Ecological and evolutionary implications of food subsidies from humans

Human activities are the main current driver of global change. From hunter‐gatherers through to Neolithic societies–and particularly in contemporary industrialised countries–humans have (voluntarily or involuntarily) provided other animals with food, often with a high spatio‐temporal predictability. Nowadays, as much as 30–40% of all food produced in Earth is wasted. We argue here that predictable anthropogenic food subsidies (PAFS) provided historically by humans to animals has shaped many communities and ecosystems as we see them nowadays. PAFS improve individual fitness triggering population increases of opportunistic species, which may affect communities, food webs and ecosystems by altering processes such as competition, predator–prey interactions and nutrient transfer between biotopes and ecosystems. We also show that PAFS decrease temporal population variability, increase resilience of opportunistic species and reduce community diversity. Recent environmental policies, such as the regulation of dumps or the ban of fishing discards, constitute natural experiments that should improve our understanding of the role of food supply in a range of ecological and evolutionary processes at the ecosystem level. Comparison of subsidised and non‐subsidised ecosystems can help predict changes in diversity and the related ecosystem services that have suffered the impact of other global change agents.     

Prey Vulnerability Limits Top-Down Control and Alters Reciprocal Feedbacks in a Subsidized Model Food Web

Resource subsidies increase the productivity of recipient food webs and can affect ecosystem dynamics. Subsidies of prey often support elevated predator biomass which may intensify top-down control and reduce the flow of reciprocal subsidies into adjacent ecosystems. However, top-down control in subsidized food webs may be limited if primary consumers posses morphological or behavioral traits that limit vulnerability to predation. In forested streams, terrestrial prey support high predator biomass creating the potential for strong top-down control, however armored primary consumers often dominate the invertebrate assemblage. Using empirically based simulation models, we tested the response of stream food webs to variations in subsidy magnitude, prey vulnerability, and the presence of two top predators. While terrestrial prey inputs increased predator biomass (+12%), the presence of armored primary consumers inhibited top-down control, and diverted most aquatic energy (∼75%) into the riparian forest through aquatic insect emergence. Food webs without armored invertebrates experienced strong trophic cascades, resulting in higher algal (∼50%) and detrital (∼1600%) biomass, and reduced insect emergence (−90%). These results suggest prey vulnerability can mediate food web responses to subsidies, and that top-down control can be arrested even when predator-invulnerable consumers are uncommon (20%) regardless of the level of subsidy.     

A modified niche model for generating food webs with stage‐structured consumers: The stabilizing effects of life‐history stages on complex food webs

1. Almost all organisms grow in size during their lifetime and switch diets, trophic positions, and interacting partners as they grow. Such ontogenetic development introduces life‐history stages and flows of biomass between the stages through growth and reproduction. However, current research on complex food webs rarely considers life‐history stages. The few previously proposed methods do not take full advantage of the existing food web structural models that can produce realistic food web topologies.
2. We extended the niche model developed by Williams and Martinez (Nature, 2000, 404, 180–183) to generate food webs that included trophic species with a life‐history stage structure. Our method aggregated trophic species based on niche overlap to form a life‐history structured population; therefore, it largely preserved the topological structure of food webs generated by the niche model. We applied the theory of allometric predator–prey body mass ratio and parameterized an allometric bioenergetic model augmented with biomass flow between stages via growth and reproduction to study the effects of a stage structure on the stability of food webs.
3. When life‐history stages were linked via growth and reproduction, more food webs persisted, and persisting food webs tended to retain more trophic species. Topological differences between persisting linked and unlinked food webs were small to modest. The slopes of biomass spectra were lower, and weak interaction links were more prevalent in the linked food webs than the unlinked ones, suggesting that a life‐history stage structure promotes characteristics that can enhance stability of complex food webs.
4. Our results suggest a positive relationship between the complexity and stability of complex food webs. A life‐history stage structure in food webs may play important roles in dynamics of and diversity in food webs.

     

Predator diversity effects cascade across an ecosystem boundary

Food webs in different ecosystems are often connected through spatial resource subsidies. As a result, biodiversity effects in one ecosystem may cascade to adjacent ecosystems. I tested the hypothesis that aquatic predator diversity effects cascade to terrestrial food webs by altering a prey subsidy (biomass and trophic structure of emerging aquatic insects) entering terrestrial food webs, in turn altering the distribution of a terrestrial consumer (spider) that feeds on emerging aquatic insects. Fish presence, but not diversity, altered the trophic structure of emerging aquatic insects by strongly reducing the biomass of emerging predators (dragonflies) relative to non‐feeding taxa (chironomid midges). Fish diversity reduced emerging insect biomass through enhanced effects on the most common prey taxa: predatory dragonflies Pantala flavescens and non‐feeding chironomids. Terrestrial spiders (Tetragnathidae) primarily captured emerging chironomids, which were reduced in the high richness (3 spp.) treatment relative to the 1 and 2 species treatments. As a result, terrestrial spider abundance was lower above pools with high fish richness (3 species) than pools with 1 and 2 species. Synergistic predation effects were mostly limited to the high richness treatment, in which fish occupied each level of vertical microhabitat in the water‐column (benthic, middle, surface). This study demonstrates that predator diversity effects are not limited to the habitat of the predator, but can propagate to adjacent ecosystems, and demonstrates the utility of using simple predator functional traits (foraging domain) to more accurately predict the direction of predator diversity effects.     

Examining the potential effects of species aggregation on the network structure of food webs

One of the key measures that have been used to describe the topological properties of complex networks is the “degree distribution”, which is a measure that describes the frequency distribution of number of links per node. Food webs are complex ecological networks that describe the trophic relationships among species in a community, and the topological properties of empirical food webs, including degree distributions, have been examined previously. Previously, the “niche model” has been shown to accurately predict degree distributions of empirical food webs, however, the niche model-generated food webs were referenced against empirical food webs that had their species grouped together based on their taxonomic and/or trophic relationships (aggregated food webs). Here, we explore the effects of species aggregation on the ability of the niche model to predict the total- (sum of prey and predator links per node), in- (number of predator links per node), and out- (number of prey links per node) degree distributions of empirical food webs by examining two food webs that can be aggregated at different levels of resolution. The results showed that (1) the cumulative total- and out-degree distributions were consistent with the niche model predictions when the species were aggregated, (2) when the species were disaggregated (i.e., higher resolution), there were mixed conclusions with regards to the niche model's ability to predict total- and out-degree distributions, (3) the model's ability to predict the in-degree distributions of the two food webs was generally inadequate. Although it has been argued that universal functional form based on the niche model could describe the degree distribution patterns of empirical food webs, we believe there are some limitations to the model's ability to accurately predict the structural properties of food webs.     

Effects of trophic skewing of species richness on ecosystem functioning in a diverse marine community

Widespread overharvesting of top consumers of the world's ecosystems has "skewed" food webs, in terms of biomass and species richness, towards a generally greater domination at lower trophic levels. This skewing is exacerbated in locations where exotic species are predominantly low-trophic level consumers such as benthic macrophytes, detritivores, and filter feeders. However, in some systems where numerous exotic predators have been added, sometimes purposefully as in many freshwater systems, food webs are skewed in the opposite direction toward consumer dominance. Little is known about how such modifications to food web topology, e.g., changes in the ratio of predator to prey species richness, affect ecosystem functioning. We experimentally measured the effects of trophic skew on production in an estuarine food web by manipulating ratios of species richness across three trophic levels in experimental mesocosms. After 24 days, increasing macroalgal richness promoted both plant biomass and grazer abundance, although the positive effect on plant biomass disappeared in the presence of grazers. The strongest trophic cascade on the experimentally stocked macroalgae emerged in communities with a greater ratio of prey to predator richness (bottom-rich food webs), while stronger cascades on the accumulation of naturally colonizing algae (primarily microalgae with some early successional macroalgae that recruited and grew in the mesocosms) generally emerged in communities with greater predator to prey richness (the more top-rich food webs). These results suggest that trophic skewing of species richness and overall changes in food web topology can influence marine community structure and food web dynamics in complex ways, emphasizing the need for multitrophic approaches to understand the consequences of marine extinctions and invasions.     

Carnivory and resource-based niche differentiation in anuran larvae: implications for food web and experimental ecology

1.  Food webs represent the paths of material and energy flow through organisms in an ecosystem. Anuran larvae are important components of pond food webs: they are abundant, consume large quantities of food and serve as prey for many organisms. However, there are very basic uncertainties about the feeding ecology of anuran larvae; for instance, as to which trophic level they belong and whether species differ in resource use. Because anuran larvae have been employed in model systems in experimental ecology for decades, these uncertainties could lead to misinterpretation of published experiments, or inadequate designs of experiments directed at general, conceptual issues in ecology.
2.  Using ¹³C and ¹⁵N stable isotope and gut content analyses of free-ranging and enclosed tadpoles of four ranid species ( Lithobates sylvaticus , L. pipiens , L. clamitans , L. catesbeianus ) in the food webs of six wetlands, we tested the following null hypotheses: (i) that anuran larvae are strict primary consumers; (ii) that they are non-selective feeders and therefore exhibit little feeding niche differentiation; (iii) that they are opportunistic consumers and (iv) that their diet remains unchanged through ontogeny.
3.  All four species consumed and assimilated substantial amounts of animal food; bullfrog larvae, in particular, appear to be predatory. Significant feeding niche differentiation among species occurred with respect to the sources of carbon, consumption of animal matter and nutritional quality of food ingested. We further documented opportunistic feeding habits and ontogenetic shifts in diet.
4.  Collectively, these studies revealed complex trophic relationships that might require a reconsideration of the role of anuran larvae in pond food webs, as well as a reinterpretation of results of previous studies employing anuran larvae in model experimental systems.     

Rigorous conditions for food-web intervality in high-dimensional trophic niche spaces

Food webs represent trophic (feeding) interactions in ecosystems. Since the late 1970s, it has been recognized that food-webs have a surprisingly close relationship to interval graphs. One interpretation of food-web intervality is that trophic niche space is low-dimensional, meaning that the trophic character of a species can be expressed by a single or at most a few quantitative traits. In a companion paper we demonstrated, by simulating a minimal food-web model, that food webs are also expected to be interval when niche-space is high-dimensional. Here we characterize the fundamental mechanisms underlying this phenomenon by proving a set of rigorous conditions for food-web intervality in high-dimensional niche spaces. Our results apply to a large class of food-web models, including the special case previously studied numerically.     

Avian Community Responses to Variability in River Hydrology

River flow is a major driver of morphological structure and community dynamics in riverine-floodplain ecosystems. Flow influences in-stream communities through changes in water velocity, depth, temperature, turbidity and nutrient fluxes, and perturbations in the organisation of lower trophic levels are cascaded through the food web, resulting in shifts in food availability for consumer species. River birds are sensitive to spatial and phenological mismatches with aquatic prey following flow disturbances; however, the role of flow as a determinant of riparian ecological structure remains poorly known. This knowledge is crucial to help to predict if, and how, riparian communities will be influenced by climate-induced changes in river flow characterised by more extreme high (i.e. flood) and/or low (i.e. drought) flow events. Here, we combine national-scale datasets of river bird surveys and river flow archives to understand how hydrological disturbance has affected the distribution of riparian species at higher trophic levels. Data were analysed for 71 river locations using a Generalized Additive Model framework and a model averaging procedure. Species had complex but biologically interpretable associations with hydrological indices, with species’ responses consistent with their ecology, indicating that hydrological-disturbance has implications for higher trophic levels in riparian food webs. Our quantitative analysis of river flow-bird relationships demonstrates the potential vulnerability of riparian species to the impacts of changing flow variability and represents an important contribution in helping to understand how bird communities might respond to a climate change-induced increase in the intensity of floods and droughts. Moreover, the success in relating parameters of river flow variability to species’ distributions highlights the need to include river flow data in climate change impact models of species’ distributions.     

Delineating reef fish trophic guilds with global gut content data synthesis and phylogeny

Understanding species’ roles in food webs requires an accurate assessment of their trophic niche. However, it is challenging to delineate potential trophic interactions across an ecosystem, and a paucity of empirical information often leads to inconsistent definitions of trophic guilds based on expert opinion, especially when applied to hyperdiverse ecosystems. Using coral reef fishes as a model group, we show that experts disagree on the assignment of broad trophic guilds for more than 20% of species, which hampers comparability across studies. Here, we propose a quantitative, unbiased, and reproducible approach to define trophic guilds and apply recent advances in machine learning to predict probabilities of pairwise trophic interactions with high accuracy. We synthesize data from community-wide gut content analyses of tropical coral reef fishes worldwide, resulting in diet information from 13,961 individuals belonging to 615 reef fish. We then use network analysis to identify 8 trophic guilds and Bayesian phylogenetic modeling to show that trophic guilds can be predicted based on phylogeny and maximum body size. Finally, we use machine learning to test whether pairwise trophic interactions can be predicted with accuracy. Our models achieved a misclassification error of less than 5%, indicating that our approach results in a quantitative and reproducible trophic categorization scheme, as well as high-resolution probabilities of trophic interactions. By applying our framework to the most diverse vertebrate consumer group, we show that it can be applied to other organismal groups to advance reproducibility in trait-based ecology. Our work thus provides a viable approach to account for the complexity of predator–prey interactions in highly diverse ecosystems.

The diversity of life on our planet has produced a remarkable variety of biological traits that characterize different species, and such traits are widely considered an alternative to taxonomy to increase our understanding of biodiversity and ecosystem functioning. This study presents an unbiased and fully reproducible framework to delineate trophic guilds in reef fishes.     

Functional diversity buffers the effects of a pulse perturbation on the dynamics of tritrophic food webs

Biodiversity decline causes a loss of functional diversity, which threatens ecosystems through a dangerous feedback loop: This loss may hamper ecosystems’ ability to buffer environmental changes, leading to further biodiversity losses. In this context, the increasing frequency of human‐induced excessive loading of nutrients causes major problems in aquatic systems. Previous studies investigating how functional diversity influences the response of food webs to disturbances have mainly considered systems with at most two functionally diverse trophic levels. We investigated the effects of functional diversity on the robustness, that is, resistance, resilience, and elasticity, using a tritrophic—and thus more realistic—plankton food web model. We compared a non‐adaptive food chain with no diversity within the individual trophic levels to a more diverse food web with three adaptive trophic levels. The species fitness differences were balanced through trade‐offs between defense/growth rate for prey and selectivity/half‐saturation constant for predators. We showed that the resistance, resilience, and elasticity of tritrophic food webs decreased with larger perturbation sizes and depended on the state of the system when the perturbation occurred. Importantly, we found that a more diverse food web was generally more resistant and resilient but its elasticity was context‐dependent. Particularly, functional diversity reduced the probability of a regime shift toward a non‐desirable alternative state. The basal‐intermediate interaction consistently determined the robustness against a nutrient pulse despite the complex influence of the shape and type of the dynamical attractors. This relationship was strongly influenced by the diversity present and the third trophic level. Overall, using a food web model of realistic complexity, this study confirms the destructive potential of the positive feedback loop between biodiversity loss and robustness, by uncovering mechanisms leading to a decrease in resistance, resilience, and potentially elasticity as functional diversity declines.     

Effects of trophic similarity on community composition

Understanding how ecological processes determine patterns among species coexisting within ecosystems is central to ecology. Here, we explore relationships between species’ local coexistence and their trophic niches in terms of their feeding relationships both as consumers and as resources. We build on recent concepts and methods from community phylogenetics to develop a framework for analysing mechanisms responsible for community composition using trophic similarity among species and null models of community assembly. We apply this framework to 50 food webs found in 50 Adirondack lakes and find that species composition in these communities appears to be driven by both bottom‐up effects by which the presence of prey species selects for predators of those prey, and top‐down effects by which prey more tolerant of predation out‐compete less tolerant prey of the same predators. This approach to community food webs is broadly applicable and shows how species interaction networks can inform an increasingly large array of theory central to community ecology.     

Trophic cascades alter eco-evolutionary dynamics and body size evolution

Trait evolution in predator–prey systems can feed back to the dynamics of interacting species as well as cascade to impact the dynamics of indirectly linked species (eco-evolutionary trophic cascades; EETCs). A key mediator of trophic cascades is body mass, as it both strongly influences and evolves in response to predator–prey interactions. Here, we use Gillespie eco-evolutionary models to explore EETCs resulting from top predator loss and mediated by body mass evolution. Our four-trophic-level food chain model uses allometric scaling to link body mass to different functions (ecological pleiotropy) and is realistically parameterized from the FORAGE database to mimic the parameter space of a typical freshwater system. To track real-time changes in selective pressures, we also calculated fitness gradients for each trophic level. As predicted, top predator loss generated alternating shifts in abundance across trophic levels, and, depending on the nature and strength in changes to fitness gradients, also altered trajectories of body mass evolution. Although more distantly linked, changes in the abundance of top predators still affected the eco-evolutionary dynamics of the basal producers, in part because of their relatively short generation times. Overall, our results suggest that impacts on top predators can set off transient EETCs with the potential for widespread indirect impacts on food webs.     

The importance of omnivory and predator regulation of prey in freshwater fish assemblages of North America

Synopsis Food webs for 15 freshwater ecosystems in North America are reconstructed, based upon fish feeding habits in these ecosystems and established trophic categorizations for aquatic invertebrates. My own research in Goose Creek, Virginia, as well as literature data, provided the necessary information. One property of theoretical interest for food webs, namely omnivory, is examined, and the results are related to various topics more typically studied by freshwater fish ecologists, including predator-prey regulation, optimal foraging theory, and tropho-dynamics. The data indicate that omnivory is often important in freshwater ecosystems, such that fish may not always control the abundance of their prey. It is emphasized that knowledge of omnivory patterns can provide important insights into community structure and function in freshwater ecosystems.     

Sensory cues of a top‐predator indirectly control a reef fish mesopredator

Behavioural trophic cascades highlight the importance of indirect/risk effects in the maintenance of healthy trophic‐level links in complex ecosystems. However, there is limited understanding on how the loss of indirect top–down control can cascade through the food‐web to modify lower level predator–prey interactions. Using a reef fish food‐web, our study examines behavioural interactions among predators to assess how fear elicited by top‐predator cues (visual and chemical stimuli) can alter mesopredator behaviour and modify their interaction with resource prey. Under experimental conditions, the presence of any cue (visual, chemical, or both) from the top‐predator (coral trout Plectropomus leopardus) strongly restricted the distance swum, area explored and foraging activity of the mesopredator (dottyback Pseudochromis fuscus), while indirectly triggering a behavioural release of the resource prey (recruits of the damselfish Pomacentrus chrysurus). Interestingly, the presence of a large non‐predator species (thicklip wrasse Hemigymnus melapterus) also mediated the impact of the mesopredator on prey, as it provoked mesopredators to engage in an ‘inspection’ behaviour, while significantly reducing their feeding activity. Our study describes for the first time a three‐level behavioural cascade of coral reef fish and stresses the importance of indirect interactions in marine food‐webs.     

Highly resolved early Eocene food webs show development of modern trophic structure after the end-Cretaceous extinction

Generalities of food web structure have been identified for extant ecosystems. However, the trophic organization of ancient ecosystems is unresolved, as prior studies of fossil webs have been limited by low-resolution, high-uncertainty data. We compiled highly resolved, well-documented feeding interaction data for 700 taxa from the 48 million-year-old latest early Eocene Messel Shale, which contains a species assemblage that developed after an interval of protracted environmental and biotal change during and following the end-Cretaceous extinction. We compared the network structure of Messel lake and forest food webs to extant webs using analyses that account for scale dependence of structure with diversity and complexity. The Messel lake web, with 94 taxa, displays unambiguous similarities in structure to extant webs. While the Messel forest web, with 630 taxa, displays differences compared to extant webs, they appear to result from high diversity and resolution of insect–plant interactions, rather than substantive differences in structure. The evidence presented here suggests that modern trophic organization developed along with the modern Messel biota during an 18 Myr interval of dramatic post-extinction change. Our study also has methodological implications, as the Messel forest web analysis highlights limitations of current food web data and models.     

Regime shifts in exploited marine food webs: detecting mechanisms underlying alternative stable states using size-structured community dynamics theory

Many marine ecosystems have undergone ‘regime shifts’, i.e. abrupt reorganizations across trophic levels. Establishing whether these constitute shifts between alternative stable states is of key importance for the prospects of ecosystem recovery and for management. We show how mechanisms underlying alternative stable states caused by predator–prey interactions can be revealed in field data, using analyses guided by theory on size-structured community dynamics. This is done by combining data on individual performance (such as growth and fecundity) with information on population size and prey availability. We use Atlantic cod (Gadus morhua) and their prey in the Baltic Sea as an example to discuss and distinguish two types of mechanisms, ‘cultivation-depensation’ and ‘overcompensation’, that can cause alternative stable states preventing the recovery of overexploited piscivorous fish populations. Importantly, the type of mechanism can be inferred already from changes in the predators'' body growth in different life stages. Our approach can thus be readily applied to monitored stocks of piscivorous fish species, for which this information often can be assembled. Using this tool can help resolve the causes of catastrophic collapses in marine predatory–prey systems and guide fisheries managers on how to successfully restore collapsed piscivorous fish stocks.     

Overfishing and the Replacement of Demersal Finfish by Shellfish: An Example from the English Channel

The worldwide depletion of major fish stocks through intensive industrial fishing is thought to have profoundly altered the trophic structure of marine ecosystems. Here we assess changes in the trophic structure of the English Channel marine ecosystem using a 90-year time-series (1920–2010) of commercial fishery landings. Our analysis was based on estimates of the mean trophic level (mTL) of annual landings and the Fishing-in-Balance index (FiB). Food webs of the Channel ecosystem have been altered, as shown by a significant decline in the mTL of fishery landings whilst increases in the FiB index suggest increased fishing effort and fishery expansion. Large, high trophic level species (e.g. spurdog, cod, ling) have been increasingly replaced by smaller, low trophic level fish (e.g. small spotted catsharks) and invertebrates (e.g. scallops, crabs and lobster). Declining trophic levels in fisheries catches have occurred worldwide, with fish catches progressively being replaced by invertebrates. We argue that a network of fisheries closures would help rebalance the trophic status of the Channel and allow regeneration of marine ecosystems.     

Stable isotopes show food web changes after invasion by the predatory cladoceran <Emphasis Type="Italic">Cercopagis pengoi</Emphasis> in a Baltic Sea bay

Cercopagis pengoi, a recent invader to the Baltic Sea and the Laurentian Great Lakes, is a potential competitor with fish for zooplankton prey. We used stable C and N isotope ratios to elucidate trophic relationships between C. pengoi, zooplankton (microzooplankton, 90–200 m, mostly copepod nauplii and rotifers; mesozooplankton, >200 m, mostly copepods), and zooplanktivorous fish (herring, size range 5–15 cm and sprat, 9–11 cm) in a coastal area of the northern Baltic Sea. The isotope ratios in C. pengoi and fish were much higher than those of zooplankton, showing general trends of enrichment with trophic level. Young-of-the-year (YOY) herring had a significantly higher ¹⁵N/¹⁴N ratio than C. pengoi, suggesting of a trophic linkage between the two species. To evaluate the possible relative importance of different food sources for C. pengoi and YOY herring, two-source isotope-mixing models for N were used, with micro- and mesozooplankton as prey for C. pengoi and mesozooplankton and C. pengoi as prey for YOY herring. These models indicate that mesozooplankton was the major food source of both species. However, microzooplankton may be important prey for young stages of C. pengoi. Comparative analyses of the herring trophic position before and after the invasion by C. pengoi showed a trophic level shift from 2.6 to 3.4, indicating substantial alterations in the food web structure. Our findings contribute to a growing body of evidence, showing that C. pengoi can modify food webs and trophic interactions in invaded ecosystems.