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Constraints and variation in food web link-species space
Predicting food web structure in future climates is a pressing goal of ecology. These predictions may be impossible without a solid understanding of the factors that structure current food webs. Here, the most fundamental aspect of food web structure—the relationship between the number of links and species—is still poorly understood. Some species interactions may be physically or physiologically ‘forbidden'—like consumption by non-consumer species—with possible consequences for food web structure. We show that accounting for these ‘forbidden interactions' constrains the feasible link-species space, in tight agreement with empirical data. Rather than following one particular scaling relationship, food webs are distributed throughout this space according to shared biotic and abiotic features. Our study provides new insights into the long-standing question of which factors determine this fundamental aspect of food web structure.
Genetic and plastic rewiring of food webs under climate change
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Predator mass mortality events restructure food webs through trophic decoupling
Predators have a key role in structuring ecosystems. However, predator loss is accelerating globally, and predator mass-mortality events (MMEs)—rapid large-scale die-offs—are now emblematic of the Anthropocene epoch. Owing to their rare and unpredictable nature, we lack an understanding of how MMEs immediately impact ecosystems. Past predator-removal studies may be insufficient to understand the ecological consequences of MMEs because, in nature, dead predators decompose in situ and generate a resource pulse, which could alter ensuing ecosystem dynamics by temporarily enhancing productivity. Here we experimentally induce MMEs in tritrophic, freshwater lake food webs and report ecological dynamics that are distinct from predator losses or resource pulses alone, but that can be predicted from theory. MMEs led to the proliferation of diverse consumer and producer communities resulting from weakened top-down predator control and stronger bottom-up effects through predator decomposition. In contrast to predator removals alone, enhanced primary production after MMEs dampened the consumer community response. As a consequence, MMEs generated biomass dynamics that were most similar to those of undisturbed systems, indicating that they may be cryptic disturbances in nature. These biomass dynamics led to trophic decoupling, whereby the indirect beneficial effects of predators on primary producers are lost and later materialize as direct bottom-up effects that stimulate primary production amid intensified herbivory. Furthermore, these results reveal ecological signatures of MMEs and demonstrate the feasibility of forecasting novel ecological dynamics arising with intensifying global change.
Temperature and nutrients drive eco-phenotypic dynamics in a microbial food web
Anthropogenic increases in temperature and nutrient loads will likely impact food web structure and stability. Although their independent effects have been reasonably well studied, their joint effects—particularly on coupled ecological and phenotypic dynamics—remain poorly understood. Here we experimentally manipulated temperature and nutrient levels in microbial food webs and used time-series analysis to quantify the strength of reciprocal effects between ecological and phenotypic dynamics across trophic levels. We found that (1) joint—often interactive—effects of temperature and nutrients on ecological dynamics are more common at higher trophic levels, (2) temperature and nutrients interact to shift the relative strength of top-down versus bottom-up control, and (3) rapid phenotypic change mediates observed ecological responses to changes in temperature and nutrients. Our results uncover how feedback between ecological and phenotypic dynamics mediate food web responses to environmental change. As a result, this suggests important but previously unknown ways that temperature and nutrients might jointly control the rapid eco-phenotypic feedback that determine food web dynamics in a changing world.
Food web dynamics drive variation in Smallmouth Bass Micropterus dolomieu mercury contamination in protected Southern Appalachian streams
Mercury is a global pollutant that threatens otherwise protected aquatic ecosystems. Mercury food web dynamics are not well understood in streams with no point sources of contamination but have the potential to concentrate this dangerous pollutant in upper trophic level consumers. A 2016 study revealed that mercury concentrations of Smallmouth Bass Micropterus dolomieu varied between three streams in Great Smoky Mountains National Park (GSMNP), Tennessee, USA. We tested the hypothesis that food web interactions drive spatial variation in mercury concentrations of the apex predator of protected stream ecosystems. We measured carbon and nitrogen stable isotope ratios, and mercury concentrations of eight food web components of GSMNP streams including basal resources, intermediate consumers, and Smallmouth Bass, the apex predator. Mean THg concentrations of basal resources did not differ between streams, but the spatial pattern of concentrations of intermediate consumers mirrored Smallmouth Bass. Relationships between organismal contaminant concentrations and trophic level were positive in all three streams, indicating biomagnification is occurring in the protected streams of GSMNP. Furthermore, our findings indicate that mercury dynamics in intermediate trophic levels, rather than differences in basal resource concentrations, may drive differences in mercury contamination of apex predators of the protected stream ecosystems of GSMNP.
Integrating viruses into soil food web biogeochemistry
The soil microbiome is recognized as an essential component of healthy soils. Viruses are also diverse and abundant in soils, but their roles in soil systems remain unclear. Here we argue for the consideration of viruses in soil microbial food webs and describe the impact of viruses on soil biogeochemistry. The soil food web is an intricate series of trophic levels that span from autotrophic microorganisms to plants and animals. Each soil system encompasses contrasting and dynamic physicochemical conditions, with labyrinthine habitats composed of particles. Conditions are prone to shifts in space and time, and this variability can obstruct or facilitate interactions of microorganisms and viruses. Because viruses can infect all domains of life, they must be considered as key regulators of soil food web dynamics and biogeochemical cycling. Finally, we highlight future research avenues that will enable a more robust understanding of the roles of viruses in soil function and health.
Mutualism increases diversity, stability, and function of multiplex networks that integrate pollinators into food webs
Ecosystems are composed of complex networks of many species interacting in different ways. While ecologists have long studied food webs of feeding interactions, recent studies increasingly focus on mutualistic networks including plants that exchange food for reproductive services provided by animals such as pollinators. Here, we synthesize both types of consumer-resource interactions to better understand the controversial effects of mutualism on ecosystems at the species, guild, and whole-community levels. We find that consumer-resource mechanisms underlying plant-pollinator mutualisms can increase persistence, productivity, abundance, and temporal stability of both mutualists and non-mutualists in food webs. These effects strongly increase with floral reward productivity and are qualitatively robust to variation in the prevalence of mutualism and pollinators feeding upon resources in addition to rewards. This work advances the ability of mechanistic network theory to synthesize different types of interactions and illustrates how mutualism can enhance the diversity, stability, and function of complex ecosystems.
Ectomycorrhizal fungi alter soil food webs and the functional potential of bacterial communities
Most of Earth’s trees rely on critical soil nutrients that ectomycorrhizal fungi (EcMF) liberate and provide, and all of Earth’s land plants associate with bacteria that help them survive in nature. Yet, our understanding of how the presence of EcMF modifies soil bacterial communities, soil food webs, and root chemistry requires direct experimental evidence to comprehend the effects that EcMF may generate in the belowground plant microbiome. To this end, we grew Pinus muricata plants in soils that were either inoculated with EcMF and native forest bacterial communities or only native bacterial communities. We then profiled the soil bacterial communities, applied metabolomics and lipidomics, and linked omics data sets to understand how the presence of EcMF modifies belowground biogeochemistry, bacterial community structure, and their functional potential. We found that the presence of EcMF (i) enriches soil bacteria linked to enhanced plant growth in nature, (ii) alters the quantity and composition of lipid and non-lipid soil metabolites, and (iii) modifies plant root chemistry toward pathogen suppression, enzymatic conservation, and reactive oxygen species scavenging. Using this multi-omic approach, we therefore show that this widespread fungal symbiosis may be a common factor for structuring soil food webs.
Experimental nitrogen and phosphorus enrichment stimulates multiple trophic levels of algal and detrital-based food webs: a global meta-analysis from streams and rivers
Anthropogenic increases in nitrogen (N) and phosphorus (P) concentrations can strongly influence the structure and function of ecosystems. Even though lotic ecosystems receive cumulative inputs of nutrients applied to and deposited on land, no comprehensive assessment has quantified nutrient-enrichment effects within streams and rivers. We conducted a meta-analysis of published studies that experimentally increased concentrations of N and/or P in streams and rivers to examine how enrichment alters ecosystem structure (state: primary producer and consumer biomass and abundance) and function (rate: primary production, leaf breakdown rates, metabolism) at multiple trophic levels (primary producer, microbial heterotroph, primary and secondary consumers, and integrated ecosystem). Our synthesis included 184 studies, 885 experiments, and 3497 biotic responses to nutrient enrichment. We documented widespread increases in organismal biomass and abundance (mean response = +48%) and rates of ecosystem processes (+54%) to enrichment across multiple trophic levels, with no large differences in responses among trophic levels or between autotrophic or heterotrophic food-web pathways. Responses to nutrient enrichment varied with the nutrient added (N, P, or both) depending on rate versus state variable and experiment type, and were greater in flume and whole-stream experiments than in experiments using nutrient-diffusing substrata. Generally, nutrient-enrichment effects also increased with water temperature and light, and decreased under elevated ambient concentrations of inorganic N and/or P. Overall, increased concentrations of N and/or P altered multiple food-web pathways and trophic levels in lotic ecosystems. Finally, our results indicate that preservation or restoration of biodiversity and ecosystem functions of streams and rivers requires management of nutrient inputs and consideration of multiple trophic pathways.
Arbuscular mycorrhiza convey significant plant carbon to a diverse hyphosphere microbial food web and mineral‐associated organic matter
Summary Arbuscular mycorrhizal fungi (AMF) transport substantial plant carbon (C) that serves as a substrate for soil organisms, a precursor of soil organic matter (SOM), and a driver of soil microbial dynamics. Using two‐chamber microcosms where an air gap isolated AMF from roots, we 13 CO 2 ‐labeled Avena barbata for 6 wk and measured the C Rhizophagus intraradices transferred to SOM and hyphosphere microorganisms. NanoSIMS imaging revealed hyphae and roots had similar 13 C enrichment. SOM density fractionation, 13 C NMR, and IRMS showed AMF transferred 0.77 mg C g −1 of soil (increasing total C by 2% relative to non‐mycorrhizal controls); 33% was found in occluded or mineral‐associated pools. In the AMF hyphosphere, there was no overall change in community diversity but 36 bacterial ASVs significantly changed in relative abundance. With stable isotope probing (SIP)‐enabled shotgun sequencing, we found taxa from the Solibacterales, Sphingobacteriales, Myxococcales, and Nitrososphaerales (ammonium oxidizing archaea) were highly enriched in AMF‐imported 13 C (> 20 atom%). Mapping sequences from 13 C‐SIP metagenomes to total ASVs showed at least 92 bacteria and archaea were significantly 13 C‐enriched. Our results illustrate the quantitative and ecological impact of hyphal C transport on the formation of potentially protective SOM pools and microbial roles in the AMF hyphosphere soil food web.
Three‐trophic level food webs support the safety of a biocontrol agent 3 years after release
Biological control (biocontrol) is a powerful tool for managing invasive alien species and assisting the restoration of native ecosystems. Rigorous post‐release monitoring of biocontrol agents is critical to evaluate the success of biocontrol programs; however, this is still rarely implemented. Here, we combined the use of species interaction networks with a Before‐After Control‐Impact design to evaluate the target and non‐target, direct and indirect effects of the Australian gall wasp Trichilogaster acaciaelongifoliae , released to control the invasive plant Acacia longifolia in Portugal. We compared the structure of plant‐galling insect‐parasitoid food webs before and 3 years after the release of the biocontrol agent. Exhaustive sampling did not detect any non‐target effects, either direct (on non‐target plants) or indirect (on other galling insects via shared plants). Additionally, no significant changes were detected in network structure that could be related to the establishment of the biocontrol agent. This study shows that monitoring biocontrol at the community level is possible and that, when carefully planned, biocontrol poses minimal risk of non‐target effects.
Mixotrophic microbes create carbon tipping points under warming
Mixotrophs are ubiquitous and integral to microbial food webs, but their impacts on the dynamics and functioning of broader ecosystems are largely unresolved. Here, we show that mixotrophy produces a unique type of food web module that exhibits unusual ecological dynamics, with surprising consequences for carbon flux under warming. We develop a generalizable model of a mixotrophic food web module that incorporates dynamic switching between phototrophy and phagotrophy to assess ecological dynamics and total system CO 2 flux. We find that warming switches mixotrophic systems between alternative stable carbon states—including a phototrophy-dominant carbon sink state, a phagotrophy-dominant carbon source state and cycling between these two. Moreover, warming always shifts this mixotrophic system from a carbon sink state to a carbon source state, but a coordinated increase in nutrients can erase early warning signals of this transition and expand hysteresis. This suggests that mixotrophs can generate critical carbon tipping points under warming that will be more abrupt and less reversible when combined with increased nutrient levels, having widespread implications for ecosystem functioning in the face of rapid global change.
Environmental fate of radiocesium in biota inhabiting a contaminated ecosystem on the U.S. Department of Energy's Savannah River Site
Although biomagnification of radiocesium ( 137 Cs) has been reported in food webs, most previous research has been limited to select trophic linkages. Few studies have included a comprehensive survey of fauna associated with aquatic, semi-aquatic, and terrestrial habitats within a single study framework. The objectives of this study were to advance our understanding of the dynamics of 137 Cs accumulation within food webs by quantifying 137 Cs activity across a wide range of biota found within a contaminated canal, as well as test the hypothesis that life-stage and body size influence 137 Cs bioaccumulation in select herpetofauna. With extensive sampling across multiple taxa collected from a contaminated canal system and associated floodplain on the Savannah River Site, we assessed 137 Cs activity and stable nitrogen isotopes for both aquatic organisms that were restricted to the contaminated effluent canal, and semi-aquatic organisms able to move freely between the contaminated canal and the adjacent uncontaminated terrestrial habitat. We found 137 Cs activity to be highly variable among species, with evidence for and against biomagnification in semi-aquatic and aquatic organisms, respectively. Furthermore, 137 Cs activity decreased with life stage and body size in bullfrogs (Lithobates catesbeianus), despite post-metamorphic bullfrogs having a more carnivorous diet compared to tadpoles, while cottonmouths (Agkistrodon piscivorus) retained similar 137 Cs activity regardless of their age and size. While evidence of biomagnification has been observed in some contaminated systems, results of our study suggest the extent to which 137 Cs biomagnifies within food webs is context-dependent and likely influenced by a suite of biotic and abiotic factors. Further, our data indicate sampling of a broad suite of species and environmental attributes are needed to elucidate the fate and dynamics of anthropogenic pollutants within contaminated ecosystems.
Viral infections likely mediate microbial controls on ecosystem responses to global warming
Abstract Climate change is affecting how energy and matter flow through ecosystems, thereby altering global carbon and nutrient cycles. Microorganisms play a fundamental role in carbon and nutrient cycling and are thus an integral link between ecosystems and climate. Here, we highlight a major black box hindering our ability to anticipate ecosystem climate responses: viral infections within complex microbial food webs. We show how understanding and predicting ecosystem responses to warming could be challenging—if not impossible—without accounting for the direct and indirect effects of viral infections on different microbes (bacteria, archaea, fungi, protists) that together perform diverse ecosystem functions. Importantly, understanding how rising temperatures associated with climate change influence viruses and virus-host dynamics is crucial to this task, yet is severely understudied. In this perspective, we (i) synthesize existing knowledge about virus-microbe-temperature interactions and (ii) identify important gaps to guide future investigations regarding how climate change might alter microbial food web effects on ecosystem functioning. To provide real-world context, we consider how these processes may operate in peatlands—globally significant carbon sinks that are threatened by climate change. We stress that understanding how warming affects biogeochemical cycles in any ecosystem hinges on disentangling complex interactions and temperature responses within microbial food webs.
Contrary effects of phytoplankton Chlorella vulgaris and its exudates on mercury methylation by iron- and sulfate-reducing bacteria
Mercury (Hg) is a pervasive environmental pollutant and poses serious health concerns as inorganic Hg(II) can be converted to the neurotoxin methylmercury (MeHg), which bioaccumulates and biomagnifies in food webs. Phytoplankton, representing the base of aquatic food webs, can take up Hg(II) and influence MeHg production, but currently little is known about how and to what extent phytoplankton may impact Hg(II) methylation by itself or by methylating bacteria it harbors. This study investigated whether some species of phytoplankton could produce MeHg and how the live or dead phytoplankton cells and excreted algal organic matter (AOM) impact Hg(II) methylation by several known methylators, including iron-reducing bacteria (FeRB), Geobacter anodireducens SD-1 and Geobacter sulfurreducens PCA, and the sulfate-reducing bacterium (SRB) Desulfovibrio desulfuricans ND132 (or Pseudodesulfovibrio mercurii). Here our results indicate that, among the 4 phytoplankton species studied, none were capable of methylating Hg(II). However, the presence of phytoplankton cells (either live or dead) from Chlorella vulgaris (CV) generally inhibited Hg(II) methylation by FeRB but substantially enhanced methylation by SRB D. desulfuricans ND132. Enhanced methylation was attributed in part to CV-excreted AOM, which increased Hg(II) complexation and methylation by ND132 cells. In contrast, inhibition of methylation by FeRB was attributed to these bacteria incapable of competing with phytoplankton for Hg(II) binding and uptake. These observations suggest that phytoplankton could play different roles in affecting Hg(II) methylation by the two groups of anaerobic bacteria, FeRB and SRB, and thus shed additional light on how phytoplankton blooms may modulate MeHg production and bioaccumulation in the aquatic environment.
Roundup causes embryonic development failure and alters metabolic pathways and gut microbiota functionality in non-target species
Background: Research around the weedkiller Roundup is among the most contentious of the twenty-first century. Scientists have provided inconclusive evidence that the weedkiller causes cancer and other life-threatening diseases, while industry-paid research reports that the weedkiller has no adverse effect on humans or animals. Much of the controversial evidence on Roundup is rooted in the approach used to determine safe use of chemicals, defined by outdated toxicity tests. We apply a system biology approach to the biomedical and ecological model species Daphnia to quantify the impact of glyphosate and of its commercial formula, Roundup, on fitness, genome-wide transcription and gut microbiota, taking full advantage of clonal reproduction in Daphnia. We then apply machine learning-based statistical analysis to identify and prioritize correlations between genome-wide transcriptional and microbiota changes. Results: We demonstrate that chronic exposure to ecologically relevant concentrations of glyphosate and Roundup at the approved regulatory threshold for drinking water in the US induce embryonic developmental failure, induce significant DNA damage (genotoxicity), and interfere with signaling. Furthermore, chronic exposure to the weedkiller alters the gut microbiota functionality and composition interfering with carbon and fat metabolism, as well as homeostasis. Using the “Reactome,” we identify conserved pathways across the Tree of Life, which are potential targets for Roundup in other species, including liver metabolism, inflammation pathways, and collagen degradation, responsible for the repair of wounds and tissue remodeling. Conclusions: Our results show that chronic exposure to concentrations of Roundup and glyphosate at the approved regulatory threshold for drinking water causes embryonic development failure and alteration of key metabolic functions via direct effect on the host molecular processes and indirect effect on the gut microbiota. The ecological model species Daphnia occupies a central position in the food web of aquatic ecosystems, being the preferred food of small vertebrates and invertebrates as well as a grazer of algae and bacteria. The impact of the weedkiller on this keystone species has cascading effects on aquatic food webs, affecting their ability to deliver critical ecosystem services.