How collectively integrated are ecological communities?

Beyond abiotic conditions, do population dynamics mostly depend on a species' direct predators, preys and conspecifics? Or can indirect feedback that ripples across the whole community be equally important? Determining where ecological communities sit on the spectrum between these two characterizations requires a metric able to capture the difference between them. Here we show that the spectral radius of a community's interaction matrix provides such a metric, thus a measure of ecological collectivity, which is accessible from imperfect knowledge of biotic interactions and related to observable signatures. This measure of collectivity integrates existing approaches to complexity, interaction structure and indirect interactions. Our work thus provides an original perspective on the question of to what degree communities are more than loose collections of species or simple interaction motifs and explains when pragmatic reductionist approaches ought to suffice or fail when applied to ecological communities.

Decoupled responses of above- and below-ground beta-diversity to nitrogen enrichment in a typical steppe.

Increased atmospheric nitrogen (N) deposition affects biodiversity in terrestrial ecosystems. However, we do not know whether the effects of N on above-ground plant ß-diversity are coupled with changes occurring in the soil seed bank. We conducted a long-term N-addition experiment in a typical steppe and found that above-ground ß-diversity increased and then decreased with increasing N addition, whereas below-ground ß-diversity decreased linearly. This suggests decoupled dynamics of plant communities and their soil seed bank under N enrichment. Species substitution determined above- and below-ground ß-diversity change via an increasing role of deterministic processes with N addition. These effects were mostly driven by differential responses of the above-ground vegetation and the soil seed bank ß-diversities to N-induced changes in environmental heterogeneity, increased soil inorganic N concentrations and soil acidification. Our findings highlight the importance of considering above- and below-ground processes simultaneously for effectively conserving grassland ecosystems under N enrichment.

Metapopulation capacity determines food chain length in fragmented landscapes.

Metapopulation capacity provides an analytic tool to quantify the impact of landscape configuration on metapopulation persistence, which has proven powerful in biological conservation. Yet surprisingly few efforts have been made to apply this approach to multispecies systems. Here, we extend metapopulation capacity theory to predict the persistence of trophically interacting species. Our results demonstrate that metapopulation capacity could be used to predict the persistence of trophic systems such as prey-predator pairs and food chains in fragmented landscapes. In particular, we derive explicit predictions for food chain length as a function of metapopulation capacity, top-down control, and population dynamical parameters. Under certain assumptions, we show that the fraction of empty patches for the basal species provides a useful indicator to predict the length of food chains that a fragmented landscape can support and confirm this prediction for a host-parasitoid interaction. We further show that the impact of habitat changes on biodiversity can be predicted from changes in metapopulation capacity or approximately by changes in the fraction of empty patches. Our study provides an important step toward a spatially explicit theory of trophic metacommunities and a useful tool for predicting their responses to habitat changes.

Partitioning the biodiversity effects on productivity into density and size components.

Plant density and size - two factors that represent plant survival and growth - are key determinants of yield but have rarely been analysed explicitly in the context of biodiversity-productivity relationships. Here, we derive equations to partition the net, complementarity and selection effects of biodiversity into additive components that reflect diversity-induced changes in plant density and size. Applications of the new method to empirical datasets reveal contrasting ways in which plant density and size regulate yield in species mixtures. In an annual plant diversity experiment, overyielding is largely explained by selection effects associated with increased size of highly productive plant species. In a tree diversity experiment, the cause of overyielding shifts from enhanced growth in tree size to reduced mortality by complementary use of canopy space during stand development. These results highlight the capability of the new method to resolve crucial, yet understudied, demographic links between biodiversity and productivity.

Spatial heterogeneity of biomass turnover has contrasting effects on synchrony and stability in trophic metacommunities.

Spatial heterogeneity is a fundamental feature of ecosystems, and ecologists have identified it as a factor promoting the stability of population dynamics. In particular, differences in interaction strengths and resource supply between patches generate an asymmetry of biomass turnover with a fast and a slow patch coupled by a mobile predator. Here, we demonstrate that asymmetry leads to opposite stability patterns in metacommunities receiving localized perturbations depending on the characteristics of the perturbed patch. Perturbing prey in the fast patch synchronizes the dynamics of prey biomass between the two patches and destabilizes predator dynamics by increasing the predator's temporal variability. Conversely, perturbing prey in the slow patch decreases the synchrony of the prey's dynamics and stabilizes predator dynamics. Our results have implications for conservation ecology and suggest reinforcing protection policies in fast patches to dampen the effects of perturbations and promote the stability of population dynamics at the regional scale.

Opportunities to advance the synthesis of ecology and evolution.

Despite decades of research on the interactions between ecology and evolution, opportunities still remain to further integrate the two disciplines, especially when considering multispecies systems. Here, we discuss two such opportunities. First, the traditional emphasis on the distinction between evolutionary and ecological processes should be further relaxed as it is particularly unhelpful in the study of microbial communities, where the very notion of species is hard to define. Second, key processes of evolutionary theory such as adaptation should be exported to hierarchical levels higher than populations to make sense of biodiversity dynamics. Together, we argue that broadening our perspective of eco-evolutionary dynamics to be more inclusive of all biodiversity, both phylogenetically and hierarchically, will open up fertile new research directions and help us to address one of the major scientific challenges of our time, that is, to understand and predict changes in biodiversity in the face of rapid environmental change.

Will a large complex system be productive?

While the relationship between food web complexity and stability has been well documented, how complexity affects productivity remains elusive. In this study, we combine food web theory and a data set of 149 aquatic food webs to investigate the effect of complexity (i.e. species richness, connectance, and average interaction strength) on ecosystem productivity. We find that more complex ecosystems tend to be more productive, although different facets of complexity have contrasting effects. A higher species richness and/or average interaction strength increases productivity, whereas a higher connectance often decreases it. These patterns hold not only between realized complexity and productivity, but also characterize responses of productivity to simulated declines of complexity. Our model also predicts a negative association between productivity and stability along gradients of complexity. Empirical analyses support our predictions on positive complexity-productivity relationships and negative productivity-stability relationships. Our study provides a step forward towards reconciling ecosystem complexity, productivity and stability.

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.

Habitat percolation transition undermines sustainability in social-ecological agricultural systems.

Steady increases in human population size and resource consumption are driving rampant agricultural expansion and intensification. Habitat loss caused by agriculture puts the integrity of ecosystems at risk and threatens the persistence of human societies that rely on ecosystem services. We develop a spatially explicit model describing the coupled dynamics of an agricultural landscape and human population size to assess the effect of different land-use management strategies, defined by agricultural clustering and intensification, on the sustainability of the social-ecological system. We show how agricultural expansion can cause natural habitats to undergo a percolation transition leading to abrupt habitat fragmentation that feedbacks on human's decision making, aggravating landscape degradation. We found that agricultural intensification to spare land from conversion is a successful strategy only in highly natural landscapes, and that clustering agricultural land is the most effective measure to preserve large connected natural fragments, prevent severe fragmentation and thus, enhance sustainability.

The hidden role of multi-trophic interactions in driving diversity-productivity relationships.

Resource-use complementarity of producer species is often invoked to explain the generally positive diversity-productivity relationships. Additionally, multi-trophic interactions that link processes across trophic levels have received increasing attention as a possible key driver. Given that both are integral to natural ecosystems, their interactive effect should be evident but has remained hidden. We address this issue by analysing diversity-productivity relationships in a simulation experiment of producer communities nested within complex food-webs, manipulating resource-use complementarity and multi-trophic animal richness. We show that these two mechanisms interactively create diverse communities of complementary producer species. This shapes diversity-productivity relationships such that their joint contribution generally exceeds their individual effects. Specifically, multi-trophic interactions in animal-rich ecosystems facilitate producer coexistence by preventing competitive exclusion despite overlaps in resource-use, which increases the realised complementarity. The interdependence of food-webs and producer complementarity in creating biodiversity-productivity relationships highlights the importance to adopt a multi-trophic perspective on biodiversity-ecosystem functioning relationships.

Linking scaling laws across eukaryotes.

Scaling laws relating body mass to species characteristics are among the most universal quantitative patterns in biology. Within major taxonomic groups, the 4 key ecological variables of metabolism, abundance, growth, and mortality are often well described by power laws with exponents near 3/4 or related to that value, a commonality often attributed to biophysical constraints on metabolism. However, metabolic scaling theories remain widely debated, and the links among the 4 variables have never been formally tested across the full domain of eukaryote life, to which prevailing theory applies. Here we present datasets of unprecedented scope to examine these 4 scaling laws across all eukaryotes and link them to test whether their combinations support theoretical expectations. We find that metabolism and abundance scale with body size in a remarkably reciprocal fashion, with exponents near ±3/4 within groups, as expected from metabolic theory, but with exponents near ±1 across all groups. This reciprocal scaling supports "energetic equivalence" across eukaryotes, which hypothesizes that the partitioning of energy in space across species does not vary significantly with body size. In contrast, growth and mortality rates scale similarly both within and across groups, with exponents of ±1/4. These findings are inconsistent with a metabolic basis for growth and mortality scaling across eukaryotes. We propose that rather than limiting growth, metabolism adjusts to the needs of growth within major groups, and that growth dynamics may offer a viable theoretical basis to biological scaling.

Consistently positive effect of species diversity on ecosystem, but not population, temporal stability.

Despite much recent progress, our understanding of diversity-stability relationships across different study systems remains incomplete. In particular, recent theory clarified that within-species population stability and among-species asynchronous population dynamics combine to determine ecosystem temporal stability, but their relative importance in modulating diversity-ecosystem temporal stability relationships in different ecosystems remains unclear. We addressed this issue with a meta-analysis of empirical studies of ecosystem and population temporal stability in relation to species diversity across a range of taxa and ecosystems. We show that ecosystem temporal stability tended to increase with species diversity, regardless of study systems. Increasing diversity promoted asynchrony, which, in turn, contributed to increased ecosystem stability. The positive diversity-ecosystem stability relationship persisted even after accounting for the influences of environmental covariates (e.g., precipitation and nutrient input). By contrast, species diversity tended to reduce population temporal stability in terrestrial systems but increase population temporal stability in aquatic systems, suggesting that asynchronous dynamics among species are essential for stabilizing diverse terrestrial ecosystems. We conclude that there is compelling empirical evidence for a general positive relationship between species diversity and ecosystem-level temporal stability, but the contrasting diversity-population temporal stability relationships between terrestrial and aquatic systems call for more investigations into their underlying mechanisms.

Can biomass distribution across trophic levels predict trophic cascades?

The biomass distribution across trophic levels (biomass pyramid) and cascading responses to perturbations (trophic cascades) are archetypal representatives of the interconnected set of static and dynamical properties of food chains. A vast literature has explored their respective ecological drivers, sometimes generating correlations between them. Here we instead reveal a fundamental connection: both pyramids and cascades reflect the dynamical sensitivity of the food chain to changes in species intrinsic rates. We deduce a direct relationship between cascades and pyramids, modulated by what we call trophic dissipation - a synthetic concept that encodes the contribution of top-down propagation of consumer losses in the biomass pyramid. Predictable across-ecosystem patterns emerge when systems are in similar regimes of trophic dissipation. Data from 31 aquatic mesocosm experiments demonstrate how our approach can reveal the causal mechanisms linking trophic cascades and biomass distributions, thus providing a road map to deduce reliable predictions from empirical patterns.

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.

Synchrony and Perturbation Transmission in Trophic Metacommunities.

AbstractIn a world where natural habitats are ever more fragmented, the dynamics of metacommunities are essential to properly understand species responses to perturbations. If species' populations fluctuate asynchronously, the risk of their simultaneous extinction is low, thus reducing the species' regional extinction risk. However, identifying synchronizing or desynchronizing mechanisms in systems containing several species and when perturbations affect multiple species is challenging. We propose a metacommunity model consisting of two food chains connected by dispersal to study the transmission of small perturbations affecting populations in the vicinity of an equilibrium. In spite of the complex responses produced by such a system, two elements enable us to understand the key processes that rule the synchrony between populations: (1) knowing which species have the strongest response to perturbations and (2) the relative importance of dispersal processes compared with local dynamics for each species. We show that perturbing a species in one patch can lead to asynchrony between patches if the perturbed species is not the most affected by dispersal. The synchrony patterns of rare species are the most sensitive to the relative strength of dispersal to demographic processes, thus making biomass distribution critical to understanding the response of trophic metacommunities to perturbations. We further partition the effect of each perturbation on species synchrony when perturbations affect multiple trophic levels. Our approach allows disentangling and predicting the responses of simple trophic metacommunities to perturbations, thus providing a theoretical foundation for future studies considering more complex spatial ecological systems.

Scaling up biodiversity-ecosystem functioning relationships: the role of environmental heterogeneity in space and time.

The biodiversity and ecosystem functioning (BEF) relationship is expected to be scale-dependent. The autocorrelation of environmental heterogeneity is hypothesized to explain this scale dependence because it influences how quickly biodiversity accumulates over space or time. However, this link has yet to be demonstrated in a formal model. Here, we use a Lotka-Volterra competition model to simulate community dynamics when environmental conditions vary across either space or time. Species differ in their optimal environmental conditions, which results in turnover in community composition. We vary biodiversity by modelling communities with different sized regional species pools and ask how the amount of biomass per unit area depends on the number of species present, and the spatial or temporal scale at which it is measured. We find that more biodiversity is required to maintain functioning at larger temporal and spatial scales. The number of species required increases quickly when environmental autocorrelation is low, and slowly when autocorrelation is high. Both spatial and temporal environmental heterogeneity lead to scale dependence in BEF, but autocorrelation has larger impacts when environmental change is temporal. These findings show how the biodiversity required to maintain functioning is expected to increase over space and time.

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.

Thermal mismatches in biological rates determine trophic control and biomass distribution under warming.

Temperature has numerous effects on the structure and dynamics of ecological communities. Yet, there is no general trend or consensus on the magnitude and directions of these effects. To fill this gap, we propose a mechanistic framework based on key biological rates that predicts how temperature influences biomass distribution and trophic control in food webs. We show that these predictions arise from thermal mismatches between biological rates and across trophic levels. We couple our theory with experimental data for a wide range of species and find that warming should lead to top-heavier terrestrial food chains and stronger top-down control in aquatic environments. We then derive predictions for the effects of temperature on herbivory and validate them with data on stream grazers. Our study provides a mechanistic explanation of thermal effects on consumer-resource systems which is crucial to better understand the biogeography and the consequences of global warming on trophic dynamics.

Divergent above- and below-ground biodiversity pathways mediate disturbance impacts on temperate forest multifunctionality.

Biodiversity plays a fundamental role in provisioning and regulating forest ecosystem functions and services. Above-ground (plants) and below-ground (soil microbes) biodiversity could have asynchronous change paces to human-driven land-use impacts. Yet, we know very little how they affect the provision of multiple forest functions related to carbon accumulation, water retention capacity and nutrient cycling simultaneously (i.e. ecosystem multifunctionality; EMF). We used a dataset of 22,000 temperate forest trees from 260 plots within 11 permanent forest sites in Northeastern China, which are recovering from three post-logging disturbances. We assessed the direct and mediating effects of multiple attributes of plant biodiversity (taxonomic, phylogenetic, functional and stand structure) and soil biodiversity (bacteria and fungi) on EMF under the three disturbance levels. We found the highest EMF in highly disturbed rather than undisturbed mature forests. Plant taxonomic, phylogenetic, functional and stand structural diversity had both positive and negative effects on EMF, depending on how the EMF index was quantified, whereas soil microbial diversity exhibited a consistent positive impact. Biodiversity indices explained on average 45% (26%-58%) of the variation in EMF, whereas climate and disturbance together explained on average 7% (0.4%-15%). Our result highlighted that the tremendous effect of biodiversity on EMF, largely overpassing those of both climate and disturbance. While above- (ß = 0.02-0.19) and below-ground (ß = 0.16-0.26) biodiversity had direct positive effects on EMF, their opposite mediating effects (ß = -0.22 vs. ß = 0.35 respectively) played as divergent pathways to human disturbance impacts on EMF. Our study sheds light on the need for integrative frameworks simultaneously considering above- and below-ground attributes to grasp the global picture of biodiversity effects on ecosystem functioning and services. Suitable management interventions could maintain both plant and soil microbial biodiversity, and thus guarantee a long-term functioning and provisioning of ecosystem services in an increasing disturbance frequency world.