while overlooking biotic factors, such as vegetation structure. We tested these hypotheses using spatiotemporal models fit to remote-sensing data sets to assess how vegetation structure and climate influence temporal sensitivity across five dryland ecoregions of the western USA. Temporal sensitivity was higher in locations and ecoregions dominated by herbaceous vegetation. By contrast, much less spatial variation in temporal sensitivity was explained by mean annual PPT. In fact, ecoregion-specific models showed inconsistent associations of sensitivity and PPT; whereas sensitivity decreased with increasing mean annual PPT in most ecoregions, it increased with mean annual PPT in the most arid ecoregion, the hot deserts. The strong, positive influence of herbaceous vegetation on temporal sensitivity indicates that herbaceous-dominated drylands will be particularly sensitive to future increases in precipitation variability and that dramatic changes in cover type caused by invasions or shrub encroachment will lead to changes in dryland NPP dynamics, perhaps independent of changes in precipitation.

Technical Comment on Pande et al. (2020): Why invasion analysis is important for understanding coexistence.

Pande et al. (2020) point out that persistence time can decrease even as invader growth rates (IGRs) increase, which potentially undermines modern coexistence theory. However, because persistence time increases rapidly with system size only when IGR > 0, to understand how any real community persists, we should first identify the mechanisms producing positive IGR.

What processes must we understand to forecast regional-scale population dynamics?

An urgent challenge facing biologists is predicting the regional-scale population dynamics of species facing environmental change. Biologists suggest that we must move beyond predictions based on phenomenological models and instead base predictions on underlying processes. For example, population biologists, evolutionary biologists, community ecologists and ecophysiologists all argue that the respective processes they study are essential. Must our models include processes from all of these fields? We argue that answering this critical question is ultimately an empirical exercise requiring a substantial amount of data that have not been integrated for any system to date. To motivate and facilitate the necessary data collection and integration, we first review the potential importance of each mechanism for skilful prediction. We then develop a conceptual framework based on reaction norms, and propose a hierarchical Bayesian statistical framework to integrate processes affecting reaction norms at different scales. The ambitious research programme we advocate is rapidly becoming feasible due to novel collaborations, datasets and analytical tools.

Nutrient availability controls the impact of mammalian herbivores on soil carbon and nitrogen pools in grasslands.

Grasslands are subject to considerable alteration due to human activities globally, including widespread changes in populations and composition of large mammalian herbivores and elevated supply of nutrients. Grassland soils remain important reservoirs of carbon (C) and nitrogen (N). Herbivores may affect both C and N pools and these changes likely interact with increases in soil nutrient availability. Given the scale of grassland soil fluxes, such changes can have striking consequences for atmospheric C concentrations and the climate. Here, we use the Nutrient Network experiment to examine the responses of soil C and N pools to mammalian herbivore exclusion across 22 grasslands, under ambient and elevated nutrient availabilities (fertilized with NPK + micronutrients). We show that the impact of herbivore exclusion on soil C and N pools depends on fertilization. Under ambient nutrient conditions, we observed no effect of herbivore exclusion, but under elevated nutrient supply, pools are smaller upon herbivore exclusion. The highest mean soil C and N pools were found in grazed and fertilized plots. The decrease in soil C and N upon herbivore exclusion in combination with fertilization correlated with a decrease in aboveground plant biomass and microbial activity, indicating a reduced storage of organic matter and microbial residues as soil C and N. The response of soil C and N pools to herbivore exclusion was contingent on temperature - herbivores likely cause losses of C and N in colder sites and increases in warmer sites. Additionally, grasslands that contain mammalian herbivores have the potential to sequester more N under increased temperature variability and nutrient enrichment than ungrazed grasslands. Our study highlights the importance of conserving mammalian herbivore populations in grasslands worldwide. We need to incorporate local-scale herbivory, and its interaction with nutrient enrichment and climate, within global-scale models to better predict land-atmosphere interactions under future climate change.

Global impacts of fertilization and herbivore removal on soil net nitrogen mineralization are modulated by local climate and soil properties.

Soil nitrogen (N) availability is critical for grassland functioning. However, human activities have increased the supply of biologically limiting nutrients, and changed the density and identity of mammalian herbivores. These anthropogenic changes may alter net soil N mineralization (soil net Nmin ), that is, the net balance between N mineralization and immobilization, which could severely impact grassland structure and functioning. Yet, to date, little is known about how fertilization and herbivore removal individually, or jointly, affect soil net Nmin across a wide range of grasslands that vary in soil and climatic properties. Here we collected data from 22 grasslands on five continents, all part of a globally replicated experiment, to assess how fertilization and herbivore removal affected potential (laboratory-based) and realized (field-based) soil net Nmin . Herbivore removal in the absence of fertilization did not alter potential and realized soil net Nmin . However, fertilization alone and in combination with herbivore removal consistently increased potential soil net Nmin. Realized soil net Nmin , in contrast, significantly decreased in fertilized plots where herbivores were removed. Treatment effects on potential and realized soil net Nmin were contingent on site-specific soil and climatic properties. Fertilization effects on potential soil net Nmin were larger at sites with higher mean annual precipitation (MAP) and temperature of the wettest quarter (T.q.wet). Reciprocally, realized soil net Nmin declined most strongly with fertilization and herbivore removal at sites with lower MAP and higher T.q.wet. In summary, our findings show that anthropogenic nutrient enrichment, herbivore exclusion and alterations in future climatic conditions can negatively impact soil net Nmin across global grasslands under realistic field conditions. This is an important context-dependent knowledge for grassland management worldwide.

Eutrophication weakens stabilizing effects of diversity in natural grasslands.

Studies of experimental grassland communities have demonstrated that plant diversity can stabilize productivity through species asynchrony, in which decreases in the biomass of some species are compensated for by increases in others. However, it remains unknown whether these findings are relevant to natural ecosystems, especially those for which species diversity is threatened by anthropogenic global change. Here we analyse diversity-stability relationships from 41 grasslands on five continents and examine how these relationships are affected by chronic fertilization, one of the strongest drivers of species loss globally. Unmanipulated communities with more species had greater species asynchrony, resulting in more stable biomass production, generalizing a result from biodiversity experiments to real-world grasslands. However, fertilization weakened the positive effect of diversity on stability. Contrary to expectations, this was not due to species loss after eutrophication but rather to an increase in the temporal variation of productivity in combination with a decrease in species asynchrony in diverse communities. Our results demonstrate separate and synergistic effects of diversity and eutrophication on stability, emphasizing the need to understand how drivers of global change interactively affect the reliable provisioning of ecosystem services in real-world systems.

Herbivores and nutrients control grassland plant diversity via light limitation.

Human alterations to nutrient cycles and herbivore communities are affecting global biodiversity dramatically. Ecological theory predicts these changes should be strongly counteractive: nutrient addition drives plant species loss through intensified competition for light, whereas herbivores prevent competitive exclusion by increasing ground-level light, particularly in productive systems. Here we use experimental data spanning a globally relevant range of conditions to test the hypothesis that herbaceous plant species losses caused by eutrophication may be offset by increased light availability due to herbivory. This experiment, replicated in 40 grasslands on 6 continents, demonstrates that nutrients and herbivores can serve as counteracting forces to control local plant diversity through light limitation, independent of site productivity, soil nitrogen, herbivore type and climate. Nutrient addition consistently reduced local diversity through light limitation, and herbivory rescued diversity at sites where it alleviated light limitation. Thus, species loss from anthropogenic eutrophication can be ameliorated in grasslands where herbivory increases ground-level light.

An expanded modern coexistence theory for empirical applications.

Understanding long-term coexistence of numerous competing species is a longstanding challenge in ecology. Progress requires determining which processes and species differences are most important for coexistence when multiple processes operate and species differ in many ways. Modern coexistence theory (MCT), formalised by Chesson, holds out the promise of doing that, but empirical applications remain scarce. We argue that MCT's mathematical complexity and subtlety have obscured the simplicity and power of its underlying ideas and hindered applications. We present a general computational approach that extends our previous solution for the storage effect to all of standard MCT's spatial and temporal coexistence mechanisms, and also process-defined mechanisms amenable to direct study such as resource partitioning, indirect competition, and life history trade-offs. The main components are a method to partition population growth rates into contributions from different mechanisms and their interactions, and numerical calculations in which some mechanisms are removed and others retained. We illustrate how our approach handles features that have not been analysed in the standard framework through several case studies: competing diatom species under fluctuating temperature, plant-soil feedbacks in grasslands, facilitation in a beach grass community, and niche differences with independent effects on recruitment, survival and growth in sagebrush steppe.

Size-by-environment interactions: a neglected dimension of species' responses to environmental variation.

In both plant and animal systems, size can determine whether an individual survives and grows under different environmental conditions. However, it is unclear whether and when size-dependent responses to exogenous environmental fluctuations affect population dynamics. Size-by-environment interactions create pathways for environmental fluctuations to influence population dynamics by allowing for negative covariation between sizes within vital rates (e.g. small and large individuals have negatively covarying survival rates) and/or size-dependent variability in a vital rate (e.g. survival of large individuals varies less than small individuals through time). Whether these phenomena affect population dynamics depends on how they are mediated by elasticities (they must affect the sizes and vital rates that matter) and their projected impacts will depend on model functional form (the impact of reduced variance depends on the relationship between the environment and vital rate). We demonstrate these ideas with an analysis of fifteen species from five semiarid plant communities. We find that size-by-environment interactions are common but do not impact long-term population dynamics. Size-by-environment interactions may yet be important for other species. Our approach can be applied to species in other ecosystems to determine if and how size-by-environment interactions allow them to cope with, or exploit, fluctuating environments.

Survival rates indicate that correlations between community-weighted mean traits and environments can be unreliable estimates of the adaptive value of traits.

Correlations between community-weighted mean (CWM) traits and environmental gradients are often assumed to quantify the adaptive value of traits. We tested this assumption by comparing these correlations with models of survival probability using 46 perennial species from long-term permanent plots in pine forests of Arizona. Survival was modelled as a function of trait × environment interactions, plant size, climatic variation and neighbourhood competition. The effect of traits on survival depended on the environmental conditions, but the two statistical approaches were inconsistent. For example, CWM-specific leaf area (SLA) and soil fertility were uncorrelated. However, survival was highest for species with low SLA in infertile soil, a result which agreed with expectations derived from the physiological trade-off underpinning leaf economic theory. CWM trait-environment relationships were unreliable estimates of how traits affected survival, and should only be used in predictive models when there is empirical support for an evolutionary trade-off that affects vital rates.

Competition and coexistence in plant communities: intraspecific competition is stronger than interspecific competition.

Theory predicts that intraspecific competition should be stronger than interspecific competition for any pair of stably coexisting species, yet previous literature reviews found little support for this pattern. We screened over 5400 publications and identified 39 studies that quantified phenomenological intraspecific and interspecific interactions in terrestrial plant communities. Of the 67% of species pairs in which both intra- and interspecific effects were negative (competitive), intraspecific competition was, on average, four to five-fold stronger than interspecific competition. Of the remaining pairs, 93% featured intraspecific competition and interspecific facilitation, a situation that stabilises coexistence. The difference between intra- and interspecific effects tended to be larger in observational than experimental data sets, in field than greenhouse studies, and in studies that quantified population growth over the full life cycle rather than single fitness components. Our results imply that processes promoting stable coexistence at local scales are common and consequential across terrestrial plant communities.

Spatial heterogeneity in species composition constrains plant community responses to herbivory and fertilisation.

Environmental change can result in substantial shifts in community composition. The associated immigration and extinction events are likely constrained by the spatial distribution of species. Still, studies on environmental change typically quantify biotic responses at single spatial (time series within a single plot) or temporal (spatial beta diversity at single time points) scales, ignoring their potential interdependence. Here, we use data from a global network of grassland experiments to determine how turnover responses to two major forms of environmental change - fertilisation and herbivore loss - are affected by species pool size and spatial compositional heterogeneity. Fertilisation led to higher rates of local extinction, whereas turnover in herbivore exclusion plots was driven by species replacement. Overall, sites with more spatially heterogeneous composition showed significantly higher rates of annual turnover, independent of species pool size and treatment. Taking into account spatial biodiversity aspects will therefore improve our understanding of consequences of global and anthropogenic change on community dynamics.