Biodiversity increases and decreases ecosystem stability.

Losses and gains in species diversity affect ecological stability1-7 and the sustainability of ecosystem functions and services8-13. Experiments and models have revealed positive, negative and no effects of diversity on individual components of stability, such as temporal variability, resistance and resilience2,3,6,11,12,14. How these stability components covary remains poorly understood15. Similarly, the effects of diversity on overall ecosystem stability16, which is conceptually akin to ecosystem multifunctionality17,18, remain unknown. Here we studied communities of aquatic ciliates to understand how temporal variability, resistance and overall ecosystem stability responded to diversity (that is, species richness) in a large experiment involving 690 micro-ecosystems sampled 19 times over 40 days, resulting in 12,939 samplings. Species richness increased temporal stability but decreased resistance to warming. Thus, two stability components covaried negatively along the diversity gradient. Previous biodiversity manipulation studies rarely reported such negative covariation despite general predictions of the negative effects of diversity on individual stability components3. Integrating our findings with the ecosystem multifunctionality concept revealed hump- and U-shaped effects of diversity on overall ecosystem stability. That is, biodiversity can increase overall ecosystem stability when biodiversity is low, and decrease it when biodiversity is high, or the opposite with a U-shaped relationship. The effects of diversity on ecosystem multifunctionality would also be hump- or U-shaped if diversity had positive effects on some functions and negative effects on others. Linking the ecosystem multifunctionality concept and ecosystem stability can transform the perceived effects of diversity on ecological stability and may help to translate this science into policy-relevant information.

Functional diversity can facilitate the collapse of an undesirable ecosystem state.

Biodiversity may increase ecosystem resilience. However, we have limited understanding if this holds true for ecosystems that respond to gradual environmental change with abrupt shifts to an alternative state. We used a mathematical model of anoxic-oxic regime shifts and explored how trait diversity in three groups of bacteria influences resilience. We found that trait diversity did not always increase resilience: greater diversity in two of the groups increased but in one group decreased resilience of their preferred ecosystem state. We also found that simultaneous trait diversity in multiple groups often led to reduced or erased diversity effects. Overall, our results suggest that higher diversity can increase resilience but can also promote collapse when diversity occurs in a functional group that negatively influences the state it occurs in. We propose this mechanism as a potential management approach to facilitate the recovery of a desired ecosystem state.

Failures to disagree are essential for environmental science to effectively influence policy development.

While environmental science, and ecology in particular, is working to provide better understanding to base sustainable decisions on, the way scientific understanding is developed can at times be detrimental to this cause. Locked-in debates are often unnecessarily polarised and can compromise any common goals of the opposing camps. The present paper is inspired by a resolved debate from an unrelated field of psychology where Nobel laureate David Kahneman and Garry Klein turned what seemed to be a locked-in debate into a constructive process for their fields. The present paper is also motivated by previous discourses regarding the role of thresholds in natural systems for management and governance, but its scope of analysis targets the scientific process within complex social-ecological systems in general. We identified four features of environmental science that appear to predispose for locked-in debates: (1) The strongly context-dependent behaviour of ecological systems. (2) The dominant role of single hypothesis testing. (3) The high prominence given to theory demonstration compared investigation. (4) The effect of urgent demands to inform and steer policy. This fertile ground is further cultivated by human psychological aspects as well as the structure of funding and publication systems.

Forecasting in the face of ecological complexity: Number and strength of species interactions determine forecast skill in ecological communities.

The potential for forecasting the dynamics of ecological systems is currently unclear, with contrasting opinions regarding its feasibility due to ecological complexity. To investigate forecast skill within and across systems, we monitored a microbial system exposed to either constant or fluctuating temperatures in a 5-month-long laboratory experiment. We tested how forecasting of species abundances depends on the number and strength of interactions and on model size (number of predictors). We also tested how greater system complexity (i.e. the fluctuating temperatures) impacted these relations. We found that the more interactions a species had, the weaker these interactions were and the better its abundance was predicted. Forecast skill increased with model size. Greater system complexity decreased forecast skill for three out of eight species. These insights into how abundance prediction depends on the connectedness of the species within the system and on overall system complexity could improve species forecasting and monitoring.

Biodiversity promotes ecosystem functioning despite environmental change.

Three decades of research have demonstrated that biodiversity can promote the functioning of ecosystems. Yet, it is unclear whether the positive effects of biodiversity on ecosystem functioning will persist under various types of global environmental change drivers. We conducted a meta-analysis of 46 factorial experiments manipulating both species richness and the environment to test how global change drivers (i.e. warming, drought, nutrient addition or CO2 enrichment) modulated the effect of biodiversity on multiple ecosystem functions across three taxonomic groups (microbes, phytoplankton and plants). We found that biodiversity increased ecosystem functioning in both ambient and manipulated environments, but often not to the same degree. In particular, biodiversity effects on ecosystem functioning were larger in stressful environments induced by global change drivers, indicating that high-diversity communities were more resistant to environmental change. Using a subset of studies, we also found that the positive effects of biodiversity were mainly driven by interspecific complementarity and that these effects increased over time in both ambient and manipulated environments. Our findings support biodiversity conservation as a key strategy for sustainable ecosystem management in the face of global environmental change.

Predicting the effects of multiple global change drivers on microbial communities remains challenging.

Microbial communities in many ecosystems are facing a broad range of global change drivers, such as nutrient enrichment, chemical pollution, and temperature change. These drivers can cause changes in the abundance of taxa, the composition of communities, and the properties of ecosystems. While the influence of single drivers is already described in numerous studies, the effect and predictability of multiple drivers changing simultaneously is still poorly understood. In this study, we used 240 highly replicable oxic/anoxic aquatic lab microcosms and four drivers (fertilizer, glyphosate, metal pollution, antibiotics) in all possible combinations at three different temperatures (20, 24, and 28°C) to shed light into consequences of multiple drivers on different levels of organization, ranging from species abundance to community and ecosystem parameters. We found (i) that at all levels of ecological organization, combinations of drivers can change the biological consequence and direction of effect compared to single drivers, (ii) that effects of combinations are further modified by temperature, (iii) that a larger number of drivers occurring simultaneously is often quite closely related to their effect size, and (iv) that there is little evidence that any of these effects are associated with the level of ecological organization of the state variable. These findings suggest that, at least in this experimental ecosystem approximating a stratified aquatic ecosystem, there may be relatively little scope for predicting the effects of combinations of drivers from the effects of individual drivers, or by accounting for the level of ecological organization in question, though there may be some scope for prediction based on the number of drivers that are occurring simultaneous. A priority, though also a considerable challenge, is to extend such research to consider continuous variation in the magnitude of multiple drivers acting together.

Warming and top predator loss drive direct and indirect effects on multiple trophic groups within and across ecosystems.

The interspecific interactions within and between adjacent ecosystems strongly depend on the changes in their abiotic and biotic components. However, little is known about how climate change and biodiversity loss in a specific ecosystem can impact the multiple trophic interactions of different biological groups within and across ecosystems. We used natural microecosystems (tank-bromeliads) as a model system to investigate the main and interactive effects of aquatic warming and aquatic top predator loss (i.e. trophic downgrading) on trophic relationships in three integrated food web compartments: (a) aquatic micro-organisms, (b) aquatic macro-organisms and (c) terrestrial predators (i.e. via cross-ecosystem effects). The aquatic top predator loss substantially impacted the three food web compartments. In the aquatic macrofauna compartment, trophic downgrading increased the filter feeder richness and abundance directly and indirectly via an increase in detritivore richness, likely through a facilitative interaction. For the microbiota compartment, aquatic top predator loss had a negative effect on algae richness, probably via decreasing the input of nutrients from predator biological activities. Furthermore, the more active terrestrial predators responded more to aquatic top predator loss, via an increase in some components of aquatic macrofauna, than more stationary terrestrial predators. The aquatic trophic downgrading indirectly altered the richness and abundance of cursorial terrestrial predators, but these effects had different direction according to the aquatic functional group, filter feeder or other detritivores. The web-building predators were indirectly affected by aquatic trophic downgrading due to increased filter feeder richness. Aquatic warming did not affect the aquatic micro- or macro-organisms but did positively affect the abundance of web-building terrestrial predators. These results allow us to raise a predictive framework of how different anthropogenic changes predicted for the next decades, such as aquatic warming and top predator loss, could differentially affect multiple biological groups through interactions within and across ecosystems.

As interações interespecíficas dentro e entre ecossistemas adjacentes dependem fortemente das mudanças de seus componentes abióticos e bióticos. Entretanto, pouco se sabe sobre como mudanças climáticas e a perda de biodiversidade em um ecossistema específico pode impactar as múltiplas interações tróficas de diferentes grupos biológicos dentro e entre ecossistemas. Nós utilizamos micro ecossistemas naturais (bromélias-tanque) como sistema modelo para investigar os efeitos individuais e interativos do aquecimento e da perda de predadores aquáticos (simplificação trófica) nas relações tróficas em três compartimentos integrados da teia alimentar: i) micro-organismos aquáticos, ii) macroorganismos aquáticos e iii) predadores terrestres (via efeito entre ecossistemas). A perda de predadores de topo aquáticos afetou substancialmente os três compartimentos da rede trófica. No compartimento da macrofauna aquática, a simplificação trófica aumentou a riqueza e abundância de filtradores, direta e indiretamente, por meio de um aumento da riqueza de espécies de detritívoros, provavelmente através de uma interação de facilitação. Para o compartimento da microbiota, a perda de predadores de topo aquáticos teve um efeito negativo sobre a riqueza de espécies de algas, provavelmente por meio da diminuição da entrada de nutrientes provenientes das atividades biológicas dos predadores. Além disso, os predadores terrestres mais ativos responderam mais à perda de predadores de topo aquáticos, por meio de um aumento de alguns componentes da macrofauna aquática, do que predadores terrestres mais estacionários. A simplificação trófica aquática alterou indiretamente a riqueza e abundância de predadores cursoriais terrestres, mas esses efeitos tiveram direção diferente de acordo com o grupo funcional aquático, filtradores ou outros detritívoros. Os predadores construtores de teias foram indiretamente afetados pela simplificação trófica aquática devido ao aumento da riqueza de filtradores. O aquecimento aquático não afetou os micro ou macro organismos aquáticos, mas afetou positivamente a abundância de predadores terrestres construtores de teias. Esses resultados nos permitem levantar um quadro preditivo de como diferentes mudanças antropogênicas preditas para as próximas décadas, como o aquecimento e a perda de predadores de topo aquáticos, podem afetar diferencialmente vários grupos biológicos por meio de interações dentro e entre os ecossistemas.

Trophic downgrading decreases species asynchrony and community stability regardless of climate warming.

Theory and some evidence suggest that biodiversity promotes stability. However, evidence of how trophic interactions and environmental changes modulate this relationship in multitrophic communities is lacking. Given the current scenario of biodiversity loss and climate changes, where top predators are disproportionately more affected, filling these knowledge gaps is crucial. We simulated climate warming and top predator loss in natural microcosms to investigate their direct and indirect effects on temporal stability of microbial communities and the role of underlying stabilising mechanisms. Community stability was insensitive to warming, but indirectly decreased due to top predator loss via increased mesopredator abundance and consequent reduction of species asynchrony and species stability. The magnitude of destabilising effects differed among trophic levels, being disproportionally higher at lower trophic levels (e.g. producers). Our study unravels major patterns and causal mechanisms by which trophic downgrading destabilises large food webs, regardless of climate warming scenarios.

Warming reduces the effects of enrichment on stability and functioning across levels of organisation in an aquatic microbial ecosystem.

Warming and nutrient enrichment are major environmental factors shaping ecological dynamics. However, cross-scale investigation of their combined effects by linking theory and experiments is lacking. We collected data from aquatic microbial ecosystems investigating the interactive effects of warming (constant and rising temperatures) and enrichment across levels of organisation and contrasted them with community models based on metabolic theory. We found high agreement between our observations and theoretical predictions: we observed in many cases the predicted antagonistic effects of high temperature and high enrichment across levels of organisation. Temporal stability of total biomass decreased with warming but did not differ across enrichment levels. Constant and rising temperature treatments with identical mean temperature did not show qualitative differences. Overall, we conclude that model and empirical results are in broad agreement due to robustness of the effects of temperature and enrichment, that the mitigating effects of temperature on effects of enrichment may be common, and that models based on metabolic theory provide qualitatively robust predictions of the combined ecological effects of enrichment and temperature.

Warming can destabilize predator-prey interactions by shifting the functional response from Type III to Type II.

The potential for climate change and temperature shifts to affect community stability remains relatively unknown. One mechanism by which temperature may affect stability is by altering trophic interactions. The functional response quantifies the per capita resource consumption by the consumer as a function of resource abundance and is a suitable framework for the description of nonlinear trophic interactions. We studied the effect of temperature on a ciliate predator-prey pair (Spathidium sp. and Dexiostoma campylum) by estimating warming effects on the functional response and on the associated conversion efficiency of the predator. We recorded prey and predator dynamics over 24 hr and at three temperature levels (15, 20 and 25°C). To these data, we fitted a population dynamic model including the predator functional response, such that the functional response parameters (space clearance rate, handling time and density dependence of space clearance rate) were estimated for each temperature separately. To evaluate the ecological significance of temperature effects on the functional response parameters, we simulated predator-prey population dynamics. We considered the predator-prey system to be destabilized, if the prey was driven extinct by the predator. Effects of increased temperature included a transition of the functional response from a Type III to a Type II and an increase of the conversion efficiency of the predator. The simulated population dynamics showed a destabilization of the system with warming, with greater risk of prey extinction at higher temperatures likely caused by the transition from a Type III to a Type II functional response. Warming-induced shifts from a Type III to II are not commonly considered in modelling studies that investigate how population dynamics respond to warming. Future studies should investigate the mechanism and generality of the effect we observed and simulate temperature effects in complex food webs including shifts in the type of the functional response as well as consider the possibility of a temperature-dependent conversion efficiency.

Warming and top predator loss drive ecosystem multifunctionality.

Global change affects ecosystem functioning both directly by modifications in physicochemical processes, and indirectly, via changes in biotic metabolism and interactions. Unclear, however, is how multiple anthropogenic drivers affect different components of community structure and the performance of multiple ecosystem functions (ecosystem multifunctionality). We manipulated small natural freshwater ecosystems to investigate how warming and top predator loss affect seven ecosystem functions representing two major dimensions of ecosystem functioning, productivity and metabolism. We investigated their direct and indirect effects on community diversity and standing stock of multitrophic macro and microorganisms. Warming directly increased multifunctional ecosystem productivity and metabolism. In contrast, top predator loss indirectly affected multifunctional ecosystem productivity via changes in the diversity of detritivorous macroinvertebrates, but did not affect ecosystem metabolism. In addition to demonstrating how multiple anthropogenic drivers have different impacts, via different pathways, on ecosystem multifunctionality components, our work should further spur advances in predicting responses of ecosystems to multiple simultaneous environmental changes.

Ecological opportunity and predator-prey interactions: linking eco-evolutionary processes and diversification in adaptive radiations.

Much of life's diversity has arisen through ecological opportunity and adaptive radiations, but the mechanistic underpinning of such diversification is not fully understood. Competition and predation can affect adaptive radiations, but contrasting theoretical and empirical results show that they can both promote and interrupt diversification. A mechanistic understanding of the link between microevolutionary processes and macroevolutionary patterns is thus needed, especially in trophic communities. Here, we use a trait-based eco-evolutionary model to investigate the mechanisms linking competition, predation and adaptive radiations. By combining available micro-evolutionary theory and simulations of adaptive radiations we show that intraspecific competition is crucial for diversification as it induces disruptive selection, in particular in early phases of radiation. The diversification rate is however decreased in later phases owing to interspecific competition as niche availability, and population sizes are decreased. We provide new insight into how predation tends to have a negative effect on prey diversification through decreased population sizes, decreased disruptive selection and through the exclusion of prey from parts of niche space. The seemingly disparate effects of competition and predation on adaptive radiations, listed in the literature, may thus be acting and interacting in the same adaptive radiation at different relative strength as the radiation progresses.

Environmental change and predator diversity drive alpha and beta diversity in freshwater macro and microorganisms.

Global biodiversity is eroding due to anthropogenic causes, such as climate change, habitat loss, and trophic simplification of biological communities. Most studies address only isolated causes within a single group of organisms; however, biological groups of different trophic levels may respond in particular ways to different environmental impacts. Our study used natural microcosms to investigate the predicted individual and interactive effects of warming, changes in top predator diversity, and habitat size on the alpha and beta diversity of macrofauna, microfauna, and bacteria. Alpha diversity (i.e., richness within each bromeliad) generally explained a larger proportion of the gamma diversity (partitioned in alpha and beta diversity). Overall, dissimilarity between communities occurred due to species turnover and not species loss (nestedness). Nevertheless, the three biological groups responded differently to each environmental stressor. Microfauna were the most sensitive group, with alpha and beta diversity being affected by environmental changes (warming and habitat size) and trophic structure (diversity of top predators). Macrofauna alpha and beta diversity was sensitive to changes in predator diversity and habitat size, but not warming. In contrast, the bacterial community was not influenced by the treatments. The community of each biological group was not mutually concordant with the environmental and trophic changes. Our results demonstrate that distinct anthropogenic impacts differentially affect the components of macro and microorganism diversity through direct and indirect effects (i.e., bottom-up and top-down effects). Therefore, a multitrophic and multispecies approach is necessary to assess the effects of different anthropogenic impacts on biodiversity.

Temporal scale dependent interactions between multiple environmental disturbances in microcosm ecosystems.

Global environmental change has negative impacts on ecological systems, impacting the stable provision of functions, goods, and services. Whereas effects of individual environmental changes (e.g. temperature change or change in resource availability) are reasonably well understood, we lack information about if and how multiple changes interact. We examined interactions among four types of environmental disturbance (temperature, nutrient ratio, carbon enrichment, and light) in a fully factorial design using a microbial aquatic ecosystem and observed responses of dissolved oxygen saturation at three temporal scales (resistance, resilience, and return time). We tested whether multiple disturbances combine in a dominant, additive, or interactive fashion, and compared the predictability of dissolved oxygen across scales. Carbon enrichment and shading reduced oxygen concentration in the short term (i.e. resistance); although no other effects or interactions were statistically significant, resistance decreased as the number of disturbances increased. In the medium term, only enrichment accelerated recovery, but none of the other effects (including interactions) were significant. In the long term, enrichment and shading lengthened return times, and we found significant two-way synergistic interactions between disturbances. The best performing model (dominant, additive, or interactive) depended on the temporal scale of response. In the short term (i.e. for resistance), the dominance model predicted resistance of dissolved oxygen best, due to a large effect of carbon enrichment, whereas none of the models could predict the medium term (i.e. resilience). The long-term response was best predicted by models including interactions among disturbances. Our results indicate the importance of accounting for the temporal scale of responses when researching the effects of environmental disturbances on ecosystems.

Loss of predator species, not intermediate consumers, triggers rapid and dramatic extinction cascades.

Ecological networks are tightly interconnected, such that loss of a single species can trigger additional species extinctions. Theory predicts that such secondary extinctions are driven primarily by loss of species from intermediate or basal trophic levels. In contrast, most cases of secondary extinctions from natural systems have been attributed to loss of entire top trophic levels. Here, we show that loss of single predator species in isolation can, irrespective of their identity or the presence of other predators, trigger rapid secondary extinction cascades in natural communities far exceeding those generally predicted by theory. In contrast, we did not find any secondary extinctions caused by intermediate consumer loss. A food web model of our experimental system-a marine rocky shore community-could reproduce these results only when biologically likely and plausible nontrophic interactions, based on competition for space and predator-avoidance behaviour, were included. These findings call for a reassessment of the scale and nature of extinction cascades, particularly the inclusion of nontrophic interactions, in forecasts of the future of biodiversity.

Navigating the complexity of ecological stability.

Human actions challenge nature in many ways. Ecological responses are ineluctably complex, demanding measures that describe them succinctly. Collectively, these measures encapsulate the overall 'stability' of the system. Many international bodies, including the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, broadly aspire to maintain or enhance ecological stability. Such bodies frequently use terms pertaining to stability that lack clear definition. Consequently, we cannot measure them and so they disconnect from a large body of theoretical and empirical understanding. We assess the scientific and policy literature and show that this disconnect is one consequence of an inconsistent and one-dimensional approach that ecologists have taken to both disturbances and stability. This has led to confused communication of the nature of stability and the level of our insight into it. Disturbances and stability are multidimensional. Our understanding of them is not. We have a remarkably poor understanding of the impacts on stability of the characteristics that define many, perhaps all, of the most important elements of global change. We provide recommendations for theoreticians, empiricists and policymakers on how to better integrate the multidimensional nature of ecological stability into their research, policies and actions.

Community trait overdispersion due to trophic interactions: concerns for assembly process inference.

The expected link between competitive exclusion and community trait overdispersion has been used to infer competition in local communities, and trait clustering has been interpreted as habitat filtering. Such community assembly process inference has received criticism for ignoring trophic interactions, as competition and trophic interactions might create similar trait patterns. While other theoretical studies have generally demonstrated the importance of predation for coexistence, ours provides the first quantitative demonstration of such effects on assembly process inference, using a trait-based ecological model to simulate the assembly of a competitive primary consumer community with and without the influence of trophic interactions. We quantified and contrasted trait dispersion/clustering of the competitive communities with the absence and presence of secondary consumers. Trophic interactions most often decreased trait clustering (i.e. increased dispersion) in the competitive communities due to evenly distributed invasions of secondary consumers and subsequent competitor extinctions over trait space. Furthermore, effects of trophic interactions were somewhat dependent on model parameters and clustering metric. These effects create considerable problems for process inference from trait distributions; one potential solution is to use more process-based and inclusive models in inference.

Evolutionary rescue can be impeded by temporary environmental amelioration.

Rapid evolutionary adaptation has the potential to rescue from extinction populations experiencing environmental changes. Little is known, however, about the impact of short-term environmental fluctuations during long-term environmental deterioration, an intrinsic property of realistic environmental changes. Temporary environmental amelioration arising from such fluctuations could either facilitate evolutionary rescue by allowing population recovery (a positive demographic effect) or impede it by relaxing selection for beneficial mutations required for future survival (a negative population genetic effect). We address this uncertainty in an experiment with populations of a bacteriophage virus that evolved under deteriorating conditions (gradually increasing temperature). Periodic environmental amelioration (short periods of reduced temperature) caused demographic recovery during the early phase of the experiment, but ultimately reduced the frequency of evolutionary rescue. These experimental results suggest that environmental fluctuations could reduce the potential of evolutionary rescue.

The ecological forecast horizon, and examples of its uses and determinants.

Forecasts of ecological dynamics in changing environments are increasingly important, and are available for a plethora of variables, such as species abundance and distribution, community structure and ecosystem processes. There is, however, a general absence of knowledge about how far into the future, or other dimensions (space, temperature, phylogenetic distance), useful ecological forecasts can be made, and about how features of ecological systems relate to these distances. The ecological forecast horizon is the dimensional distance for which useful forecasts can be made. Five case studies illustrate the influence of various sources of uncertainty (e.g. parameter uncertainty, environmental variation, demographic stochasticity and evolution), level of ecological organisation (e.g. population or community), and organismal properties (e.g. body size or number of trophic links) on temporal, spatial and phylogenetic forecast horizons. Insights from these case studies demonstrate that the ecological forecast horizon is a flexible and powerful tool for researching and communicating ecological predictability. It also has potential for motivating and guiding agenda setting for ecological forecasting research and development.

Are All Hosts Created Equal? Partitioning Host Species Contributions to Parasite Persistence in Multihost Communities.

Many parasites circulate endemically within communities of multiple host species. To understand disease persistence within these communities, it is essential to know the contribution each host species makes to parasite transmission and maintenance. However, quantifying those contributions is challenging. We present a conceptual framework for classifying multihost sharing, based on key thresholds for parasite persistence. We then develop a generalized technique to quantify each species' contribution to parasite persistence, allowing natural systems to be located within the framework. We illustrate this approach using data on gastrointestinal parasites circulating within rodent communities and show that, although many parasites infect several host species, parasite persistence is often driven by just one host species. In some cases, however, parasites require multiple host species for maintenance. Our approach provides a quantitative method for differentiating these cases using minimal reliance on system-specific parameters, enabling informed decisions about parasite management within poorly understood multihost communities.