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.     

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.     

Bioenergetic food webs as a means of linking toxicological effects across scales of ecological organization

Although significant progress has been made in ourability to predict population-level consequences oftoxic effects on individuals, extending thispredictive ability to communities, functional guilds,and ecosystems will require more integration ofecological theory into environmental science. Bioenergetics and food webs have long been centralthemes in ecology and greatly expanded ourunderstanding of nature. Although numerousenergetic-based toxicological endpoints have beendeveloped, few have extended this framework beyond theindividual level. Most energetic endpoints includeindividual growth, and only occasionally is thisintegrated with population dynamics. However,population-level energetic analyses (e.g., secondaryproduction) integrate individual and populationprocesses, and provide two key parameters: consumptionand energy flow. Within a food web framework,estimates of consumption and energy flow throughpopulations facilitate linking population-levelcontaminant effects to ecosystem-level effects. Several examples are given to illustrate the utilityof this approach.     

Autochthonous or allochthonous resources determine the characteristic population dynamics of ecosystem engineers and their impacts

Ecosystem engineering, or the modification of physical environments by organisms, can influence trophic interactions and thus food web dynamics. Although existing theory exclusively considers engineers using autochthonous resources, many empirical studies show that they often depend on allochthonous resources. By developing a simple mathematical model involving an ecosystem engineer that modifies the physical environment through its activities, its resource, and physical environment modified by the engineer, we compare the effects of autochthonous and allochthonous resources on the dynamics and stability of community with ecosystem engineers. To represent a variety of real situations, we consider engineers that alter either resource productivity, engineer feeding rate on the resource, or engineer mortality, and incorporate time-lagged responses of the physical environment. Our model shows that the effects of ecosystem engineering on community dynamics depend greatly on resource types. When the engineer consumes autochthonous resources, the community can exhibit oscillatory dynamics if the engineered environment affects engineer’s feeding rate or mortality. These cyclic behaviors are, however, stabilized by a slowly responding physical environment. When allochthonous resources are supplied as donor-controlled, on the other hand, the engineer population is unlikely to oscillate but instead can undergo unbounded growth if the engineered environment affects resource productivity or engineer mortality. This finding suggests that ecosystem engineers utilizing allochthonous resources may be more likely to reach high abundance and cause strong impacts on ecosystems. Our results highlight that community-based, compounding effects of trophic and physical biotic interactions of ecosystem engineers depend crucially on whether the engineers utilize autochthonous or allochthonous resources.     

Representing Variable Habitat Quality in a Spatial Food Web Model

Why are marine species where they are? The scientific community is faced with an urgent need to understand aquatic ecosystem dynamics in the context of global change. This requires development of scientific tools with the capability to predict how biodiversity, natural resources, and ecosystem services will change in response to stressors such as climate change and further expansion of fishing. Species distribution models and ecosystem models are two methodologies that are being developed to further this understanding. To date, these methodologies offer limited capabilities to work jointly to produce integrated assessments that take both food web dynamics and spatial-temporal environmental variability into account. We here present a new habitat capacity model as an implementation of the spatial-temporal model Ecospace of the Ecopath with Ecosim approach. The new model offers the ability to drive foraging capacity of species from the cumulative impacts of multiple physical, oceanographic, and environmental factors such as depth, bottom type, temperature, salinity, oxygen concentrations, and so on. We use a simulation modeling procedure to evaluate sampling characteristics of the new habitat capacity model. This development bridges the gap between envelope environmental models and classic ecosystem food web models, progressing toward the ability to predict changes in marine ecosystems under scenarios of global change and explicitly taking food web direct and indirect interactions into account.     

Stability of complex food webs: resilience, resistance and the average interaction strength

In the face of stochastic climatic perturbations, the overall stability of an ecosystem will be determined by the balance between its resilience and its resistance, but their relative importance is still unknown. Using aquatic food web models we study ecosystem stability as a function of food web complexity. We measured three dynamical stability properties: resilience, resistance, and variability. Specifically, we evaluate how a decrease in the strength of predator-prey interactions with food web complexity, reflecting a decrease in predation efficiency with the number of prey per predator, affects the overall stability of the ecosystem. We find that in mass conservative ecosystems, a lower interaction strength slows down the mass cycling rate in the system and this increases its resistance to perturbations of the growth rate of primary producers. Furthermore, we show that the overall stability of the food webs is mostly given by their resistance, and not by their resilience. Resilience and resistance display opposite trends, although they are shown not to be simply opposite concepts but rather independent properties. The ecological implication is that weaker predator-prey interactions in closed ecosystems can stabilize food web dynamics by increasing its resistance to climatic perturbations.     

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.     

Ecosystem effects of partial fish migration in lakes

Migration is a widespread phenomenon in many ecosystems. Most often, studies on migration have focused on how migration strategies are dependent on ecological parameters, but little attention has been paid to the top-down effect of migration on ecosystem processes. Cyprinid fish in many European lakes undergo partial migration, where a part of the population leaves the lake and enters streams for the winter. In this study, we model the effect of partial migration by fish on lower trophic levels in a lake ecosystem. Our results suggest that spring phyto- and zooplankton dynamics, including occurrences of clear-water phases, can be related to the timing and magnitude of partial migration of planktivorous fish. From our results we conclude that partial migration can influence the dynamics of lower trophic levels in the ecosystem. Furthermore, we hypothesize that partial migration may affect the stability of alternative stable states and transitions between them.     

Mainstem‐tributary linkages by mayfly migration help sustain salmonids in a warming river network

Animal migrations can link ecosystems across space. We discovered an aquatic insect that migrates between a river mainstem and its tributaries, and provides an important trophic subsidy for tributary predators. A mayfly, Ephemerella maculata, rears in a warm, sunlit productive river mainstem, then migrates as adults to cool, shaded unproductive tributaries where they oviposit and die. This migration tripled insect flux into a tributary for 1 month in summer. A manipulative field experiment showed that this E. maculata subsidy nearly tripled the growth of the young of the year steelhead trout (Oncorhynchus mykiss) in the recipient tributary over the summer months, and was more important than terrestrial invertebrate subsidies, which have been considered the primary food source for predators in small, forested creeks. By delivering food subsidies from productive but warming river mainstems to cool but food‐limited tributaries, aquatic insect migrations could enhance resilience to cool‐water predators in warming river networks.     

Bottom-up regulation of a pelagic community through spatial aggregations

The importance of spatial pattern in ecosystems has long been recognized. However, incorporating patchiness into our understanding of forces regulating ecosystems has proved challenging. We used a combination of continuously sampling moored sensors, complemented by shipboard sampling, to measure the temporal variation, abundance and vertical distribution of four trophic levels in Hawaii's near shore pelagic ecosystem. Using an analysis approach from trophic dynamics, we found that the frequency and intensity of spatial aggregations-rather than total biomass-in each step of a food chain involving phytoplankton, copepods, mesopelagic micronekton and spinner dolphins (Stenella longirostris) were the most significant predictors of variation in adjacent trophic levels. Patches of organisms had impacts disproportionate to the biomass of organisms within them. Our results are in accordance with resource limitation-mediated by patch dynamics-regulating structure at each trophic step in this ecosystem, as well as the foraging behaviour of the top predator. Because of their high degree of heterogeneity, ecosystem-level effects of patchiness such as this may be common in many pelagic marine systems.     

Predator shadows: complex life histories as generators of spatially patterned indirect interactions across ecosystems

Ecological coupling by material exchanges or dispersal between spatially distinct communities has important impacts on ecological processes, such as diversity–stability relationships, ecosystem function, and food web dynamics. One important mode of coupling between ecosystems occurs via organisms with complex life histories, which often switch between distinct ecosystems during their life cycle, and so can be channels of material exchanges between these ecosystems. Some organisms with complex life histories (e.g. frogs, dragonflies) can be abundant and effective predators during one or more life stages, and so provide conduits for strong direct and indirect interactions across ecosystem boundaries, linking the dynamics of discrete and often quite dissimilar community types. We present simple models and a case study (tailored to pond ecosystems), to explore how interactions within larval habitats can indirectly impact ecological interactions in adult habitats. Using our case study as a springboard, we propose that cohorts of predators emerging from natal habitats (e.g. ponds) cast 'predation shadows' on the surrounding adult (e.g. terrestrial) landscape. Trophic interactions within ponds, and the distribution of ponds on the landscape, can thus affect the spatial pattern in the strength of these predation shadows, creating strong spatial patterning in terrestrial trophic cascades. Our findings emphasize the importance of organisms with complex life histories as generators of strong links across ecosystem boundaries, and as potential sources of spatial variation in the strength and indirect impacts of interspecific interactions.     

Nutrient Subsidies from Iteroparous Fish Migrations Can Enhance Stream Productivity

Migratory animals often transfer nutrients between ecosystems, enhancing productivity in the subsidized system. Most research on nutrient subsidies by migratory fishes has focused on Pacific salmon, whose semelparous life history is unusual among migratory fishes. To test whether iteroparous species can provide ecologically important nutrient inputs to stream ecosystems, we experimentally blocked the migration of suckers (Catostomidae) midway up an oligotrophic tributary of Lake Michigan. Comparing reaches upstream of the barrier to downstream reaches containing thousands of breeding fish, we found that suckers elevated phosphorus and nitrogen concentrations three- to five-fold. Algal accrual was doubled and caddisflies grew 12% larger in subsidized reaches relative to reference reaches. An enclosure experiment demonstrated that caddisflies with access to a fish carcass rapidly became enriched in ¹⁵N and ¹³C, and experimental carcass additions were rapidly colonized by high densities of caddisflies. However, under natural conditions below the experimental barrier, caddisflies became enriched in ¹⁵N but not ¹³C, indicating that fish-derived nutrients entered the stream food web primarily through indirect pathways rather than direct consumption of carcasses or gametes. At pupation, an average of 18% of caddisfly tissue N below the barrier was sucker-derived. In comparison to our focal stream, a reference stream with few suckers showed no seasonal or longitudinal patterns in nutrients and stable isotopes. These results demonstrate that iteroparous fish migrations can spur productivity via nutrient subsidies, despite low mortality rates. Thus, concerns about negative ecosystem-level consequences of blocking migrations of semelparous fishes are also applicable to iteroparous species when migrations are large.     

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.     

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.     

Carrion cycling in food webs: comparisons among terrestrial and marine ecosystems

In light of current global changes to ecosystem function (e.g. climate change, trophic downgrading, and invasive species), there has been a recent surge of interest in exploring differences in nutrient cycling among ecosystem types. In particular, a growing awareness has emerged concerning the importance of scavenging in food web dynamics, although no studies have focused specifically on exploring differences in carrion consumption between aquatic and terrestrial ecosystems. In this forum we synthesize the scavenging literature to elucidate differences in scavenging dynamics between terrestrial and marine ecosystems, and identify areas where future research is needed to more clearly understand the role of carrion consumption in maintaining ecosystem function within each of these environments. Although scavenging plays a similar functional role in terrestrial and aquatic food webs, here we suggest that several fundamental differences exist in scavenging dynamics among these ecosystem types due to the unique selection pressures imposed by the physical properties of water and air. In particular, the movement of carcasses in marine ecosystems (e.g. wave action, upwelling, and sinking) diffuses biological activity associated with scavenging and decomposition across large, three‐dimensional spatial scales, creating a unique spatial disconnect between the processes of production, scavenging, and decomposition, which in contrast are tightly linked in terrestrial ecosystems. Moreover, the limited role of bacteria and temporal stability of environmental conditions on the sea floor appears to have facilitated the evolution of a much more diverse community of macrofauna that relies on carrion for a higher portion of its nutrient consumption than is present in terrestrial ecosystems. Our observations are further discussed as they pertain to the potential impacts of climate change and trophic downgrading (i.e. removal of apex consumers from ecosystems) on scavenging dynamics within marine and terrestrial ecosystems.     

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.     

Trophic-dynamic considerations in relating species diversity to ecosystem resilience

Complexity in the networks of interactions among and between the living and abiotic components forming ecosystems confounds the ability of ecologists to predict the economic consequences of perturbations such as species deletions in nature. Such uncertainty hampers prudent decision making about where and when to invest most intensively in species conservation programmes. Demystifying ecosystem responses to biodiversity alterations may be best achieved through the study of the interactions allowing biotic communities to compensate internally for population changes in terms of contributing to ecosystem function, or their intrinsic functional redundancy. Because individual organisms are the biologically discrete working components of ecosystems and because environmental changes are perceived at the scale of the individual, a mechanistic understanding of functional redundancy will hinge upon understanding how individuals' behaviours influence population dynamics in the complex community setting. Here, I use analytical and graphical modelling to construct a conceptual framework for predicting the conditions under which varying degrees of interspecific functional redundancy can be found in dynamic ecosystems. The framework is founded on principles related to food web successional theory, which provides some evolutionary insights for mechanistically linking functional roles of discrete, interacting organisms with the dynamics of ecosystems because energy is the currency both for ecological fitness and for food web commerce. Net productivity is considered the most contextually relevant ecosystem process variable because of its socioeconomic significance and because it ultimately subsumes all biological processes and interactions. Redundancy relative to productivity is suggested to manifest most directly as compensatory niche shifts among adaptive foragers in exploitation ecosystems, facilitating coexistence and enhancing ecosystem recovery after disturbances which alter species' relative abundances, such as extinctions. The framework further explicates how resource scarcity and environmental stochasticity may constitute 'ecosystem legacies' influencing the emergence of redundancy by shaping the background conditions for foraging behaviour evolution and, consequently, the prevalence of compensatory interactions. Because it generates experimentally testable predictions for a priori hypothesis testing about when and where varying degrees of functional redundancy are likely to be found in food webs, the framework may be useful for advancing toward the reliable knowledge of biodiversity and ecosystem function relations necessary for prudent prioritization of conservation programmes. The theory presented here introduces explanation of how increasing diversity can have a negative influence on ecosystem sustainability by altering the environment for biotic interactions and thereby changing functional compensability among biota--under particular conditions.     

A cascade of evolutionary change alters consumer-resource dynamics and ecosystem function

It is becoming increasingly clear that intraspecific evolutionary divergence influences the properties of populations, communities and ecosystems. The different ecological impacts of phenotypes and genotypes may alter selection on many species and promote a cascade of ecological and evolutionary change throughout the food web. Theory predicts that evolutionary interactions across trophic levels may contribute to hypothesized feedbacks between ecology and evolution. However, the importance of 'cascading evolutionary change' in a natural setting is unknown. In lakes in Connecticut, USA, variation in migratory behaviour and feeding morphology of a fish predator, the alewife (Alosa pseudoharengus), drives life-history evolution in a species of zooplankton prey (Daphnia ambigua). Here we evaluated the reciprocal impacts of Daphnia evolution on ecological processes in laboratory mesocosms. We show that life-history evolution in Daphnia facilitates divergence in rates of population growth, which in turn significantly alters consumer-resource dynamics and ecosystem function. These experimental results parallel trends observed in lakes. Such results argue that a cascade of evolutionary change, which has occurred over contemporary timescales, alters community and ecosystem processes.     

Analogous aquatic and terrestrial food webs in the high Arctic: The structuring force of a harsh climate

Understanding food web structure and dynamics remains a central theme in ecology. Whilst differences between aquatic and terrestrial food webs have been the focus of several studies, we aim to reveal similarities where abiotic conditions are particularly extreme such as in the high Arctic. We propose that here, the combination of a short growing season, low temperature and low light, leads to the absence of predator control and the development of typically two-trophic, grazer-dominated food webs with high plant quality in terms of elemental ratios. Moreover, we advocate that this mechanism is evident in both aquatic and terrestrial high-Arctic environments, allowing the build-up of herbivore densities that consume a large fraction of plant primary production and tightly recycle nutrients. Thus, the particular abiotic conditions that characterise the high Arctic give rise to a unique environment that allows biotic factors to orchestrate food web structure and influence ecosystem function. Specially, the short growing season, low temperatures and low light levels collectively constrain the accumulation of structural autotroph tissue that, in temperate regions, effectively keeps herbivores at bay. While fundamental differences between terrestrial and aquatic ecosystems have been frequently advocated, we show here that harsh live-constraining conditions in the high Arctic have led to analogous, grazer-dominated, food web dynamics in both terrestrial and freshwater ecosystems.     

Linking Water Quality and Quantity in Environmental Flow Assessment in Deteriorated Ecosystems: A Food Web View

Most rivers worldwide are highly regulated by anthropogenic activities through flow regulation and water pollution. Environmental flow regulation is used to reduce the effects of anthropogenic activities on aquatic ecosystems. Formulating flow alteration–ecological response relationships is a key factor in environmental flow assessment. Traditional environmental flow models are characterized by natural relationships between flow regimes and ecosystem factors. However, food webs are often altered from natural states, which disturb environmental flow assessment in such ecosystems. In ecosystems deteriorated by heavy anthropogenic activities, the effects of environmental flow regulation on species are difficult to assess with current modeling approaches. Environmental flow management compels the development of tools that link flow regimes and food webs in an ecosystem. Food web approaches are more suitable for the task because they are more adaptive for disordered multiple species in a food web deteriorated by anthropogenic activities. This paper presents a global method of environmental flow assessment in deteriorated aquatic ecosystems. Linkages between flow regimes and food web dynamics are modeled by incorporating multiple species into an ecosystem to explore ecosystem-based environmental flow management. The approach allows scientists and water resources managers to analyze environmental flows in deteriorated ecosystems in an ecosystem-based way.