The coordination of green–brown food webs and their disruption by anthropogenic nutrient inputs

Although invasive plants are a major source of terrestrial ecosystem degradation worldwide, it remains unclear which trophic levels above the base of the food web are most vulnerable to plant invasions. We performed a meta-analysis of 38 independent studies from 32 papers to examine how invasive plants alter major groupings of primary and secondary consumers in three globally distributed ecosystems: wetlands, woodlands and grasslands. Within each ecosystem we examined if green (grazing) food webs are more sensitive to plant invasions compared to brown (detrital) food webs. Invasive plants have strong negative effects on primary consumers (detritivores, bacterivores, fungivores, and/or herbivores) in woodlands and wetlands, which become less abundant in both green and brown food webs in woodlands and green webs in wetlands. Plant invasions increased abundances of secondary consumers (predators and/or parasitoids) only in woodland brown food webs and green webs in wetlands. Effects of invasive plants on grazing and detrital food webs clearly differed between ecosystems. Overall, invasive plants had the most pronounced effects on the trophic structure of wetlands and woodlands, but caused no detectable changes to grassland trophic structure.

Nearly all ecosystems are contaminated with highly toxic methylmercury (MeHg), but the specific sources and pathways leading to the uptake of MeHg within and among food webs are not well understood. In this study, we report stable mercury (Hg) isotope compositions in food webs in a river and an adjacent forest in northern California and demonstrate the utility of Hg isotopes for studying MeHg sources and cross-habitat transfers. We observed large differences in both δ(202)Hg (mass-dependent fractionation) and Δ(199)Hg (mass-independent fractionation) within both food webs. The majority of isotopic variation within each food web could be accounted for by differing proportions of inorganic Hg [Hg(II)] and MeHg along food chains. We estimated mean isotope values of Hg(II) and MeHg in each habitat and found a large difference in δ(202)Hg between Hg(II) and MeHg (∼2.7‰) in the forest but not in the river (∼0.25‰). This is consistent with in situ Hg(II) methylation in the study river but suggests Hg(II) methylation may not be important in the forest. In fact, the similarity in δ(202)Hg between MeHg in forest food webs and Hg(II) in precipitation suggests that MeHg in forest food webs may be derived from atmospheric sources (e.g., rainfall, fog). Utilizing contrasting δ(202)Hg values between MeHg in river food webs (-1.0‰) and MeHg in forest food webs (+0.7‰), we estimate with a two-source mixing model that ∼55% of MeHg in two riparian spiders is derived from riverine sources while ∼45% of MeHg originates from terrestrial sources. Thus, stable Hg isotopes can provide new information on subtle differences in sources of MeHg and trace MeHg transfers within and among food webs in natural ecosystems.

Food web ecology has revolutionized our understanding of ecological processes, but the drivers of food web properties like trophic position (TP) and food chain length are notoriously enigmatic. In terrestrial ecosystems, above- and belowground systems were historically compartmentalized into "green" and "brown" food webs, but the coupling of these systems by animal consumers is increasingly recognized, with potential consequences for trophic structure. We used stable isotope analysis (δ13 C, δ15 N) of individual amino acids to trace the flow of essential biomolecules and jointly measure multichannel feeding, food web coupling, and TP in a guild of small mammals. We then tested the hypothesis that brown energy fluxes to aboveground consumers increase terrestrial food chain length via cryptic trophic transfers during microbial decomposition. We found that the average small mammal consumer acquired nearly 70% of their essential amino acids (69.0% ± 7.6%) from brown food webs, leading to significant increases in TP across species and functional groups. Fungi were the primary conduit of brown energy to aboveground consumers, providing nearly half the amino acid budget for small mammals on average (44.3% ± 12.0%). These findings illustrate the tightly coupled nature of green and brown food webs and show that microbially mediated energy flow ultimately regulates food web structure in aboveground consumers. Consequently, we propose that the integration of green and brown energy channels is a cryptic driver of food chain length in terrestrial ecosystems.

Riverine songbirds capture high levels of atmospheric mercury pollution from brown food webs in forests by mercury isotopic evidence.

A detailed and relatively evenly resolved food web of Little Rock Lake, Wisconsin, was constructed to evaluate the sensitivity of food—web patterns to the level of detail (degree of resolution) in food—web data. This study presents definitions (e.g., ecosystem food webs) and methods for constructing and reducing the resolution of food webs to provide relatively pragmatic and rigorous touchstones for consistency in future food—web studies. This analysis suggests that food—web patterns such as the scale—invariant links—per—species ratio, short chain lengths, and limited number of trophic levels are constrained by the resolution of food—web data rather than by ecological factors. Patterns less sensitive to changes in resolution such as directed connectance (the proportion of observed directed links to all possible directed links) may be robust food—web attributes. The food web of Little Rock Lake appears to be the first highly and evenly resolved food web of a large natural ecosystem originally documented for the purpose of examining quantitative food—web patterns. This ecosystem food web contains roughly twice as many species as the largest web to date. It also may provide the most credible portrait available of the detailed trophic structure of a whole ecosystem. The 93—trophic—species web of Little Rock Lake differs from previously published trophic—species webs by having more links per species (L/S = 11), longer chain lengths (average: ≥10, maximum: ≥16), species at higher trophic levels (maximum: = 12), higher fractions of intermediate species, and smaller fractions of top species and links to top species. The sensitivity of quantitative food—web patterns to changes in resolution was examined in several series of tropically aggregated Little Rock Lake webs. Each of the series starts with a highly and relatively evenly resolved web with 182 consumer, producer, and decomposer taxa and ends with low—resolution webs with 9 aggregates of taxa. Taxa were aggregated based on the proportion of predators and prey shared by the taxa. Different series of webs were generated using different criteria for linking aggregates to evaluate the sensitivity of food—web patterns to linkage criteria. The sensitivity analysis revealed that several, but not all, quantitative food—web patterns are very sensitive to systematic aggregation of the web. Sensitive patterns include number of links per species, linkage complexity, the distributions of chain lengths and species among trophic levels, and the proportions of top species and links to top species. Less—sensitive patterns include connectance, the ratio of predators to prey, the proportions of intermediate and basal species, and the proportions of links that are between intermediate and basal species. Directed connectance is the only pattern examined that is both very robust to trophic aggregation and generally comparable to other community webs. Quantitative food—web patterns in published community webs are generally similar to highly aggregated Little Rock Lake webs (versions with 9—40 aggregates). These findings suggest that previously described community food webs are severely aggregated versions of more elaborate webs similar to that of Little Rock Lake.

The brown-world role of insectivores: Frogs reduce plant growth by suppressing detritivores in an alpine meadow

Ecosystems worldwide receive large amounts of nutrients from both natural processes and human activities. While direct subsidy effects on primary production are relatively well-known (the green food web), the indirect effects of subsidies on producers as mediated by the brown food web and predators are poorly considered. With a dynamical green-brown food web model, parameterized using empirical estimates from the literature, we illustrate the effect of organic and inorganic nutrient subsidies on net primary production (NPP) (i.e., after removing loss to herbivory) in two idealized ecosystems—one terrestrial and one aquatic. We find that nutrient subsidies increase net primary production, an effect that saturates with increasing subsidies. Changing the quality of subsidies from inorganic to organic tends to increase net primary production in terrestrial ecosystems, but less often so in aquatic ecosystems. This occurs when organic nutrient inputs promote detritivores in the brown food web, and hence predators that in turn regulate herbivores, thereby promoting primary production. This previously largely overlooked effect is further enhanced by ecosystem properties such as fast decomposition and low rates of nutrient additions and demonstrates the importance of nutrient subsidy quality on ecosystem functioning.

The framework of ecological stoichiometry was developed primarily within the context of “green” autotroph-based food webs. While stoichiometric principles also apply in “brown” detritus-based systems, these systems have been historically understudied and differ from green ones in several important aspects including carbon (C) quality and the nutrient [nitrogen (N) and phosphorus (P)] contents of food resources for consumers. In this paper, we review work over the last decade that has advanced the application of ecological stoichiometry from green to brown food webs, focusing on freshwater ecosystems. We first review three focal areas where green and brown food webs differ: (1) bottom–up controls by light and nutrient availability, (2) stoichiometric constraints on consumer growth and nutritional regulation, and (3) patterns in consumer-driven nutrient dynamics. Our review highlights the need for further study of how light and nutrient availability affect autotroph–heterotroph interactions on detritus and the subsequent effects on consumer feeding and growth. To complement this conceptual review, we formally quantified differences in stoichiometric principles between green and brown food webs using a meta-analysis across feeding studies of freshwater benthic invertebrates. From 257 datasets collated across 46 publications and several unpublished studies, we compared effect sizes (Pearson’s r) of resource N:C and P:C on growth, consumption, excretion, and egestion between herbivorous and detritivorous consumers. The meta-analysis revealed that both herbivore and detritivore growth are limited by resource N:C and P:C contents, but effect sizes only among detritivores were significantly above zero. Consumption effect sizes were negative among herbivores but positive for detritivores in the case of both N:C and P:C, indicating distinct compensatory feeding responses across resource stoichiometry gradients. Herbivore P excretion rates responded significantly positively to resource P:C, whereas detritivore N and P excretion did not respond; detritivore N and P egestion responded positively to resource N:C and P:C, respectively. Our meta-analysis highlights resource N and P contents as broadly limiting in brown and green benthic food webs, but indicates contrasting mechanisms of limitation owing to differing consumer regulation. We suggest that green and brown food webs share fundamental stoichiometric principles, while identifying specific differences toward applying ecological stoichiometry across ecosystems.

In freshwater ecosystems, consumers can play large roles in nutrient cycling by modifying nutrient availability for autotrophic and heterotrophic microbes. Nutrients released by consumers directly support green food webs based on primary production and brown food webs based on decomposition. While much research has focused on impacts of consumer driven nutrient dynamics on green food webs, less attention has been given to studying the effects of these dynamics on brown food webs. Freshwater mussels (Bivalvia: Unionidae) can dominate benthic biomass in aquatic systems as they often occur in dense aggregations that create biogeochemical hotspots that can control ecosystem structure and function through nutrient release. However, despite functional similarities as filter‐feeders, mussels exhibit variation in nutrient excretion and tissue stoichiometry due in part to their phylogenetic origin. Here, we conducted a mesocosm experiment to evaluate how communities of three phylogenetically distinct species of mussels individually and collectively influence components of green and brown food webs. We predicted that the presence of mussels would elicit a positive response in both brown and green food webs by providing nutrients and energy via excretion and biodeposition to autotrophic and heterotrophic microbes. We also predicted that bottom‐up provisioning of nutrients would vary among treatments as a result of stoichiometric differences of species combinations, and that increasing species richness would lead to greater ecosystem functioning through complementarity resulting from greater trait diversity. Our results show that mussels affect the functioning of green and brown food webs through altering nutrient availability for both autotrophic and heterotrophic microbes. These effects are likely to be driven by phylogenetic constraints on tissue nutrient stoichiometry and consequential excretion stoichiometry, which can have functional effects on ecosystem processes. Our study highlights the importance of measuring multiple functional responses across a gradient of diversity in ecologically similar consumers to gain a more holistic view of aquatic food webs.

Summary The concepts of top‐down and bottom‐up controls are central to our understanding of cascading trophic effects on ecosystem functioning. Classical food web theory has focused either on food webs based on primary production (green food webs) or on food webs based on detritus (brown food webs) and generally ignored nutrient cycling. We argue that nutrient cycling connects the two food webs, which questions the traditional concept of top‐down and bottom‐up controls. By integrating these two food webs and nutrient cycling into simple models, we investigate the cascading effects from one food web to the other one. Both analytical calculations and simulations show that these two cascading effects depend on simple but distinct mechanisms that are derived from different ecological processes. Predators of decomposers can affect primary production in the green food chain. The signs of these effects are determined by relative proportions of nutrient cycling within the brown food chain. Cascading effects within the green food chain can affect decomposer production in a bottom‐up way. The carbon/nutrient limitation of decomposers determines the way the green food chain affects decomposer production. These theoretical findings are applicable to explore real interactions and cascading effects between the green and the brown food webs, such as pelagic–benthic interactions or above‐ground–below‐ground interactions.

Anthropogenic climate change can give rise to trophic mismatches in food webs owing to differential responses of consumer and resource organisms. However, we know little about the community and ecosystem level consequences of trophic mismatches in food webs. Terrestrial food webs are broadly comprised of two types of food webs: green food webs aboveground and brown food webs belowground between which mass and energy flow mainly via plants. Here, I highlight that the extent of warming-induced trophic mismatches in green and brown food webs differ owing to a greater stasis in brown food webs, which could trigger an imbalance in mass and energy flow between the two food webs. I then discuss the consequences of green–brown imbalance on terrestrial ecosystems and propose research avenues that can help understand the relationships between food webs and ecosystem functions in a warmer world.

Green vs brown food web: Effects of habitat type on multidimensional stability proxies for a highly-resolved Antarctic food web

Omnivory has been implicated in both diffusing and intensifying the effects of consumer control in food chains. Some have postulated that the strong, community level, top-down control apparent in lakes is not expressed in terrestrial systems because terrestrial food webs are reticulate, with high degrees of omnivory and diverse plant communities. In contrast, lake food webs are depicted as simple linear chains based on phytoplankton-derived energy. Here, we explore the dynamic implications of recent evidence showing that attached algal (periphyton) carbon contributes substantially to lake primary and secondary productivity, including fish production. Periphyton production represents a cryptic energy source in oligotrophic and mesotrophic lakes that is overlooked by previous theoretical treatment of trophic control in lakes. Literature data demonstrate that many fish are multi-chain omnivores, exploiting food chains based on both littoral and pelagic primary producers. Using consumer-resource models, we examine how multiple food chains affect fourth-level trophic control across nutrient gradients in lakes. The models predict that the stabilizing effects of linked food chains are strongest in lakes where both phytoplankton and periphyton contribute substantially to production of higher trophic levels. This stabilization enables a strong and persistent top down control on the pelagic food chain in mesotrophic lakes. The extension of classical trophic cascade theory to incorporate more complex food web structures driven by multi-chain predators provides a conceptual framework for analysis of reticulate food webs in ecosystems.

The role of environmental factors in aquatic ecosystems results from basic lake characteristics, human disturbances (‘cultural eutrophication’) and climate-related trends in the physical and chemical components of lakes. Although the influence of environmental factors on the abundance of aquatic animals is fairly well documented, less has been done to research their influence on food web interactions. The aim of the study was to evaluate microbial and classical food webs in lakes, with special emphasis placed on the role of environmental factors as influencing strengths. Variation partitioning, based on redundancy analysis, revealed that environmental factors played the most important role in structuring aquatic communities by accounting for 87.5% of their variation. Among all the factors measured, total solids (TS), transparency (Secchi disc) and temperature were most closely related to the variation in trophic communities. The analyses of food web interactions under low and high levels of those factors revealed that they differently influenced strengths among food web components. The strongest relations among distinct trophic levels were found under conditions of low TS, the lowest number of relations was found under conditions of low temperature. Only in low TS did bacteria correlate significantly with biogenes. Under high TS, bacteria positively influenced plenty of higher trophic levels. Top-down control was observed under conditions of high temperature. Conditions of low and high transparency did not diversify food web interactions. The obtained results can broaden our knowledge of the response of food webs to environmental factors in advanced stages of global eutrophication of water bodies and in the early stage of projected trends of global climate change.

The majority of research on food webs has focused on temperate lakes, and little is known about the food web of lakes in polar regions. Subarctic lakes are particularly sensitive to climate change, which affects their stability. Therefore, the trophic structure of the food web in such lakes was considered as the object of this study. We studied a clear-water oligotrophic lake located in the subarctic region of Eurasia, specifically in northern Karelia and the White Sea coast of Russia. The study examined both open water periods (summer–autumn) and ice-covered periods (winter–spring) in this lake. Stable isotope analysis of carbon (13C/12C ratio or δ13C value) and nitrogen (15N/14N, δ15N) in producers and consumers was applied and revealed significant seasonal variations in the structure of the food web. The results indicate the presence of both pelagic and littoral/benthic food web compartments, with a notable contribution of autochthonous carbon derived from benthic sources. Omnivorous fish (perch, Perca fluviatilis; vendace, Coregonus albula; nine-spined sticklebacks, Pungitius pungitius) and some benthic invertebrates (mayfly, Ephemera vulgata; bivalves, Sphaerium corneum) had intermediate δ13C values, integrating these compartments by obtaining resources from both. Planktonic invertebrates had significantly depleted 13C, with the lowest δ13C value reaching −41.7‰, indicating an important contribution of methane-derived carbon. The study also revealed close trophic relationships between lake invertebrates and cyanobacteria, namely with planktonic Dolichospermum lemmermannii and benthic Phormidium sp. Seasonal changes in δ15N values and in trophic position have been observed among predacious omnivorous fish and crustaceans (amphipods, Gammaracanthus loricatus, and copepods, Cyclops scutifer), which are capable of a generalist feeding strategy depending on food availability. Using the example of this lake, it can be concluded that polar lake ecosystems are characterized by different seasonal intakes of allochthonous organic carbon from wetland catchment (humic compounds) and nitrogen because of nitrogen fixation in the air by cyanoprocaryotes. Alternative energy sources, such as carbon derived from methane, can also contribute to the energy balance of lake ecosystems. This study contributes to our understanding of energy flow and connectivity between producers and consumers in high-latitude lakes.