A function-based typology for Earth's ecosystems.

As the United Nations develops a post-2020 global biodiversity framework for the Convention on Biological Diversity, attention is focusing on how new goals and targets for ecosystem conservation might serve its vision of 'living in harmony with nature'1,2. Advancing dual imperatives to conserve biodiversity and sustain ecosystem services requires reliable and resilient generalizations and predictions about ecosystem responses to environmental change and management3. Ecosystems vary in their biota4, service provision5 and relative exposure to risks6, yet there is no globally consistent classification of ecosystems that reflects functional responses to change and management. This hampers progress on developing conservation targets and sustainability goals. Here we present the International Union for Conservation of Nature (IUCN) Global Ecosystem Typology, a conceptually robust, scalable, spatially explicit approach for generalizations and predictions about functions, biota, risks and management remedies across the entire biosphere. The outcome of a major cross-disciplinary collaboration, this novel framework places all of Earth's ecosystems into a unifying theoretical context to guide the transformation of ecosystem policy and management from global to local scales. This new information infrastructure will support knowledge transfer for ecosystem-specific management and restoration, globally standardized ecosystem risk assessments, natural capital accounting and progress on the post-2020 global biodiversity framework.

Divergent ecological responses to typhoon disturbance revealed via landscape-scale acoustic monitoring.

Climate change is increasing the frequency, intensity, and duration of extreme weather events across the globe. Understanding the capacity for ecological communities to withstand and recover from such events is critical. Typhoons are extreme weather events that are expected to broadly homogenize ecological dynamics through structural damage to vegetation and longer-term effects of salinization. Given their unpredictable nature, monitoring ecological responses to typhoons is challenging, particularly for mobile animals such as birds. Here, we report spatially variable ecological responses to typhoons across terrestrial landscapes. Using a high temporal resolution passive acoustic monitoring network across 24 sites on the subtropical island of Okinawa, Japan, we found that typhoons elicit divergent ecological responses among Okinawa's diverse terrestrial habitats, as indicated by increased spatial variability of biological sound production (biophony) and individual species detections. This suggests that soniferous communities are capable of a diversity of different responses to typhoons. That is, spatial insurance effects among local ecological communities provide resilience to typhoons at the landscape scale. Even though site-level typhoon impacts on soundscapes and bird detections were not particularly strong, monitoring at scale with high temporal resolution across a broad spatial extent nevertheless enabled detection of spatial heterogeneity in typhoon responses. Further, species-level responses mirrored those of acoustic indices, underscoring the utility of such indices for revealing insight into fundamental questions concerning disturbance and stability. Our findings demonstrate the significant potential of landscape-scale acoustic sensor networks to capture the understudied ecological impacts of unpredictable extreme weather events.

Breakdown in seasonal dynamics of subtropical ant communities with land-cover change.

Concerns about widespread human-induced declines in insect populations are mounting, yet little is known about how land-use change modifies both the trends and variability of insect communities, particularly in understudied regions. Here, we examine how the seasonal activity patterns of ants-key drivers of terrestrial ecosystem functioning-vary with anthropogenic land-cover change on a subtropical island landscape, and whether differences in temperature or species composition can explain observed patterns. Using trap captures sampled biweekly over 2 years from a biodiversity monitoring network covering Okinawa Island, Japan, we processed 1.2 million individuals and reconstructed activity patterns within and across habitat types. Forest communities exhibited greater temporal variability of activity than those in more developed areas. Using time-series decomposition to deconstruct this pattern, we found that sites with greater human development exhibited ant communities with diminished seasonality, reduced synchrony and higher stochasticity compared with sites with greater forest cover. Our results cannot be explained by variation in regional or site temperature patterns, or by differences in species richness or composition among sites. Our study raises the possibility that disruptions to natural seasonal patterns of functionally key insect communities may comprise an important and underappreciated consequence of global environmental change that must be better understood across Earth's biomes.

Linking changes in species composition and biomass in a globally distributed grassland experiment.

Global change drivers, such as anthropogenic nutrient inputs, are increasing globally. Nutrient deposition simultaneously alters plant biodiversity, species composition and ecosystem processes like aboveground biomass production. These changes are underpinned by species extinction, colonisation and shifting relative abundance. Here, we use the Price equation to quantify and link the contributions of species that are lost, gained or that persist to change in aboveground biomass in 59 experimental grassland sites. Under ambient (control) conditions, compositional and biomass turnover was high, and losses (i.e. local extinctions) were balanced by gains (i.e. colonisation). Under fertilisation, the decline in species richness resulted from increased species loss and decreases in species gained. Biomass increase under fertilisation resulted mostly from species that persist and to a lesser extent from species gained. Drivers of ecological change can interact relatively independently with diversity, composition and ecosystem processes and functions such as aboveground biomass due to the individual contributions of species lost, gained or persisting.

Predators mitigate the destabilising effects of heatwaves on multitrophic stream communities.

Amidst the global extinction crisis, climate change will expose ecosystems to more frequent and intense extreme climatic events, such as heatwaves. Yet, whether predator species loss-a prevailing characteristic of the extinction crisis-will exacerbate the ecological consequences of extreme climatic events remains largely unknown. Here, we show that the loss of predator species can interact with heatwaves to moderate the compositional stability of ecosystems. We exposed multitrophic stream communities, with and without a dominant predator species, to realistic current and future heatwaves and found that heatwaves destabilised algal communities by homogenising them in space. However, this happened only when the predator was absent. Additional heatwave impacts on multiple aspects of stream communities, including changes to the structure of algal and macroinvertebrate communities, as well as total algal biomass and its temporal variability, were not apparent during heatwaves and emerged only after the heatwaves had passed. Taken together, our results suggest that the ecological consequences of heatwaves can amplify over time as their impacts propagate through biological interaction networks, but the presence of predators can help to buffer such impacts. These findings underscore the importance of conserving trophic structure, and highlight the potential for species extinctions to amplify the effects of climate change and extreme events.

Nutrients and herbivores impact grassland stability across spatial scales through different pathways.

Nutrients and herbivores are well-known drivers of grassland diversity and stability in local communities. However, whether they interact to impact the stability of aboveground biomass and whether these effects depend on spatial scales remain unknown. It is also unclear whether nutrients and herbivores impact stability via different facets of plant diversity including species richness, evenness, and changes in community composition through time and space. We used a replicated experiment adding nutrients and excluding herbivores for 5 years in 34 global grasslands to explore these questions. We found that both nutrient addition and herbivore exclusion alone reduced stability at the larger spatial scale (aggregated local communities; gamma stability), but through different pathways. Nutrient addition reduced gamma stability primarily by increasing changes in local community composition over time, which was mainly driven by species replacement. Herbivore exclusion reduced gamma stability primarily by decreasing asynchronous dynamics among local communities (spatial asynchrony). Their interaction weakly increased gamma stability by increasing spatial asynchrony. Our findings indicate that disentangling the processes operating at different spatial scales may improve conservation and management aiming at maintaining the ability of ecosystems to reliably provide functions and services for humanity.

General statistical scaling laws for stability in ecological systems.

Ecological stability refers to a family of concepts used to describe how systems of interacting species vary through time and respond to disturbances. Because observed ecological stability depends on sampling scales and environmental context, it is notoriously difficult to compare measurements across sites and systems. Here, we apply stochastic dynamical systems theory to derive general statistical scaling relationships across time, space, and ecological level of organisation for three fundamental stability aspects: resilience, resistance, and invariance. These relationships can be calibrated using random or representative samples measured at individual scales, and projected to predict average stability at other scales across a wide range of contexts. Moreover deviations between observed vs. extrapolated scaling relationships can reveal information about unobserved heterogeneity across time, space, or species. We anticipate that these methods will be useful for cross-study synthesis of stability data, extrapolating measurements to unobserved scales, and identifying underlying causes and consequences of heterogeneity.

Soil properties as key predictors of global grassland production: Have we overlooked micronutrients?

Fertilisation experiments have demonstrated that nutrient availability is a key determinant of biomass production and carbon sequestration in grasslands. However, the influence of nutrients in explaining spatial variation in grassland biomass production has rarely been assessed. Using a global dataset comprising 72 sites on six continents, we investigated which of 16 soil factors that shape nutrient availability associate most strongly with variation in grassland aboveground biomass. Climate and N deposition were also considered. Based on theory-driven structural equation modelling, we found that soil micronutrients (particularly Zn and Fe) were important predictors of biomass and, together with soil physicochemical properties and C:N, they explained more unique variation (32%) than climate and N deposition (24%). However, the association between micronutrients and biomass was absent in grasslands limited by NP. These results highlight soil properties as key predictors of global grassland biomass production and point to serial co-limitation by NP and micronutrients.

Fertilized graminoids intensify negative drought effects on grassland productivity.

Droughts can strongly affect grassland productivity and biodiversity, but responses differ widely. Nutrient availability may be a critical factor explaining this variation, but is often ignored in analyses of drought responses. Here, we used a standardized nutrient addition experiment covering 10 European grasslands to test if full-factorial nitrogen, phosphorus, and potassium addition affected plant community responses to inter-annual variation in drought stress and to the extreme summer drought of 2018 in Europe. We found that nutrient addition amplified detrimental drought effects on community aboveground biomass production. Drought effects also differed between functional groups, with a negative effect on graminoid but not forb biomass production. Our results imply that eutrophication in grasslands, which promotes dominance of drought-sensitive graminoids over forbs, amplifies detrimental drought effects. In terms of climate change adaptation, agricultural management would benefit from taking into account differential drought impacts on fertilized versus unfertilized grasslands, which differ in ecosystem services they provide to society.

Warming can alter host behavior in a similar manner to infection with behavior-manipulating parasites.

Parasites are ecologically ubiquitous and, by modifying the physiology and behavior of their host organisms, act as key regulators of the dynamics and stability of ecosystems. It is, however, as yet unclear how parasitic relationships will act to moderate or accelerate the ecological impacts of global climate change. Here, we explore experimentally how the effects of parasites on both the physiology and behavior of their hosts can be moderated by warming, utilising a well-established aquatic host-parasite model system-the ecologically important amphipod Gammarus duebeni and its acanthocephalan parasite Polymorphus minutus. We show that, while only warming affected measured components of host physiology, parasite infection and warming both supressed predator-avoidance behavior of the host independently, yet in a similar manner. Six degrees of warming altered geotactic behaviors to the same extent as infection with behavior-manipulating parasites. These results indicate a novel mechanism by which parasites impact their ecosystems that could be critical to predicting the ecological impacts of warming. Our findings highlight the need for holistic knowledge of interaction networks, incorporating multiple interaction types and behaviors, to predict the effects of both warming and parasitism on the dynamics and stability of ecosystems.

Advancing our understanding of ecological stability.

The concept of ecological stability occupies a prominent place in both fundamental and applied ecological research. We review decades of work on the topic and examine how our understanding has progressed. We show that our understanding of stability has remained fragmented and is limited largely to simple or simplified systems. There has been a profusion of metrics proposed to quantify stability, of which only a handful are used commonly. Furthermore, studies typically quantify one to two metrics of stability at a time and in response to a single perturbation, with some of the main environmental pressures of today being the least studied. We argue that we need to build on the existing consensus and strong theoretical foundation of the stability concept to better understand its multidimensionality and the interdependencies between metrics, levels of organisation and types of perturbations. Only by doing so can we make progress in the quantification of stability in theory and in practice, and eventually build a more comprehensive understanding of how ecosystems will respond to ongoing environmental change.

Infection with behaviour-manipulating parasites enhances bioturbation by key aquatic detritivores.

The ecological ubiquity of parasites and their potential impacts on host behaviour have led to the suggestion that parasites can act as ecosystem engineers, structuring their environment and physical habitats. Potential modification of the relationship between parasites and their hosts by climate change has important implications for how hosts interact with both their biotic and abiotic environment. Here, we show that warming and parasitic infection independently increase rates of bioturbation by a key detritivore in aquatic ecosystems (Gammarus). These findings have important implications for ecosystem structure and functioning in a warming world, as alterations to rates of bioturbation could significantly modify oxygenation penetration and nutrient cycling in benthic sediments of rivers and lakes. Our results demonstrate a need for future ecosystem management strategies to account for parasitic infection when predicting the impacts of a warming climate.

Combined effects of warming and nutrients on marine communities are moderated by predators and vary across functional groups.

Warming, nutrient enrichment and biodiversity modification are among the most pervasive components of human-induced global environmental change. We know little about their cumulative effects on ecosystems; however, even though this knowledge is fundamental to predicting and managing their consequences in a changing world. Here, we show that shifts in predator species composition can moderate both the individual and combined effects of warming and nutrient enrichment in marine systems. However, all three aspects of global change also acted independently to alter different functional groups in our flow-through marine rock-pool mesocosms. Specifically, warming reduced macroalgal biomass and assemblage productivity, whereas enrichment led to increased abundance of meso-invertebrate consumers, and loss of predator species led to increased gastropod grazer biomass. This disparity in responses, both across trophic levels (macroalgae and intermediate consumers), and between detecting additive effects on aggregate measures of ecosystem functioning, yet interactive effects on community composition, illustrates that our forecasting ability depends strongly on the level of ecological complexity incorporated within global change experiments. We conclude that biodiversity change-and loss of predator species in particular-plays a critical and overarching role in determining how ecological communities respond to stressors.

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.

Warming can enhance invasion success through asymmetries in energetic performance.

Both climate warming and biological invasions are prominent drivers of global environmental change and it is important to determine how they interact. However, beyond tolerance and reproductive thresholds, little is known about temperature dependence of invaders' performance, particularly in the light of competitive attributes of functionally similar native species. We used experimentally derived energy budgets and field temperature data to determine whether anticipated warming will asymmetrically affect the energy budgets of the globally invasive Ponto-Caspian mysid crustacean Hemimysis anomala and a functionally similar native competitor (Mysis salemaai) whose range is currently being invaded. In contrast to M. salemaai, which maintains a constant feeding rate with temperature leading to diminishing energy assimilation, we found that H. anomala increases its feeding rate with temperature in parallel with growing metabolic demand. This enabled the invader to maintain high energy assimilation rates, conferring substantially higher scope for growth compared to the native analogue at spring-to-autumn temperatures. Anticipated warming will likely exacerbate this energetic asymmetry and remove the winter overlap, which, given the seasonal limitation of mutually preferred prey, appears to underpin coexistence of the two species. These results indicate that temperature-dependent asymmetries in scope for growth between invaders and native analogues comprise an important mechanism determining invasion success under warming climates. They also highlight the importance of considering relevant spectra of ecological contexts in predicting successful invaders and their impacts under warming scenarios.

Dietary niche constriction when invaders meet natives: evidence from freshwater decapods.

Invasive species are a key driver of global environmental change, with frequently strong negative consequences for native biodiversity and ecosystem processes. Understanding competitive interactions between invaders and functionally similar native species provides an important benchmark for predicting the consequences of invasion. However, even though having a broad dietary niche is widely considered a key factor determining invasion success, little is known about the effects of competition with functionally similar native competitors on the dietary niche breadths of invasive species. We used a combination of field experiments and field surveys to examine the impacts of competition with a functionally similar native crab species on the population densities, growth rates and diet of the globally widespread invasive red swamp crayfish in an African river ecosystem. The presence of native crabs triggered significant dietary niche constriction within the invasive crayfish population. Further, growth rates of both species were reduced significantly, and by a similar extent, in the presence of one another. In spite of this, crayfish maintained positive growth rates in the presence of crabs, whereas crabs lost mass in the presence of crayfish. Consequently, over the 3-year duration of the study, crab abundance declined at those sites invaded by the crayfish, becoming locally extinct at one. The invasive crayfish had a dramatic effect on ecosystem structure and functioning, halving benthic invertebrate densities and increasing decomposition rates fourfold compared to the crabs. This indicates that replacement of native crabs by invasive crayfish likely alters the structure and functioning of African river ecosystems significantly. This study provides a novel example of the constriction of the dietary niche of a successful invasive population in the presence of competition from a functionally similar native species. This finding highlights the importance of considering both environmental and ecological contexts in order to predict and manage the impacts of invasive species on ecosystems.

Ecosystem-level effects of a globally spreading invertebrate invader are not moderated by a functionally similar native.

Biological invasions are a key element of human-induced global environmental change. However, lack of knowledge of the indirect consequences of invasions, combined with poor understanding of how their ecological effects depend upon competitive attributes of the receiving community, hinders our ability to manage and predict the effects of invasive species on ecosystems. We established an experiment using a combination of both additive and substitutive experimental designs to explore the effects of the globally spreading mysid shrimp Hemimysis anomala on the biological structure of outdoor pond mesocosms in the absence and presence of a functionally similar native competitor, Mysis salemaai. The naturally smaller H. anomala had considerably stronger effects on primary producers, multiple aspects of consumer assemblages and overall biological structure of the ponds in comparison with the functionally similar native. Moreover, the magnitude of these effects was generally independent of the presence of M. salemaai and even total mysid density. Hemimysis anomala reduced both the abundance and diversity of zooplankton assemblages significantly, triggering a strong trophic cascade on phytoplankton and a simultaneous increase of benthic invertebrate biomass. These findings indicate that invasion by H. anomala may exacerbate the effects of nutrient enrichment on lakes. Our results demonstrate that introduced species can, irrespective of the presence of functionally similar natives, induce complex changes to ecosystems that reach beyond direct consumptive effects. Moreover, the cascading indirect effects of invasion can exacerbate the impacts of other stressors. Disregarding the complexity of indirect effects therefore risks underestimating significantly the global ecological footprint of biological invasions.

Ecology and mode-of-life explain lifespan variation in birds and mammals.

Maximum lifespan in birds and mammals varies strongly with body mass such that large species tend to live longer than smaller species. However, many species live far longer than expected given their body mass. This may reflect interspecific variation in extrinsic mortality, as life-history theory predicts investment in long-term survival is under positive selection when extrinsic mortality is reduced. Here, we investigate how multiple ecological and mode-of-life traits that should reduce extrinsic mortality (including volancy (flight capability), activity period, foraging environment and fossoriality), simultaneously influence lifespan across endotherms. Using novel phylogenetic comparative analyses and to our knowledge, the most species analysed to date (n = 1368), we show that, over and above the effect of body mass, the most important factor enabling longer lifespan is the ability to fly. Within volant species, lifespan depended upon when (day, night, dusk or dawn), but not where (in the air, in trees or on the ground), species are active. However, the opposite was true for non-volant species, where lifespan correlated positively with both arboreality and fossoriality. Our results highlight that when studying the molecular basis behind cellular processes such as those underlying lifespan, it is important to consider the ecological selection pressures that shaped them over evolutionary time.

How strongly does diet variation explain variation in isotope values of animal consumers?

Analysis of stable isotopes in consumers is used commonly to study their ecological and/or environmental niche. There is, however, considerable debate regarding how isotopic values relate to diet and how other sources of variation confound this link, which can undermine the utility. From the analysis of a simple, but general, model of isotopic incorporation in consumer organisms, we examine the relationship between isotopic variance among individuals, and diet variability within a consumer population. We show that variance in consumer isotope values is directly proportional to variation in diet (through Simpson indices), to the number of isotopically distinct food sources in the diet, and to the baseline variation within and among the isotope values of the food sources. Additionally, when considering temporal diet variation within a consumer we identify the interplay between diet turnover rates and tissue turnover rates that controls the sensitivity of stable isotopes to detect diet variation. Our work demonstrates that variation in the stable isotope values of consumers reflect variation in their diet. This relationship, however, can be confounded with other factors to the extent that they may mask the signal coming from diet. We show how simple quantitative corrections can recover a direct 1:1 correlation in some situations, and in others we can adjust our interpretation in light of the new understanding arising from our models. Our framework provides guidance for the design and analysis of empirical studies where the goal is to infer niche width from stable isotope data.