Energetic constraints imposed on trophic interaction strengths enhance resilience in empirical and model food webs.

Food web stability and resilience are at the heart of understanding the structure and functioning of ecosystems. Previous studies show that models of empirical food webs are substantially more stable than random ones, due to a few strong interactions embedded in a majority of weak interactions. Analyses of trophic interaction loops show that in empirical food webs the patterns of the interaction strengths prevent the occurrence of destabilizing heavy loops and thereby enhances resilience. Yet, it is still unexplored which biological mechanisms cause these patterns that enhance food web resilience. We quantified food web resilience using the real part of the maximum eigenvalue of the Jacobian matrix of the food web from a seagrass bed in the Yellow River Delta (YRD) wetland, that could be parametrized by the empirical data of the food web. We found that the empirically based Jacobian matrix of the YRD food web indicated a much higher resilience than random matrices with the same element values but arranged in random ways. Investigating the trophic interaction loops revealed that the high resilience was due to a negative correlation between the negative and positive interaction strengths (per capita top-down and bottom-up effects, respectively) within positive feedback loops with three species. The negative correlation showed that when the negative interaction strengths were strong the positive was weak, and vice versa. Our invented reformulation of loop weight in terms of biomasses and specific production rates showed that energetic properties of the trophic groups in the loop and mass-balance constraints, for example, the food uptake has to balance all losses, created the negative correlation between the interaction strengths. This result could be generalized using a dynamic intraguild predation model, which delivered the same pattern for a wide range of model parameters. Our results shed light on how energetic constraints at the trophic group and food web level create a pattern of interaction strengths within trophic interaction loops that enhances food web resilience.

Modulation of Litter Decomposition by the Soil Microbial Food Web Under Influence of Land Use Change.

Soil microbial communities modulate soil organic matter (SOM) dynamics by catalyzing litter decomposition. However, our understanding of how litter-derived carbon (C) flows through the microbial portion of the soil food web is far from comprehensive. This information is necessary to facilitate reliable predictions of soil C cycling and sequestration in response to a changing environment such as land use change in the form of agricultural abandonment. To examine the flow of litter-derived C through the soil microbial food web and it's response to land use change, we carried out an incubation experiment with soils from six fields; three recently abandoned and three long term abandoned fields. In these soils, the fate of 13C-labeled plant litter was followed by analyzing phospholipid fatty acids (PLFA) over a period of 56 days. The litter-amended soils were sampled over time to measure 13CO2 and mineral N dynamics. Microbial 13C-incorporation patterns revealed a clear succession of microbial groups during litter decomposition. Fungi were first to incorporate 13C-label, followed by G- bacteria, G+ bacteria, actinomycetes and micro-fauna. The order in which various microbial groups responded to litter decomposition was similar across all the fields examined, with no clear distinction between recent and long-term abandoned soils. Although the microbial biomass was initially higher in long-term abandoned soils, the net amount of 13C-labeled litter that was incorporated by the soil microbial community was ultimately comparable between recent and long-term abandoned fields. In relative terms, this means there was a higher efficiency of litter-derived 13C-incorporation in recent abandoned soil microbial communities compared to long-term abandoned soils, most likely due to a net shift from SOM-derived C toward root-derived C input in the soil microbial food web following land-abandonment.

How habitat-modifying organisms structure the food web of two coastal ecosystems.

The diversity and structure of ecosystems has been found to depend both on trophic interactions in food webs and on other species interactions such as habitat modification and mutualism that form non-trophic interaction networks. However, quantification of the dependencies between these two main interaction networks has remained elusive. In this study, we assessed how habitat-modifying organisms affect basic food web properties by conducting in-depth empirical investigations of two ecosystems: North American temperate fringing marshes and West African tropical seagrass meadows. Results reveal that habitat-modifying species, through non-trophic facilitation rather than their trophic role, enhance species richness across multiple trophic levels, increase the number of interactions per species (link density), but decrease the realized fraction of all possible links within the food web (connectance). Compared to the trophic role of the most highly connected species, we found this non-trophic effects to be more important for species richness and of more or similar importance for link density and connectance. Our findings demonstrate that food webs can be fundamentally shaped by interactions outside the trophic network, yet intrinsic to the species participating in it. Better integration of non-trophic interactions in food web analyses may therefore strongly contribute to their explanatory and predictive capacity.

Food-web stability signals critical transitions in temperate shallow lakes.

A principal aim of ecologists is to identify critical levels of environmental change beyond which ecosystems undergo radical shifts in their functioning. Both food-web theory and alternative stable states theory provide fundamental clues to mechanisms conferring stability to natural systems. Yet, it is unclear how the concept of food-web stability is associated with the resilience of ecosystems susceptible to regime change. Here, we use a combination of food web and ecosystem modelling to show that impending catastrophic shifts in shallow lakes are preceded by a destabilizing reorganization of interaction strengths in the aquatic food web. Analysis of the intricate web of trophic interactions reveals that only few key interactions, involving zooplankton, diatoms and detritus, dictate the deterioration of food-web stability. Our study exposes a tight link between food-web dynamics and the dynamics of the whole ecosystem, implying that trophic organization may serve as an empirical indicator of ecosystem resilience.

Intensive agriculture reduces soil biodiversity across Europe.

Soil biodiversity plays a key role in regulating the processes that underpin the delivery of ecosystem goods and services in terrestrial ecosystems. Agricultural intensification is known to change the diversity of individual groups of soil biota, but less is known about how intensification affects biodiversity of the soil food web as a whole, and whether or not these effects may be generalized across regions. We examined biodiversity in soil food webs from grasslands, extensive, and intensive rotations in four agricultural regions across Europe: in Sweden, the UK, the Czech Republic and Greece. Effects of land-use intensity were quantified based on structure and diversity among functional groups in the soil food web, as well as on community-weighted mean body mass of soil fauna. We also elucidate land-use intensity effects on diversity of taxonomic units within taxonomic groups of soil fauna. We found that between regions soil food web diversity measures were variable, but that increasing land-use intensity caused highly consistent responses. In particular, land-use intensification reduced the complexity in the soil food webs, as well as the community-weighted mean body mass of soil fauna. In all regions across Europe, species richness of earthworms, Collembolans, and oribatid mites was negatively affected by increased land-use intensity. The taxonomic distinctness, which is a measure of taxonomic relatedness of species in a community that is independent of species richness, was also reduced by land-use intensification. We conclude that intensive agriculture reduces soil biodiversity, making soil food webs less diverse and composed of smaller bodied organisms. Land-use intensification results in fewer functional groups of soil biota with fewer and taxonomically more closely related species. We discuss how these changes in soil biodiversity due to land-use intensification may threaten the functioning of soil in agricultural production systems.

Infectious disease agents mediate interaction in food webs and ecosystems.

Infectious agents are part of food webs and ecosystems via the relationship with their host species that, in turn, interact with both hosts and non-hosts. Through these interactions, infectious agents influence food webs in terms of structure, functioning and stability. The present literature shows a broad range of impacts of infectious agents on food webs, and by cataloguing that range, we worked towards defining the various mechanisms and their specific effects. To explore the impact, a direct approach is to study changes in food-web properties with infectious agents as separate species in the web, acting as additional nodes, with links to their host species. An indirect approach concentrates not on adding new nodes and links, but on the ways that infectious agents affect the existing links across host and non-host nodes, by influencing the 'quality' of consumer-resource interaction as it depends on the epidemiological state host involved. Both approaches are natural from an ecological point of view, but the indirect approach may connect more straightforwardly to commonly used tools in infectious disease dynamics.

Low investment in sexual reproduction threatens plants adapted to phosphorus limitation.

Plant species diversity in Eurasian wetlands and grasslands depends not only on productivity but also on the relative availability of nutrients, particularly of nitrogen and phosphorus. Here we show that the impacts of nitrogen:phosphorus stoichiometry on plant species richness can be explained by selected plant life-history traits, notably by plant investments in growth versus reproduction. In 599 Eurasian sites with herbaceous vegetation we examined the relationship between the local nutrient conditions and community-mean life-history traits. We found that compared with plants in nitrogen-limited communities, plants in phosphorus-limited communities invest little in sexual reproduction (for example, less investment in seed, shorter flowering period, longer lifespan) and have conservative leaf economy traits (that is, a low specific leaf area and a high leaf dry-matter content). Endangered species were more frequent in phosphorus-limited ecosystems and they too invested little in sexual reproduction. The results provide new insight into how plant adaptations to nutrient conditions can drive the distribution of plant species in natural ecosystems and can account for the vulnerability of endangered species.

Soil food web changes during spontaneous succession at post mining sites: a possible ecosystem engineering effect on food web organization?

Parameters characterizing the structure of the decomposer food web, biomass of the soil microflora (bacteria and fungi) and soil micro-, meso- and macrofauna were studied at 14 non-reclaimed 1- 41-year-old post-mining sites near the town of Sokolov (Czech Republic). These observations on the decomposer food webs were compared with knowledge of vegetation and soil microstructure development from previous studies. The amount of carbon entering the food web increased with succession age in a similar way as the total amount of C in food web biomass and the number of functional groups in the food web. Connectance did not show any significant changes with succession age, however. In early stages of the succession, the bacterial channel dominated the food web. Later on, in shrub-dominated stands, the fungal channel took over. Even later, in the forest stage, the bacterial channel prevailed again. The best predictor of fungal bacterial ratio is thickness of fermentation layer. We argue that these changes correspond with changes in topsoil microstructure driven by a combination of plant organic matter input and engineering effects of earthworms. In early stages, soil is alkaline, and a discontinuous litter layer on the soil surface promotes bacterial biomass growth, so the bacterial food web channel can dominate. Litter accumulation on the soil surface supports the development of the fungal channel. In older stages, earthworms arrive, mix litter into the mineral soil and form an organo-mineral topsoil, which is beneficial for bacteria and enhances the bacterial food web channel.

Soil food web properties explain ecosystem services across European land use systems.

Intensive land use reduces the diversity and abundance of many soil biota, with consequences for the processes that they govern and the ecosystem services that these processes underpin. Relationships between soil biota and ecosystem processes have mostly been found in laboratory experiments and rarely are found in the field. Here, we quantified, across four countries of contrasting climatic and soil conditions in Europe, how differences in soil food web composition resulting from land use systems (intensive wheat rotation, extensive rotation, and permanent grassland) influence the functioning of soils and the ecosystem services that they deliver. Intensive wheat rotation consistently reduced the biomass of all components of the soil food web across all countries. Soil food web properties strongly and consistently predicted processes of C and N cycling across land use systems and geographic locations, and they were a better predictor of these processes than land use. Processes of carbon loss increased with soil food web properties that correlated with soil C content, such as earthworm biomass and fungal/bacterial energy channel ratio, and were greatest in permanent grassland. In contrast, processes of N cycling were explained by soil food web properties independent of land use, such as arbuscular mycorrhizal fungi and bacterial channel biomass. Our quantification of the contribution of soil organisms to processes of C and N cycling across land use systems and geographic locations shows that soil biota need to be included in C and N cycling models and highlights the need to map and conserve soil biodiversity across the world.

Redefining plant systems biology: from cell to ecosystem.

Molecular biologists typically restrict systems biology to cellular levels. By contrast, ecologists define biological systems as communities of interacting individuals at different trophic levels that process energy, nutrient and information flows. Modern plant breeding needs to increase agricultural productivity while decreasing the ecological footprint. This requires a holistic systems biology approach that couples different aggregation levels while considering the variables that affect these biological systems from cell to community. The challenge is to generate accurate experimental data that can be used together with modelling concepts and techniques that allow experimentally verifying in silico predictions. The coupling of aggregation levels in plant sciences, termed Integral Quantification of Biological Organization (IQ(BiO)), might enhance our abilities to generate new desired plant phenotypes.

Robust scaling in ecosystems and the meltdown of patch size distributions before extinction.

Robust critical systems are characterized by power laws which occur over a broad range of conditions. Their robust behaviour has been explained by local interactions. While such systems could be widespread in nature, their properties are not well understood. Here, we study three robust critical ecosystem models and a null model that lacks spatial interactions. In all these models, individuals aggregate in patches whose size distributions follow power laws which melt down under increasing external stress. We propose that this power-law decay associated with the connectivity of the system can be used to evaluate the level of stress exerted on the ecosystem. We identify several indicators along the transition to extinction. These indicators give us a relative measure of the distance to extinction, and have therefore potential application to conservation biology, especially for ecosystems with self-organization and critical transitions.

Resource contrast in patterned peatlands increases along a climatic gradient.

Spatial patterning of ecosystems can be explained by several mechanisms. One approach to disentangling the influence of these mechanisms is to study a patterned ecosystem along a gradient of environmental conditions. This study focused on hummock-hollow patterning of peatlands. Previous models predicted that patterning in drainage-dominated peatlands is driven by a peat-accumulation mechanism, reflected by higher nutrient availability in hollows relative to hummocks. Alternatively, patterning in evapotranspiration (ET)-dominated peatlands may be driven by a nutrient-accumulation mechanism, reflected by reversed nutrient distribution, namely, higher nutrient availability in hummocks relative to hollows. Here, we tested these predictions by comparing nutrient distributions among patterned peatlands in maritime (Scotland), humid temperate (Sweden), and humid continental (Siberia) climates. The areas comprise a climatic gradient from very wet and drainage-dominated (Scotland) to less wet and ET-dominated (Siberia) peatlands. Nutrient distribution was quantified as resource contrast, a measure for hummock-hollow difference in nutrient availability. We tested the hypothesis that the climatic gradient shows a trend in the resource contrast; from negative (highest nutrient availability in hollows) in Scotland to positive (highest nutrient availability in hummocks) in Siberia. The resource contrasts as measured in vegetation indeed showed a trend along the climatic gradient: contrasts were negative to slightly positive in Scotland, positive in Sweden, and strongly positive in Siberia. This finding corroborates the main prediction of previous models. Our results, however, also provided indications for further model development. The low concentrations of nutrients in the water suggest that existing models could be improved by considering both the dissolved and adsorbed phase and explicit inclusion of both nutrient-uptake and nutrient-storage processes. Our study suggests that future climate change may affect the ecosystem functioning of patterned peatlands by altering the contribution of pattern-forming mechanisms to redistribution of water and nutrients within these systems.

Complexity in quantitative food webs.

Food webs depict who eats whom in communities. Ecologists have examined statistical metrics and other properties of food webs, but mainly due to the uneven quality of the data, the results have proved controversial. The qualitative data on which those efforts rested treat trophic interactions as present or absent and disregard potentially huge variation in their magnitude, an approach similar to analyzing traffic without differentiating between highways and side roads. More appropriate data are now available and were used here to analyze the relationship between trophic complexity and diversity in 59 quantitative food webs from seven studies (14-202 species) based on recently developed quantitative descriptors. Our results shed new light on food-web structure. First, webs are much simpler when considered quantitatively, and link density exhibits scale invariance or weak dependence on food-web size. Second, the "constant connectance" hypothesis is not supported: connectance decreases with web size in both qualitative and quantitative data. Complexity has occupied a central role in the discussion of food-web stability, and we explore the implications for this debate. Our findings indicate that larger webs are more richly endowed with the weak trophic interactions that recent theories show to be responsible for food-web stability.

Nutrients and hydrology indicate the driving mechanisms of peatland surface patterning.

Peatland surface patterning motivates studies that identify underlying structuring mechanisms. Theoretical studies so far suggest that different mechanisms may drive similar types of patterning. The long time span associated with peatland surface pattern formation, however, limits possibilities for empirically testing model predictions by field manipulations. Here, we present a model that describes spatial interactions between vegetation, nutrients, hydrology, and peat. We used this model to study pattern formation as driven by three different mechanisms: peat accumulation, water ponding, and nutrient accumulation. By on-and-off switching of each mechanism, we created a full-factorial design to see how these mechanisms affected surface patterning (pattern of vegetation and peat height) and underlying patterns in nutrients and hydrology. Results revealed that different combinations of structuring mechanisms lead to similar types of peatland surface patterning but contrasting underlying patterns in nutrients and hydrology. These contrasting underlying patterns suggest that the presence or absence of the structuring mechanisms can be identified by relatively simple short-term field measurements of nutrients and hydrology, meaning that longer-term field manipulations can be circumvented. Therefore, this study provides promising avenues for future empirical studies on peatland patterning.

Reconciling complexity with stability in naturally assembling food webs.

Understanding how complex food webs assemble through time is fundamental both for ecological theory and for the development of sustainable strategies of ecosystem conservation and restoration. The build-up of complexity in communities is theoretically difficult, because in random-pattern models complexity leads to instability. There is growing evidence, however, that nonrandom patterns in the strengths of the interactions between predators and prey strongly enhance system stability. Here we show how such patterns explain stability in naturally assembling communities. We present two series of below-ground food webs along natural productivity gradients in vegetation successions. The complexity of the food webs increased along the gradients. The stability of the food webs was captured by measuring the weight of feedback loops of three interacting 'species' locked in omnivory. Low predator-prey biomass ratios in these omnivorous loops were shown to have a crucial role in preserving stability as productivity and complexity increased during succession. Our results show the build-up of food-web complexity in natural productivity gradients and pin down the feedback loops that govern the stability of whole webs. They show that it is the heaviest three-link feedback loop in a network of predator-prey effects that limits its stability. Because the weight of these feedback loops is kept relatively low by the biomass build-up in the successional process, complexity does not lead to instability.

Spatial vegetation patterns and imminent desertification in Mediterranean arid ecosystems.

Humans and climate affect ecosystems and their services, which may involve continuous and discontinuous transitions from one stable state to another. Discontinuous transitions are abrupt, irreversible and among the most catastrophic changes of ecosystems identified. For terrestrial ecosystems, it has been hypothesized that vegetation patchiness could be used as a signature of imminent transitions. Here, we analyse how vegetation patchiness changes in arid ecosystems with different grazing pressures, using both field data and a modelling approach. In the modelling approach, we extrapolated our analysis to even higher grazing pressures to investigate the vegetation patchiness when desertification is imminent. In three arid Mediterranean ecosystems in Spain, Greece and Morocco, we found that the patch-size distribution of the vegetation follows a power law. Using a stochastic cellular automaton model, we show that local positive interactions among plants can explain such power-law distributions. Furthermore, with increasing grazing pressure, the field data revealed consistent deviations from power laws. Increased grazing pressure leads to similar deviations in the model. When grazing was further increased in the model, we found that these deviations always and only occurred close to transition to desert, independent of the type of transition, and regardless of the vegetation cover. Therefore, we propose that patch-size distributions may be a warning signal for the onset of desertification.

Functional stability of microbial communities from long-term stressed soils to additional disturbance.

Functional stability, measured in terms of resistance and resilience of soil respiration rate and bacterial growth rate, was studied in soils from field plots that have been exposed to copper contamination and low pH for more than two decades. We tested whether functional stability follows patterns predicted by either the "low stress-high stability" or the "high stress-high stability" theory. Treatments consisting of soils with no or high copper load (0 or 750 kg/ha) and with low or neutral pH (4.0 or 6.1) were used. Stability was examined by applying an additional disturbance by heat (50 degrees C for 18 h) or drying-rewetting cycles. After heating, the respiration rate indicated that the soils without copper were less stable (more affected) than the soils with 750 kg/ha. Bacterial growth rate was more stable (resistant) to heat in the pH 6.1 than in the pH 4.0 soils. Growth rate was stimulated rather than inhibited by heating and was highly resilient in all soils. The respiration rate was less affected by drying-rewetting cycles in the pH 4.0 soils than in the pH 6.1 soils. Bacterial growth rate after drying-rewetting disturbance showed no distinct pattern of stability. We found that the stability of a particular process could vary significantly, depending on the kind of disturbance; therefore, neither of the two theories could adequately predict the response of the microbial community to disturbance.

Self-organized patchiness and catastrophic shifts in ecosystems.

Unexpected sudden catastrophic shifts may occur in ecosystems, with concomitant losses or gains of ecological and economic resources. Such shifts have been theoretically attributed to positive feedback and bistability of ecosystem states. However, verifications and predictive power with respect to catastrophic responses to a changing environment are lacking for spatially extensive ecosystems. This situation impedes management and recovery strategies for such ecosystems. Here, we review recent studies on various ecosystems that link self-organized patchiness to catastrophic shifts between ecosystem states.