The evolution of ecosystem processes: growth rate and elemental stoichiometry of a key herbivore in temperate and arctic habitats

Understanding the reciprocal interactions between the evolved characteristics of species and the environment in which each species is embedded is a major priority for evolutionary ecology. Here we use the perspective of ecological stoichiometry to test the hypothesis that natural selection on body growth rate affects consumer body stoichiometry. As body elemental composition (nitrogen, phosphorus) of consumers influences nutrient cycling and trophic dynamics in food webs, such differences should also affect biogeochemical processes and trophic dynamics. Consistent with the growth rate hypothesis, body growth rate and phosphorus content of individuals of the Daphnia pulex species complex were lower in Wisconsin compared to Alaska, where the brevity of the growing season places a premium on growth rate. Consistent with stoichiometric theory, we also show that, relative to animals sampled in Wisconsin, animals sampled in Alaska were poor recyclers of P and suffered greater declines in growth when fed low‐quality, P‐deficient food. These results highlight the importance of evolutionary context in establishing the reciprocal relationships between single species and ecosystem processes such as trophic dynamics and consumer‐driven nutrient recycling.     

A bioenergetic framework for the temperature dependence of trophic interactions

Changing temperature can substantially shift ecological communities by altering the strength and stability of trophic interactions. Because many ecological rates are constrained by temperature, new approaches are required to understand how simultaneous changes in multiple rates alter the relative performance of species and their trophic interactions. We develop an energetic approach to identify the relationship between biomass fluxes and standing biomass across trophic levels. Our approach links ecological rates and trophic dynamics to measure temperature‐dependent changes to the strength of trophic interactions and determine how these changes alter food web stability. It accomplishes this by using biomass as a common energetic currency and isolating three temperature‐dependent processes that are common to all consumer–resource interactions: biomass accumulation of the resource, resource consumption and consumer mortality. Using this framework, we clarify when and how temperature alters consumer to resource biomass ratios, equilibrium resilience, consumer variability, extinction risk and transient vs. equilibrium dynamics. Finally, we characterise key asymmetries in species responses to temperature that produce these distinct dynamic behaviours and identify when they are likely to emerge. Overall, our framework provides a mechanistic and more unified understanding of the temperature dependence of trophic dynamics in terms of ecological rates, biomass ratios and stability.     

Integrating ecosystem engineering and food webs

Ecosystem engineering, the physical modification of the environment by organisms, is a common and often influential process whose significance to food web structure and dynamics is largely unknown. In the light of recent calls to expand food web studies to include non‐trophic interactions, we explore how we might best integrate ecosystem engineering and food webs. We provide rationales justifying their integration and present a provisional framework identifying how ecosystem engineering can affect the nodes and links of food webs and overall organization; how trophic interactions with the engineer can affect the engineering; and how feedbacks between engineering and trophic interactions can affect food web structure and dynamics. We use a simple integrative food chain model to illustrate how feedbacks between the engineer and the food web can alter 1) engineering effects on food web dynamics, and 2) food web responses to extrinsic environmental perturbations. We identify four general challenges to integration that we argue can readily be met, and call for studies that can achieve this integration and help pave the way to a more general understanding of interaction webs in nature. Synthesis All species are affected by their physical environment. Because ecosystem engineering species modify the physical environment and belong to food webs, such species are potentially one of the most important bridges between the trophic and non‐trophic. We examine how to integrate the so far, largely independent research areas of ecosystem engineering and food webs. We present a conceptual framework for understanding how engineering can affect food webs and vice versa, and how feedbacks between the two alter ecosystem dynamics. With appropriate empirical studies and models, integration is achievable, paving the way to a more general understanding of interaction webs in nature.     

Interplay between the paradox of enrichment and nutrient cycling in food webs

Nutrient cycling is fundamental to ecosystem functioning. Despite recent major advances in the understanding of complex food web dynamics, food web models have so far generally ignored nutrient cycling. However, nutrient cycling is expected to strongly impact food web stability and functioning. To make up for this gap, we built an allometric and size structured food web model including nutrient cycling. By releasing mineral nutrients, recycling increases the availability of limiting resources for primary producers and links each trophic level to the bottom of food webs. We found that nutrient cycling can provide a significant part of the total nutrient supply of the food web, leading to a strong enrichment effect that promotes species persistence in nutrient poor ecosystems but leads to a paradox of enrichment at high nutrient inputs. The presence of recycling loops linking each trophic level to the basal resources weakly affects species biomass temporal variability in the food web. Recycling loops tend to slightly dampen the destabilising effect of nutrient enrichment on consumer temporal variability while they have opposite effects for primary producers. By considering nutrient cycling, this new model improves our understanding of the response of food webs to nutrient availability and opens perspectives to better link studies on food web dynamics and ecosystem functioning.     

Trophic interactions in the Zoige Alpine wetland on the eastern edge of the Qinghai–Tibetan Plateau inferred by stable isotopes

The Zoige wetland ecosystem of the eastern edge of the Qinghai–Tibetan Plateau is the largest plateau peat bog worldwide and an important biodiversity conservation centre in China. Nevertheless, limited information is available about this Alpine wetland aquatic ecosystem, including its food-web structure and complexity. In this study, we analysed the trophic interactions among dominant organisms in the food web of this Alpine wetland aquatic ecosystem and assessed the importance of allochthonous and autochthonous carbon sources during the wet season using δ¹³C and δ¹⁵N analysis. The results supported the hypothesis that the food web of the Zoige Alpine wetland is largely maintained by allochthonous carbon sources rather than autochthonous food sources during the wet season when the allochthonous resource availability is relatively high. The food web contains approximately three trophic levels, and Schizopygopsis pylzovi (a genus of cyprinid fish) is the top predator. Intermediate trophic positions, including zooplankton and macroinvertebrates, represent the primary animal community in the food web. The allochthonous carbon sources are transferred to the food web via these macroinvertebrates (e.g., Ecdyonurus sp. and Sigara substriata). Although our findings show a low biodiversity in the Zoige wetland during the wet season, the trophic redundancy in the food-web structure could support the stability of the Zoige Alpine wetland aquatic ecosystem.     

Fish diversity as a determinant of ecosystem properties across multiple trophic levels

Biodiversity has been established as a potential determinant of function in many ecosystems; however, previous research has mostly focused on primary producers and effects at a single trophic level. A broader perspective that considers multiple components of food webs is necessary to understand natural systems. In particular, consumer diversity needs to be more thoroughly examined as trophic interactions and indirect effects can alter ecosystem properties. We test the potential for consumer diversity (fish richness and composition) to govern food web dynamics at two levels of environmental complexity (mesocosms and experimental ponds) and explore the consequences of removing individual species of fish on lower trophic levels. In mesocosms, both the richness and density of zooplankton were reduced when more fish species were present. No effects from the fish treatments were found on phytoplankton, but phosphorus levels increased with higher fish richness. Removing either generalist or specialist fish species increased the richness and density of zooplankton and the amount of phytoplankton, whereas all fish species had redundant effects on nutrients. In ponds, a dominant fish species (specialist shiner) determined the richness and density of zooplankton. In contrast, phytoplankton and nutrients were reduced by higher fish richness in the fall and spring. Overall, the specialist shiner had unique effects on the pond food web suggesting the key to understanding function is the presence of a dominant species and their biological interactions. Differences between mesocosms and ponds are likely due to increased heterogeneity of resources in the ponds allowing species to specialize on different prey. Our study links the biodiversity ecosystem function paradigm with food web concepts to improve predictions for conservation and management actions in response to changes in biodiversity.     

Biodiversity, ecosystem functioning and food webs in fresh waters: assembling the jigsaw puzzle

1. Dramatic advances have been made recently in the study of biodiversity–ecosystem functioning (B-EF) relations and food web ecology. These fields are now starting to converge, and this fusion has the potential to improve our understanding of how environmental stressors modulate ecosystem processes and the supply of 'goods and services'.
2. Food web structure and dynamics can exert particularly strong influences on B-EF relations in fresh waters, as consumer–resource interactions (e.g. trophic cascades) are often more important than horizontal interactions within trophic levels. For instance, many freshwater food webs are size structured, with large organisms tending to occupy the higher trophic levels and often exerting powerful effects on ecosystem processes. However, because they are also vulnerable to perturbations, non-random losses of these large taxa can alter both food web structure and ecosystem functioning profoundly.
3. Recently, the focus of food web research has shifted away from exploring patterns, towards developing an understanding of processes (e.g. quantifying fluxes of individuals, biomass, energy, nutrients) and how the two interact. Many of the best-characterized food webs are from fresh waters, and these ecosystems are now being used to address some of the shortcomings of earlier B-EF studies. I have identified several key gaps in our current knowledge and highlighted potentially fruitful avenues of future B-EF and food web research.
4. A major challenge for this newly emerging research is to place it within a unified theoretical framework. The application of metabolic theory and ecological stoichiometry may help to achieve this goal by considering biological systems within the constraints imposed upon them by physical and chemical laws.     

Species richness and trophic diversity increase decomposition in a co-evolved food web

Ecological communities show great variation in species richness, composition and food web structure across similar and diverse ecosystems. Knowledge of how this biodiversity relates to ecosystem functioning is important for understanding the maintenance of diversity and the potential effects of species losses and gains on ecosystems. While research often focuses on how variation in species richness influences ecosystem processes, assessing species richness in a food web context can provide further insight into the relationship between diversity and ecosystem functioning and elucidate potential mechanisms underpinning this relationship. Here, we assessed how species richness and trophic diversity affect decomposition rates in a complete aquatic food web: the five trophic level web that occurs within water-filled leaves of the northern pitcher plant, Sarracenia purpurea. We identified a trophic cascade in which top-predators--larvae of the pitcher-plant mosquito--indirectly increased bacterial decomposition by preying on bactivorous protozoa. Our data also revealed a facultative relationship in which larvae of the pitcher-plant midge increased bacterial decomposition by shredding detritus. These important interactions occur only in food webs with high trophic diversity, which in turn only occur in food webs with high species richness. We show that species richness and trophic diversity underlie strong linkages between food web structure and dynamics that influence ecosystem functioning. The importance of trophic diversity and species interactions in determining how biodiversity relates to ecosystem functioning suggests that simply focusing on species richness does not give a complete picture as to how ecosystems may change with the loss or gain of species.     

Effects of extinction on food web structures on an evolutionary time scale

Extinction affected food web structure in paleoecosystems. Recent theoretical studies that examined the effects of extinction intensity on food web structure on ecological time scales have considered extinction to involve episodic events, with pre-extinction food webs becoming established without dynamics. However, in terms of the paleontological time scale, food web structures are generated from feedback with repeated extinctions, because extinction frequency is affected by food web structure, and food web structure itself is a product of previous extinctions. We constructed a simulation model of changes in tri-trophic-level food webs to examine how continual extinction events affect food webs on an evolutionary time scale. We showed that under high extinction intensity (1) species diversity, especially that of consumer species, decreased; (2) the total population density at each trophic level decreased, while the densities of individual species increased; and (3) the trophic link density of the food web increased. In contrast to previous models, our results were based on an assumption of long-term food web development and are able to explain overall trends posited by empirical investigations based on fossil records.     

Spatial stoichiometry: cross‐ecosystem material flows and their impact on recipient ecosystems and organisms

Cross‐ecosystem material flows, in the form of inorganic nutrients, detritus and organisms, spatially connect ecosystems and impact food web dynamics. To date research on material flows has focused on the impact of the quantity of these flows and largely ignored their elemental composition, or quality. However, the ratios of elements like carbon, nitrogen and phosphorus can influence the impact material flows have on food web interactions through stoichiometric mismatches between resources and consumers. The type and movement of materials likely vary in their ability to change stoichiometric constraints within the recipient ecosystem and materials may undergo changes in their own stoichiometry during transport. In this literature review we evaluate the importance of cross‐ecosystem material flows within the framework of ecological stoichiometry. We explore how movement in space and time impacts the stoichiometry of material flow, as these transformations are essential to consider when assessing the ability of these flows to impact food web productivity and ecosystem functioning. Our review suggests that stoichiometry of cross‐ecosystem material flows are highly dynamic and undergo changes during transport across the landscape or from human influence. These material flows can impact recipient organisms if they change stoichiometry of the abiotic medium, or provide resources that have a different stoichiometry to in situ resources. They might also alter consumer excretion rates, in turn altering the availability of nutrients in the recipient ecosystem. These alterations in stoichiometric constraints of recipient organisms can have cascading trophic effects and shape food web dynamics. We highlight significant gaps in the literature and suggest new avenues for research that explore how cross‐ecosystem material flows impact recipient ecosystems when considering differences in stoichiometric quality, their movement through the landscape and across ecosystem boundaries, and the nutritional constraints of the recipient organisms.     

Highly unsaturated fatty acids in nature: what we know and what we need to learn

The supply and demand of omega‐3 highly unsaturated fatty acids (ω‐3 HUFA) in natural ecosystems may lead to resource limitation in a diverse array of animal taxa. Here, we review why food quality in terms of ω‐3 HUFAs is important, particularly for neural tissue, across a diversity of animal taxa ranging from invertebrate zooplankton to vertebrates (including humans). Our review is focused on ω‐3 HUFAs rather than other unsaturated fatty acids because these compounds are especially important biochemically, but scarce in nature. We discuss the dichotomy between ω‐3 HUFA availability between aquatic primary producers, which are often rich in these compounds, and terrestrial primary producers, which are contain little to none of them. We describe the use of fatty acids as qualitative and quantitative tracers for reconstructing animal diets in natural ecosystems. Next, we discuss both direct and indirect ecological implications of ω‐3 HUFA limitation at the individual, population, food web, and ecosystem scales, which include: changes in behavior, species composition, secondary production rates, trophic transfer efficiency and cross‐ecosystem subsidies. We finish by highlighting future research priorities including a need for more research on ω‐3 HUFAs in terrestrial systems, more research their importance for higher order consumers, and more research on the food web and ecosystem‐scale effects of ω‐3 HUFA limitation. Synthesis Mismatches between the supply of and demand for omega‐3 highly unsaturated fatty acids (ω‐3 HUFA) in natural ecosystems have the potential to result in resource limitation across a diverse array of ecosystems. We combined perspectives from ecology and nutritional science to develop a unified synthesis of ω‐3 HUFA ecology. We reviewed the importance of ω‐3 HUFAs for animals, the striking differences in ω‐3 HUFA availability at the base of terrestrial versus aquatic food webs, and the implications of ω‐3 HUFA limitation for food webs. We finished by highlighting research priorities in the field including more research on ω‐3 HUFAs in terrestrial systems, on higher order consumers, and at the food web and ecosystem‐scales.     

Phylogeny versus body size as determinants of food web structure

Food webs are the complex networks of trophic interactions that stoke the metabolic fires of life. To understand what structures these interactions in natural communities, ecologists have developed simple models to capture their main architectural features. However, apparently realistic food webs can be generated by models invoking either predator-prey body-size hierarchies or evolutionary constraints as structuring mechanisms. As a result, this approach has not conclusively revealed which factors are the most important. Here we cut to the heart of this debate by directly comparing the influence of phylogeny and body size on food web architecture. Using data from 13 food webs compiled by direct observation, we confirm the importance of both factors. Nevertheless, phylogeny dominates in most networks. Moreover, path analysis reveals that the size-independent direct effect of phylogeny on trophic structure typically outweighs the indirect effect that could be captured by considering body size alone. Furthermore, the phylogenetic signal is asymmetric: closely related species overlap in their set of consumers far more than in their set of resources. This is at odds with several food web models, which take only the view-point of consumers when assigning interactions. The echo of evolutionary history clearly resonates through current food webs, with implications for our theoretical models and conservation priorities.     

Species traits as drivers of food web structure

The use of functional traits to describe community structure is a promising approach to reveal generalities across organisms and ecosystems. Plant ecologists have demonstrated the importance of traits in explaining community structure, competitive interactions as well as ecosystem functioning. The application of trait‐based methods to more complex communities such as food webs is however more challenging owing to the diversity of animal characteristics and of interactions. The objective of this study was to determine how functional structure is related to food web structure. We consider that food web structure is the result of 1) the match between consumer and resource traits, which determine the occurence of a trophic interaction between them, and 2) the distribution of functional traits in the community. We implemented a statistical approach to assess whether or not 35 466 pairwise interactions between soil organisms are constrained by trait‐matching and then used a Procrustes analysis to investigate correlations between functional indices and network properties across 48 sites. We found that the occurrence of trophic interactions is well predicted by matching the traits of the resource with those of the consumer. Taxonomy and body mass of both species were the most important traits for the determination of an interaction. As a consequence, functional evenness and the variance of certain traits in the community were correlated to trophic complementarity between species, while trait identity, more than diversity, was related to network topology. The analysis was however limited by trait data availability, and a coarse resolution of certain taxonomic groups in our dataset. These limitations explain the importance of taxonomy, as well as the complexity of the statistical model needed. Our results outline the important implications of trait composition on ecological networks, opening promising avenues of research into the relationship between functional diversity and ecosystem functioning in multi‐trophic systems.     

Thermal acclimation modulates the impacts of temperature and enrichment on trophic interaction strengths and population dynamics

Global change affects individual phenotypes and biotic interactions, which can have cascading effects up to the ecosystem level. However, the role of environmentally induced phenotypic plasticity in species interactions is poorly understood, leaving a substantial gap in our knowledge of the impacts of global change on ecosystems. Using a cladoceran–dragonfly system, we experimentally investigated the effects of thermal acclimation, acute temperature change and enrichment on predator functional response and metabolic rate. Using our experimental data, we next parameterized a population dynamics model to determine the consequences of these effects on trophic interaction strength and food‐chain stability. We found that (1) predation and metabolic rates of the dragonfly larvae increase with acute warming, (2) warm‐acclimated larvae have a higher maximum predation rate than cold‐acclimated ones, and (3) long‐term interaction strength increases with enrichment but decreases with both acclimation and acute temperatures. Overall, our experimental results show that thermal acclimation can buffer negative impacts of environmental change on predators and increase food‐web stability and persistence. We conclude that the effect of acclimation and, more generally, phenotypic plasticity on trophic interactions should not be overlooked if we aim to understand the effects of climate change and enrichment on species interaction strength and food‐web stability.     

Austral Summer Bloom of Loricate Choanoflagellates in the Central Ross Sea Polynya

A bloom of loricate choanoflagellates was recorded for the first time in the Ross Sea polynya during the austral summer 2017. Both individual cells and uncommon large‐size colonies (200 μm length) represent the 42–55% of the total plankton community (i.e. specimens from 5 to 150 μm length). Choanoflagellates serve as a link between low and mid trophic levels since they prey on bacteria and in turn are ingested by zooplankton. This twofold role and the unusual abundance recorded in the Antarctic ecosystem may have relevant but still unknown effects on food web structure and dynamics in that area.     

When is overkill optimal? Tritrophic interactions reveal new insights into venom evolution

Organisms embedded within food webs must balance arms races with their predators and prey. For venom users, venom may mediate each arms race, but the dynamical evolutionary changes in venom production in response to the two arms races are still poorly understood. Here, we use a simple model to evaluate the evolutionary response of a venomous consumer to the presence of an apex generalist predator and evolution of the consumer’s prey. We find that introduction of the apex predator can weaken the arms race between the two lower trophic levels. In addition, when consumer prey capture and predator defense venoms functionally overlap, a reduced evolutionary response in the prey population can drive investment in venom used for prey capture going beyond what is optimal for subduing prey. These dynamics suggest that interactions with multiple trophic levels can substantially alter the venom complexity in predatory venomous animals and may explain the paradox of the overkill hypothesis.     

Cascading effects of climate change on plankton community structure

Plankton communities account for at least half of global primary production and play a key role in the global carbon cycle. Warming and acidification may alter the interaction chains in these communities from the bottom and top of the food web. Yet, the relative importance of these potentially complex interactions has not yet been quantified. Here, we examine the isolated and combined effects of warming, acidification, and reductions in phytoplankton and predator abundances in a series of factorial experiments. We find that warming directly impacts the top of the food web, but that the intermediate trophic groups are more strongly influenced by indirect effects mediated by altered top‐down interactions. Direct manipulations of predator and phytoplankton abundance reveal similar strong top‐down interactions following top predator decline. A meta‐analysis of published experiments further supports the conclusion that warming has stronger direct impacts on the top and bottom of the food web rather than the intermediate trophic groups, with important differences between freshwater and marine plankton communities. Our results reveal that the trophic effect of warming cascading down from the top of the plankton food web is a powerful agent of global change.     

Trophic cascades in the bryosphere: the impact of global change factors on top‐down control of cyanobacterial N2‐fixation

Trophic cascades in which predators regulate densities of organisms at lower trophic levels are important drivers of population dynamics, but effects of trophic cascades on ecosystem‐level fluxes and processes, and the conditions under which top‐down control is important, remain unresolved. We manipulated the structure of a food web in boreal feather mosses and found that moss‐inhabiting microfauna exerted top‐down control of N₂‐fixation by moss‐associated cyanobacteria. However, the presence of higher trophic levels alleviated this top‐down control, likely through feeding on bacterivorous microfauna. These effects of food‐web structure on cyanobacterial N₂‐fixation were dependent on global change factors and strongly suppressed under N fertilisation. Our findings illustrate how food web interactions and trophic cascades can regulate N cycling in boreal ecosystems, where carbon uptake is generally strongly N‐limited, and shifting trophic control of N cycling under global change is therefore likely to impact ecosystem functioning.