Bioenergetic mapping of 'healthy microbiomes' via compound processing potential imprinted in gut and soil metagenomes.

Despite mounting evidence of their importance in human health and ecosystem functioning, the definition and measurement of 'healthy microbiomes' remain unclear. More advanced knowledge exists on health associations for compounds used or produced by microbes. Environmental microbiome exposures (especially via soils) also help shape, and may supplement, the functional capacity of human microbiomes. Given the synchronous interaction between microbes, their feedstocks, and micro-environments, with functional genes facilitating chemical transformations, our objective was to examine microbiomes in terms of their capacity to process compounds relevant to human health. Here we integrate functional genomics and biochemistry frameworks to derive new quantitative measures of in silico potential for human gut and environmental soil metagenomes to process a panel of major compound classes (e.g., lipids, carbohydrates) and selected biomolecules (e.g., vitamins, short-chain fatty acids) linked to human health. Metagenome functional potential profile data were translated into a universal compound mapping 'landscape' based on bioenergetic van Krevelen mapping of function-level meta-compounds and corresponding functional relative abundances, reflecting imprinted genetic capacity of microbiomes to metabolize an array of different compounds. We show that measures of 'compound processing potential' associated with human health and disease (examining atherosclerotic cardiovascular disease, colorectal cancer, type 2 diabetes and anxious-depressive behavior case studies), and displayed seemingly predictable shifts along gradients of ecological disturbance in plant-soil ecosystems (three case studies). Ecosystem quality explained 60-92 % of variation in soil metagenome compound processing potential measures in a post-mining restoration case study dataset. With growing knowledge of the varying proficiency of environmental microbiota to process human health associated compounds, we might design environmental interventions or nature prescriptions to modulate our exposures, thereby advancing microbiota-oriented approaches to human health. Compound processing potential offers a simplified, integrative approach for applying metagenomics in ongoing efforts to understand and quantify the role of microbiota in environmental- and human-health.

Global fine-resolution data on springtail abundance and community structure.

Springtails (Collembola) inhabit soils from the Arctic to the Antarctic and comprise an estimated ~32% of all terrestrial arthropods on Earth. Here, we present a global, spatially-explicit database on springtail communities that includes 249,912 occurrences from 44,999 samples and 2,990 sites. These data are mainly raw sample-level records at the species level collected predominantly from private archives of the authors that were quality-controlled and taxonomically-standardised. Despite covering all continents, most of the sample-level data come from the European continent (82.5% of all samples) and represent four habitats: woodlands (57.4%), grasslands (14.0%), agrosystems (13.7%) and scrublands (9.0%). We included sampling by soil layers, and across seasons and years, representing temporal and spatial within-site variation in springtail communities. We also provided data use and sharing guidelines and R code to facilitate the use of the database by other researchers. This data paper describes a static version of the database at the publication date, but the database will be further expanded to include underrepresented regions and linked with trait data.

Consistent predator-prey biomass scaling in complex food webs.

The ratio of predator-to-prey biomass is a key element of trophic structure that is typically investigated from a food chain perspective, ignoring channels of energy transfer (e.g. omnivory) that may govern community structure. Here, we address this shortcoming by characterising the biomass structure of 141 freshwater, marine and terrestrial food webs, spanning a broad gradient in community biomass. We test whether sub-linear scaling between predator and prey biomass (a potential signal of density-dependent processes) emerges within ecosystem types and across levels of biological organisation. We find a consistent, sub-linear scaling pattern whereby predator biomass scales with the total biomass of their prey with a near ¾-power exponent within food webs - i.e. more prey biomass supports proportionally less predator biomass. Across food webs, a similar sub-linear scaling pattern emerges between total predator biomass and the combined biomass of all prey within a food web. These general patterns in trophic structure are compatible with a systematic form of density dependence that holds among complex feeding interactions across levels of organization, irrespective of ecosystem type.

A network perspective for sustainable agroecosystems.

Nature-based management aims to improve sustainable agroecosystem production, but its efficacy has been variable. We argue that nature-based agroecosystem management could be significantly improved by explicitly considering and manipulating the underlying networks of species interactions. A network perspective can link species interactions to ecosystem functioning and stability, identify influential species and interactions, and suggest optimal management approaches. Recent advances in predicting the network roles of species from their functional traits could allow direct manipulation of network architecture through additions or removals of species with targeted traits. Combined with improved understanding of the structure and dynamics of networks across spatial and temporal scales and interaction types, including social-ecological, applying these tools to nature-based management can contribute to sustainable agroecosystems.

Habitat provision is a major driver of native bird communities in restored urban forests.

Urbanization, and the drastic loss of habitat it entails, poses a major threat to global avian biodiversity. Ecological restoration of urban forests is therefore increasingly vital for native bird conservation, but control of invasive predators may also be needed to sustain native bird populations in cities where species invasions have been particularly severe. We evaluated restoration success by investigating changes in native bird communities along a restoration chronosequence of 25 restored urban forests representing 72 years of forest development, which we compared to two target reference systems and a control system. We hypothesized that total species richness and relative abundance of native forest birds would increase with the age of restoration planting. We further hypothesized that relative abundance of rats, possums and cats would negatively impact native birds, while amount of native forest in the surrounding landscape would have a positive effect. We used structural equation modelling (SEM) to investigate the relative influence of forest structure (complexity index, tree height, canopy openness, basal area, species richness and density), landscape attributes (patch area, perimeter length, landscape composition within three buffer zones, distance to the nearest road and water source) and invasive mammalian predator indices of relative abundance on total species richness and relative abundance of native forest birds. Species richness increased with age of restoration planting, with community composition progressing towards that found in target reference systems. SEM revealed that years restored was a direct driver of bird species richness but an indirect driver of abundance, which was directly driven by canopy openness. Contrary to our predictions, invasive mammals had no significant effect on native bird species richness or abundance. Our results demonstrate that provision and improvement of habitat quantity and quality through restoration is the vital first step to re-establishing native forest bird communities in cities.

For flux's sake: General considerations for energy-flux calculations in ecological communities.

Global change alters ecological communities with consequences for ecosystem processes. Such processes and functions are a central aspect of ecological research and vital to understanding and mitigating the consequences of global change, but also those of other drivers of change in organism communities. In this context, the concept of energy flux through trophic networks integrates food-web theory and biodiversity-ecosystem functioning theory and connects biodiversity to multitrophic ecosystem functioning. As such, the energy-flux approach is a strikingly effective tool to answer central questions in ecology and global-change research. This might seem straight forward, given that the theoretical background and software to efficiently calculate energy flux are readily available. However, the implementation of such calculations is not always straight forward, especially for those who are new to the topic and not familiar with concepts central to this line of research, such as food-web theory or metabolic theory. To facilitate wider use of energy flux in ecological research, we thus provide a guide to adopting energy-flux calculations for people new to the method, struggling with its implementation, or simply looking for background reading, important resources, and standard solutions to the problems everyone faces when starting to quantify energy fluxes for their community data. First, we introduce energy flux and its use in community and ecosystem ecology. Then, we provide a comprehensive explanation of the single steps towards calculating energy flux for community data. Finally, we discuss remaining challenges and exciting research frontiers for future energy-flux research.

Environmental and anthropogenic constraints on animal space use drive extinction risk worldwide.

Animals require a certain amount of habitat to persist and thrive, and habitat loss is one of the most critical drivers of global biodiversity decline. While habitat requirements have been predicted by relationships between species traits and home-range size, little is known about constraints imposed by environmental conditions and human impacts on a global scale. Our meta-analysis of 395 vertebrate species shows that global climate gradients in temperature and precipitation exert indirect effects via primary productivity, generally reducing space requirements. Human pressure, however, reduces realised space use due to ensuing limitations in available habitat, particularly for large carnivores. We show that human pressure drives extinction risk by increasing the mismatch between space requirements and availability. We use large-scale climate gradients to predict current species extinction risk across global regions, which also offers an important tool for predicting future extinction risk due to ongoing space loss and climate change.

Trade-offs between multifunctionality and profit in tropical smallholder landscapes.

Land-use transitions can enhance the livelihoods of smallholder farmers but potential economic-ecological trade-offs remain poorly understood. Here, we present an interdisciplinary study of the environmental, social and economic consequences of land-use transitions in a tropical smallholder landscape on Sumatra, Indonesia. We find widespread biodiversity-profit trade-offs resulting from land-use transitions from forest and agroforestry systems to rubber and oil palm monocultures, for 26,894 aboveground and belowground species and whole-ecosystem multidiversity. Despite variation between ecosystem functions, profit gains come at the expense of ecosystem multifunctionality, indicating far-reaching ecosystem deterioration. We identify landscape compositions that can mitigate trade-offs under optimal land-use allocation but also show that intensive monocultures always lead to higher profits. These findings suggest that, to reduce losses in biodiversity and ecosystem functioning, changes in economic incentive structures through well-designed policies are urgently needed.

Functional losses in ground spider communities due to habitat structure degradation under tropical land-use change.

Deforestation and land-use change in tropical regions result in habitat loss and extinction of species that are unable to adapt to the conditions in agricultural landscapes. If the associated loss of functional diversity is not compensated by species colonizing the converted habitats, extinctions might be followed by a reduction or loss of ecosystem functions including biological control. To date, little is known about how land-use change in the tropics alters the functional diversity of invertebrate predators and which key environmental factors may mitigate the decline in functional diversity and predation in litter and soil communities. We applied litter sieving and heat extraction to study ground spider communities and assessed structural characteristics of vegetation and parameters of litter in rainforest and agricultural land-use systems (jungle rubber, rubber, and oil palm monocultures) in a Southeast Asian hotspot of rainforest conversion: Sumatra, Indonesia. We found that (1) spider density, species richness, functional diversity, and community predation (energy flux to spiders) were reduced by 57-98% from rainforest to oil palm monoculture; (2) jungle rubber and rubber monoculture sustained relatively high diversity and predation in ground spiders, but small cryptic spider species strongly declined; (3) high species turnover compensated losses of some functional trait combinations, but did not compensate for the overall loss of functional diversity and predation per unit area; (4) spider diversity was related to habitat structure such as amount of litter, understory density, and understory height, while spider predation was better explained by plant diversity. Management practices that increase habitat-structural complexity and plant diversity such as mulching, reduced weeding, and intercropping monocultures with other plants may contribute to maintaining functional diversity of and predation services provided by ground invertebrate communities in plantations.

Predator traits determine food-web architecture across ecosystems.

Predator-prey interactions in natural ecosystems generate complex food webs that have a simple universal body-size architecture where predators are systematically larger than their prey. Food-web theory shows that the highest predator-prey body-mass ratios found in natural food webs may be especially important because they create weak interactions with slow dynamics that stabilize communities against perturbations and maintain ecosystem functioning. Identifying these vital interactions in real communities typically requires arduous identification of interactions in complex food webs. Here, we overcome this obstacle by developing predator-trait models to predict average body-mass ratios based on a database comprising 290 food webs from freshwater, marine and terrestrial ecosystems across all continents. We analysed how species traits constrain body-size architecture by changing the slope of the predator-prey body-mass scaling. Across ecosystems, we found high body-mass ratios for predator groups with specific trait combinations including (1) small vertebrates and (2) large swimming or flying predators. Including the metabolic and movement types of predators increased the accuracy of predicting which species are engaged in high body-mass ratio interactions. We demonstrate that species traits explain striking patterns in the body-size architecture of natural food webs that underpin the stability and functioning of ecosystems, paving the way for community-level management of the most complex natural ecosystems.

A niche for ecosystem multifunctionality in global change research.

Concern about human modification of Earth's ecosystems has recently motivated ecologists to address how global change drivers will impact the simultaneous provisioning of multiple functions, termed ecosystem multifunctionality (EMF). However, metrics of EMF have often been applied in global change studies with little consideration of the information they provide beyond single functions, or how and why EMF may respond to global change drivers. Here, we critically review the current state of this rapidly expanding field and provide a conceptual framework to guide the effective incorporation of EMF in global change research. In particular, we emphasize the need for a priori identification and explicit testing of the biotic and abiotic mechanisms through which global change drivers impact EMF, as well as assessing correlations among multiple single functions because these patterns underlie shifts in EMF. While the role of biodiversity in mediating global change effects on EMF has justifiably received much attention, empirical support for effects via other biotic and physicochemical mechanisms are also needed. Studies also frequently stated the importance of measuring EMF responses to global change drivers to understand the potential consequences for multiple ecosystem services, but explicit links between measured functions and ecosystem services were missing from many such studies. While there is clear potential for EMF to provide novel insights to global change research, predictive understanding will be greatly improved by insuring future research is strongly hypothesis-driven, is designed to explicitly test multiple abiotic and biotic mechanisms, and assesses how single functions and their covariation drive emergent EMF responses to global change drivers.

A multitrophic perspective on biodiversity-ecosystem functioning research.

Concern about the functional consequences of unprecedented loss in biodiversity has prompted biodiversity-ecosystem functioning (BEF) research to become one of the most active fields of ecological research in the past 25 years. Hundreds of experiments have manipulated biodiversity as an independent variable and found compelling support that the functioning of ecosystems increases with the diversity of their ecological communities. This research has also identified some of the mechanisms underlying BEF relationships, some context-dependencies of the strength of relationships, as well as implications for various ecosystem services that mankind depends upon. In this paper, we argue that a multitrophic perspective of biotic interactions in random and non-random biodiversity change scenarios is key to advance future BEF research and to address some of its most important remaining challenges. We discuss that the study and the quantification of multitrophic interactions in space and time facilitates scaling up from small-scale biodiversity manipulations and ecosystem function assessments to management-relevant spatial scales across ecosystem boundaries. We specifically consider multitrophic conceptual frameworks to understand and predict the context-dependency of BEF relationships. Moreover, we highlight the importance of the eco-evolutionary underpinnings of multitrophic BEF relationships. We outline that FAIR data (meeting the standards of findability, accessibility, interoperability, and reusability) and reproducible processing will be key to advance this field of research by making it more integrative. Finally, we show how these BEF insights may be implemented for ecosystem management, society, and policy. Given that human well-being critically depends on the multiple services provided by diverse, multitrophic communities, integrating the approaches of evolutionary ecology, community ecology, and ecosystem ecology in future BEF research will be key to refine conservation targets and develop sustainable management strategies.

Energy Flux: The Link between Multitrophic Biodiversity and Ecosystem Functioning.

Relating biodiversity to ecosystem functioning in natural communities has become a paramount challenge as links between trophic complexity and multiple ecosystem functions become increasingly apparent. Yet, there is still no generalised approach to address such complexity in biodiversity-ecosystem functioning (BEF) studies. Energy flux dynamics in ecological networks provide the theoretical underpinning of multitrophic BEF relationships. Accordingly, we propose the quantification of energy fluxes in food webs as a powerful, universal tool for understanding ecosystem functioning in multitrophic systems spanning different ecological scales. Although the concept of energy flux in food webs is not novel, its application to BEF research remains virtually untapped, providing a framework to foster new discoveries into the determinants of ecosystem functioning in complex systems.

Applying generalized allometric regressions to predict live body mass of tropical and temperate arthropods.

The ecological implications of body size extend from the biology of individual organisms to ecosystem-level processes. Measuring body mass for high numbers of invertebrates can be logistically challenging, making length-mass regressions useful for predicting body mass with minimal effort. However, standardized sets of scaling relationships covering a large range in body length, taxonomic groups, and multiple geographical regions are scarce. We collected 6,212 arthropods from 19 higher-level taxa in both temperate and tropical locations to compile a comprehensive set of linear models relating live body mass to a range of predictor variables. We measured live weight (hereafter, body mass), body length and width of each individual and conducted linear regressions to predict body mass using body length, body width, taxonomic group, and geographic region. Additionally, we quantified prediction discrepancy when using parameters from arthropods of a different geographic region. Incorporating body width into taxon- and region-specific length-mass regressions yielded the highest prediction accuracy for body mass. Using regression parameters from a different geographic region increased prediction discrepancy, causing over- or underestimation of body mass depending on geographical origin and whether body width was included. We present a comprehensive range of parameters for predicting arthropod body mass and provide guidance for selecting optimal scaling relationships. Given the importance of body mass for functional invertebrate ecology and the paucity of adequate regressions to predict arthropod body mass from different geographical regions, our study provides a long-needed resource for quantifying live body mass in invertebrate ecology research.

Warming alters the energetic structure and function but not resilience of soil food webs.

Climate warming is predicted to alter the structure, stability, and functioning of food webs1-5. Yet, despite the importance of soil food webs for energy and nutrient turnover in terrestrial ecosystems, warming effects on these food webs-particularly in combination with other global change drivers-are largely unknown. Here, we present results from two complementary field experiments testing the interactive effects of warming with forest canopy disturbance and drought on energy fluxes in boreal-temperate ecotonal forest soil food webs. The first experiment applied a simultaneous above- and belowground warming treatment (ambient, +1.7°C, +3.4°C) to closed canopy and recently clear-cut forest, simulating common forest disturbance6. The second experiment crossed warming with a summer drought treatment (-40% rainfall) in the clear-cut habitats. We show that warming reduces energy fluxes to microbes, while forest canopy disturbance and drought facilitates warming-induced increases in energy flux to higher trophic levels and exacerbates reductions in energy flux to microbes, respectively. Contrary to expectations, we find no change in whole-network resilience to perturbations, but significant losses of ecosystem functioning. Warming thus interacts with forest disturbance and drought, shaping the energetic structure of soil food webs and threatening the provisioning of multiple ecosystem functions in boreal-temperate ecotonal forests.

Direct and cascading impacts of tropical land-use change on multi-trophic biodiversity.

The conversion of tropical rainforest to agricultural systems such as oil palm alters biodiversity across a large range of interacting taxa and trophic levels. Yet, it remains unclear how direct and cascading effects of land-use change simultaneously drive ecological shifts. Combining data from a multi-taxon research initiative in Sumatra, Indonesia, we show that direct and cascading land-use effects alter biomass and species richness of taxa across trophic levels ranging from microorganisms to birds. Tropical land use resulted in increases in biomass and species richness via bottom-up cascading effects, but reductions via direct effects. When considering direct and cascading effects together, land use was found to reduce biomass and species richness, with increasing magnitude at higher trophic levels. Our analyses disentangle the multifaceted effects of land-use change on tropical ecosystems, revealing that biotic interactions on broad taxonomic scales influence the ecological outcome of anthropogenic perturbations to natural ecosystems.

Decreasing Stoichiometric Resource Quality Drives Compensatory Feeding across Trophic Levels in Tropical Litter Invertebrate Communities.

Living organisms are constrained by both resource quantity and quality. Ecological stoichiometry offers important insights into how the elemental composition of resources affects their consumers. If resource quality decreases, consumers can respond by shifting their body stoichiometry, avoiding low-quality resources, or up-regulating feeding rates to maintain the supply of required elements while excreting excess carbon (i.e., compensatory feeding). We analyzed multitrophic consumer body stoichiometry, biomass, and feeding rates along a resource-quality gradient in the litter of tropical forest and rubber and oil-palm plantations. Specifically, we calculated macroinvertebrate feeding rates based on consumer metabolic demand and assimilation efficiency. Using linear mixed effects models, we assessed resource-quality effects on macroinvertebrate detritivore and predator communities. We did not detect shifts in consumer body stoichiometry or decreases in consumer biomass in response to declining resource quality, as indicated by increasing carbon-to-nitrogen ratios. However, across trophic levels, we found a strong indication of decreasing resource quality leading to increased consumer feeding rates through altered assimilation efficiency and community body size structure. Our study reveals the influence of resource quality on multitrophic consumer feeding rates and suggests compensatory feeding to be more common across consumer trophic levels than was formerly known.

Resource stoichiometry and availability modulate species richness and biomass of tropical litter macro-invertebrates.

High biodiversity and biomass of soil communities are crucial for litter decomposition in terrestrial ecosystems such as tropical forests. However, the leaf litter that these communities consume is of particularly poor quality as indicated by elemental stoichiometry. The impact of resource quantity, quality and other habitat parameters on species richness and biomass of consumer communities is often studied in isolation, although much can be learned from simultaneously studying both community characteristics. Using a dataset of 780 macro-invertebrate consumer species across 32 sites in tropical lowland rain forest and agricultural systems on Sumatra, Indonesia, we investigated the effects of basal resource stoichiometry (C:X ratios of N, P, K, Ca, Mg, Na, S in local leaf litter), litter mass (basal resource quantity and habitat space), plant species richness (surrogate for litter habitat heterogeneity), and soil pH (acidity) on consumer species richness and biomass across different consumer groups (i.e. 3 feeding guilds and 10 selected taxonomic groups). In order to distinguish the most important predictors of consumer species richness and biomass, we applied a standardised model averaging approach investigating the effects of basal resource stoichiometry, litter mass, plant species richness and soil pH on both consumer community characteristics. This standardised approach enabled us to identify differences and similarities in the magnitude and importance of such effects on consumer species richness and biomass. Across consumer groups, we found litter mass to be the most important predictor of both species richness and biomass. Resource stoichiometry had a more pronounced impact on consumer species richness than on their biomass. As expected, taxonomic groups differed in which resource and habitat parameters (basal resource stoichiometry, litter mass, plant species richness and pH) were most important for modulating their community characteristics. The importance of litter mass for both species richness and biomass indicates that these tropical consumers strongly depend on habitat space and resource availability. Our study supports previous theoretical work indicating that consumer species richness is jointly influenced by resource availability and the balanced supply of multiple chemical elements in their resources.

A review of the ecosystem functions in oil palm plantations, using forests as a reference system.

Oil palm plantations have expanded rapidly in recent decades. This large-scale land-use change has had great ecological, economic, and social impacts on both the areas converted to oil palm and their surroundings. However, research on the impacts of oil palm cultivation is scattered and patchy, and no clear overview exists. We address this gap through a systematic and comprehensive literature review of all ecosystem functions in oil palm plantations, including several (genetic, medicinal and ornamental resources, information functions) not included in previous systematic reviews. We compare ecosystem functions in oil palm plantations to those in forests, as the conversion of forest to oil palm is prevalent in the tropics. We find that oil palm plantations generally have reduced ecosystem functioning compared to forests: 11 out of 14 ecosystem functions show a net decrease in level of function. Some functions show decreases with potentially irreversible global impacts (e.g. reductions in gas and climate regulation, habitat and nursery functions, genetic resources, medicinal resources, and information functions). The most serious impacts occur when forest is cleared to establish new plantations, and immediately afterwards, especially on peat soils. To variable degrees, specific plantation management measures can prevent or reduce losses of some ecosystem functions (e.g. avoid illegal land clearing via fire, avoid draining of peat, use of integrated pest management, use of cover crops, mulch, and compost) and we highlight synergistic mitigation measures that can improve multiple ecosystem functions simultaneously. The only ecosystem function which increases in oil palm plantations is, unsurprisingly, the production of marketable goods. Our review highlights numerous research gaps. In particular, there are significant gaps with respect to socio-cultural information functions. Further, there is a need for more empirical data on the importance of spatial and temporal scales, such as differences among plantations in different environments, of different sizes, and of different ages, as our review has identified examples where ecosystem functions vary spatially and temporally. Finally, more research is needed on developing management practices that can offset the losses of ecosystem functions. Our findings should stimulate research to address the identified gaps, and provide a foundation for more systematic research and discussion on ways to minimize the negative impacts and maximize the positive impacts of oil palm cultivation.