Predator-prey dynamics driven by feedback between functionally diverse trophic levels

Neglecting the naturally existing functional diversity of communities and the resulting potential to respond to altered conditions may strongly reduce the realism and predictive power of ecological models. We therefore propose and study a predator-prey model that describes mutual feedback via species shifts in both predator and prey, using a dynamic trait approach. Species compositions of the two trophic levels were described by mean functional traits--prey edibility and predator food-selectivity--and functional diversities by the variances. Altered edibility triggered shifts in food-selectivity so that consumers continuously respond to the present prey composition, and vice versa. This trait-mediated feedback mechanism resulted in a complex dynamic behavior with ongoing oscillations in the mean trait values, reflecting continuous reorganization of the trophic levels. The feedback was only possible if sufficient functional diversity was present in both trophic levels. Functional diversity was internally maintained on the prey level as no niche existed in our system, which was ideal under any composition of the predator level due to the trade-offs between edibility, growth and carrying capacity. The predators were only subject to one trade-off between food-selectivity and grazing ability and in the absence of immigration, one predator type became abundant, i.e., functional diversity declined to zero. In the lack of functional diversity the system showed the same dynamics as conventional models of predator-prey interactions ignoring the potential for shifts in species composition. This way, our study identified the crucial role of trade-offs and their shape in physiological and ecological traits for preserving diversity.     

Predator–prey interactions in anurans of the tropical dry forests of the Colombian Caribbean: A functional approach

Anuran–prey selection might be mediated by traits, either by mismatches in predator and prey traits (preventing interactions) or by predator selection of prey traits (encouraging interactions). These effect traits could be summarized in two contrasting foraging strategies: “active” and “sit-and-wait” foragers. We evaluated whether anurans could be classified into groups of species sharing traits associated with their diet, and what is the relation between particular effect traits of anurans and their prey. We collected anurans and identified their stomach contents once during dry, minor, and major rain seasons in six dry forest sites in the Colombian Caribbean. For each of the 19 anuran species and 436 prey items, we registered six effect traits. We applied RLQ and fourth-corner methodologies to relate predator and prey traits through their interaction matrix. Predators were assigned to five groups according to their differences in locomotion, body shape, proportion of the jaw width, mode of tongue protrusion, and strata preferred. Regarding preys, species were assigned to four groups according to their gregariousness, body shape and hardness, defensive traits, and mobility. Body size of both, predators and prey, had a minor contribution in the group assignment. We found that predators using active search target low-mobility preys, whereas species using sit-and-wait strategy target highly nutritive prey that are difficult to manipulate. By linking amphibian diet with foraging strategies, we hope to contribute to the understanding of mechanisms behind anuran–prey food web patterns and to build more realistic models of functional response to changing environments.     

The evolution of traits affecting resource acquisition and predator vulnerability: character displacement under real and apparent competition

This article investigates some simple models of the evolutionary interaction between two prey species that share a common resource and a common predator. Each prey species is characterized by a trait that determines both the rate of resource capture and vulnerability to a predator. In a simple model of a three-species food chain, such traits usually increase in response to an imposed reduction in resource density. When the per capita growth rates of each of two prey species depend linearly on resource density, such traits will change in opposite directions when the two prey come into sympatry. In addition, the ratio of the effect of the predator on prey fitness to the effect of the resource on prey fitness will diverge from the corresponding ratio in a second prey species when those species coexist in sympatry. These simple predictions need not hold under several alternative assumptions, which may be more common in biological systems. Parallel changes in sympatry may occur if the relationship between resource consumption and prey growth is nonlinear, if the prey species have partial overlap in the set of resources used or in the set of predators that consume them, or if prey experience direct intraspecific competition. The responses to a second prey can also differ significantly from those predicted by the simplest model if separate traits affect vulnerability to predators and resource acquisition rate. It is important to determine whether examples of character displacement previously interpreted as responses to competition for resources might also reflect responses to altered predation risks in sympatry.     

Seasonal shifts in predator body size diversity and trophic interactions in size-structured predator-prey systems

1.?Theory suggests that the relationship between predator diversity and prey suppression should depend on variation in predator traits such as body size, which strongly influences the type and strength of species interactions. Prey species often face a range of different sized predators, and the composition of body sizes of predators can vary between communities and within communities across seasons. 2.?Here, I test how variation in size structure of predator communities influences prey survival using seasonal changes in the size structure of a cannibalistic population as a model system. Laboratory and field experiments showed that although the per-capita consumption rates increased at higher predator-prey size ratios, mortality rates did not consistently increase with average size of cannibalistic predators. Instead, prey mortality peaked at the highest level of predator body size diversity. 3.?Furthermore, observed prey mortality was significantly higher than predictions from the null model that assumed no indirect interactions between predator size classes, indicating that different sized predators were not substitutable but had more than additive effects. Higher predator body size diversity therefore increased prey mortality, despite the increased potential for behavioural interference and predation among predators demonstrated in additional laboratory experiments. 4.?Thus, seasonal changes in the distribution of predator body sizes altered the strength of prey suppression not only through changes in mean predator size but also through changes in the size distribution of predators. In general, this indicates that variation (i.e. diversity) within a single trait, body size, can influence the strength of trophic interactions and emphasizes the importance of seasonal shifts in size structure of natural food webs for community dynamics.     

A trait‐based approach reveals the feeding selectivity of a small endangered Mediterranean fish

Functional traits are growing in popularity in modern ecology, but feeding studies remain primarily rooted in a taxonomic‐based perspective. However, consumers do not have any reason to select their prey using a taxonomic criterion, and prey assemblages are variable in space and time, which makes taxon‐based studies assemblage‐specific. To illustrate the benefits of the trait‐based approach to assessing food choice, we studied the feeding ecology of the endangered freshwater fish Barbus meridionalis. We hypothesized that B. meridionalis is a selective predator which food choice depends on several prey morphological and behavioral traits, and thus, its top‐down pressure may lead to changes in the functional composition of in‐stream macroinvertebrate communities. Feeding selectivity was inferred by comparing taxonomic and functional composition (13 traits) between ingested and free‐living potential prey using the Jacob's electivity index. Our results showed that the fish diet was influenced by 10 of the 13 traits tested. Barbus meridionalis preferred prey with a potential size of 5–10 mm, with a medium–high drift tendency, and that drift during daylight. Potential prey with no body flexibility, conical shape, concealment traits (presence of nets and/or cases, or patterned coloration), and high aggregation tendency had a low predation risk. Similarly, surface swimmers and interstitial taxa were low vulnerable to predation. Feeding selectivity altered the functional composition of the macroinvertebrate communities. Fish absence favored taxa with weak aggregation tendency, weak flexibility, and a relatively large size (10–20 mm of potential size). Besides, predatory invertebrates may increase in fish absence. In conclusion, our study shows that the incorporation of the trait‐based approach in diet studies is a promising avenue to improve our mechanistic understanding of predator–prey interactions and to help predict the ecological outcomes of predator invasions and extinctions.     

Field evidence of trait-mediated indirect interactions in a rocky intertidal food web

Studies on the implications of food web interactions to community structure have often focused on density-mediated interactions between predators and their prey. This approach emphasizes the importance of predator regulation of prey density via consumption (i.e. lethal effects), which, in turn, leads to cascading effects on the prey's resources. A more recent and contrasting view emphasizes the importance of non-lethal predator effects on prey traits (e.g. behaviour, morphology), or trait-mediated interactions. On rocky intertidal shores in New England, green crab ( Carcinus maenas ) predation is thought to be important to patterns of algal abundance and diversity by regulating the density of herbivorous snails ( Littorina littorea ). We found, however, that risk cues from green crabs can dramatically suppress snail grazing, with large effects on fucoid algal communities. Our results suggest that predator-induced changes in prey behaviour may be an important and under-appreciated component of food web interactions and community dynamics on rocky intertidal shores.     

The paradox of enrichment in an adaptive world

Paradoxically, enrichment can destabilize a predator-prey food web. While adaptive dynamics can greatly influence the stability of interaction systems, few theoretical studies have examined the effect of the adaptive dynamics of interaction-related traits on the possibility of resolution of the paradox of enrichment. We consider the evolution of attack and defence traits of a predator and two prey species in a one predator-two prey system in which the predator practises optimal diet use. The results showed that optimal foraging alone cannot eliminate a pattern of destabilization with enrichment, but trait evolution of the predator or prey can change the pattern to one of stabilization, implying a possible resolution of the paradox of enrichment. Furthermore, trait evolution in all species can broaden the parameter range of stabilization. Importantly, rapid evolution can stabilize this system, but weaken its stability in the face of enrichment.     

Eco-evolutionary trophic dynamics: loss of top predators drives trophic evolution and ecology of prey

Ecosystems are being altered on a global scale by the extirpation of top predators. The ecological effects of predator removal have been investigated widely; however, predator removal can also change natural selection acting on prey, resulting in contemporary evolution. Here we tested the role of predator removal on the contemporary evolution of trophic traits in prey. We utilized a historical introduction experiment where Trinidadian guppies (Poecilia reticulata) were relocated from a site with predatory fishes to a site lacking predators. To assess the trophic consequences of predator release, we linked individual morphology (cranial, jaw, and body) to foraging performance. Our results show that predator release caused an increase in guppy density and a "sharpening" of guppy trophic traits, which enhanced food consumption rates. Predator release appears to have shifted natural selection away from predator escape ability and towards resource acquisition ability. Related diet and mesocosm studies suggest that this shift enhances the impact of guppies on lower trophic levels in a fashion nuanced by the omnivorous feeding ecology of the species. We conclude that extirpation of top predators may commonly select for enhanced feeding performance in prey, with important cascading consequences for communities and ecosystems.     

Optimizing time and resource allocation trade-offs for investment into morphological and behavioral defense

Prey organisms are confronted with time and resource allocation trade-offs. Time allocation trade-offs partition time, for example, between foraging effort to acquire resources and behavioral defense. Resource allocation trade-offs partition the acquired resources between multiple traits, such as growth or morphological defense. We develop a mathematical model for prey organisms that comprise time and resource allocation trade-offs for multiple defense traits. Fitness is determined by growth and survival during ontogeny. We determine optimal defense strategies for environments that differ in their resource abundance, predation risk, and defense effectiveness. We compare the results with results of simplified models where single defense traits are optimized. Our results indicate that selection acts in favor of integrated traits. The selective advantage of expressing multiple defense traits is most pronounced at intermediate environmental conditions. Optimizing single traits generally leads to a more pronounced response of the defense traits, which implies that studying single traits leads to an overestimation of their response to predation. Behavioral defense and morphological defense compensate for and augment each other depending on predator densities and the effectiveness of the defense mechanisms. In the presence of time constraints, the model shows peak investment into morphological and behavioral defense at intermediate resource levels.     

Intraguild interactions among generalist predator functional groups drive impact on herbivore and decomposer prey

Different functional groups of generalist predators may complement each other in controlling prey populations; but intraguild interactions, common among generalist predators, may also reduce the strength of top–down control. In natural communities greater alterations to ecosystem function are expected if a whole functional group declines in abundance or is lost. Therefore studying functional group diversity is important for predicting effects of predator loss. We studied the top–down impact of web‐building spiders, hunting spiders and ants, which are highly abundant generalist predators in most terrestrial ecosystems, on prey from the herbivore and decomposer system of a grassland food web. The density of the three predator groups was manipulated by continuous removal in a three‐factorial designed field experiment, which was carried out for two years. We found no positive effect of increasing predator functional group richness on prey control. However there was evidence for strong composition effects between the functional groups. The presence of ants in predator assemblages reduced the prey suppression through mostly trait‐mediated intraguild interactions, while hunting and web‐building spiders contributed additively to prey suppression and reduced the density of herbivore and decomposer prey by 50–60%. A trophic cascade on plant biomass triggered by web‐builders and hunting spiders was diminished at levels of higher predator group diversity. In conclusion, our experiments showed that intraguild interactions strongly influence the strength of top–down control by generalist predators. Among spiders there was evidence for a positive relation between functional group richness and prey suppression but the overall outcome strongly depended on the occurrence of interference, driven by trait‐mediated indirect interactions.     

A trait-based approach for modelling microbial litter decomposition

Trait-based models are an emerging tool in ecology with the potential to link community dynamics, environmental responses and ecosystem processes. These models represent complex communities by defining taxa with trait combinations derived from prior distributions that may be constrained by trade-offs. Herein I develop a model that links microbial community composition with physiological and enzymatic traits to predict litter decomposition rates. This approach allows for trade-offs among traits that represent alternative microbial strategies for resource acquisition. The model predicts that optimal strategies depend on the level of enzyme production in the whole community, which determines resource availability and decomposition rates. There is also evidence for facilitation and competition among microbial taxa that co-occur on decomposing litter. These interactions vary with community investment in extracellular enzyme production and the magnitude of trade-offs affecting enzyme biochemical traits. The model accounted for 69% of the variation in decomposition rates of 15 Hawaiian litter types and up to 26% of the variation in enzyme activities. By explicitly representing diversity, trait-based models can predict ecosystem processes based on functional trait distributions in a community. The model developed herein illustrates that traits influencing microbial enzyme production are some of the key controls on litter decomposition rates.     

Quantifying predator dependence in the functional response of generalist predators

A long‐standing debate concerns how functional responses are best described. Theory suggests that ratio dependence is consistent with many food web patterns left unexplained by the simplest prey‐dependent models. However, for logistical reasons, ratio dependence and predator dependence more generally have seen infrequent empirical evaluation and then only so in specialist predators, which are rare in nature. Here we develop an approach to simultaneously estimate the prey‐specific attack rates and predator‐specific interference (facilitation) rates of predators interacting with arbitrary numbers of prey and predator species in the field. We apply the approach to surveys and experiments involving two intertidal whelks and their full suite of potential prey. Our study provides strong evidence for predator dependence that is poorly described by the ratio dependent model over manipulated and natural ranges of species abundances. It also indicates how, for generalist predators, even the qualitative nature of predator dependence can be prey‐specific.     

Seasonal Trophic Niche Shift and Cascading Effect of a Generalist Predator Fish

Few studies have examined how foraging niche shift of a predator over time cascade down to local prey communities. Here we examine patterns of temporal foraging niche shifts of a generalist predator (yellow catfish, Pelteobagrus fulvidraco) and the abundance of prey communities in a subtropical lake. We predicted that the nature of these interactions would have implications for patterns in diet shifts and growth of the predator. Our results show significant decreases in planktivory and benthivory from late spring to summer and autumn, whereas piscivory increased significantly from mid-summer until late autumn and also increased steadily with predator body length. The temporal dynamics in predator/prey ratios indicate that the predation pressure on zooplankton and zoobenthos decreased when the predation pressure on the prey fish and shrimps was high. Yellow catfish adjusted their foraging strategies to temporal changes in food availability, which is in agreement with optimal foraging theory. Meanwhile the decrease in planktivory and benthivory of yellow catfish enabled primary consumers, such as zooplankton and benthic invertebrates, to develop under low grazing pressure via trophic cascading effects in the local food web. Thus, yellow catfish shifts its foraging niche to intermediate consumers in the food web to benefit the energetic demand on growth and reproduction during summer, which in turn indirectly facilitate the primary consumers. In complex food webs, trophic interactions are usually expected to reduce the strength and penetrance of trophic cascades. However, our study demonstrates strong associations between foraging niche of piscivorous fish and abundance of prey. This relationship appeared to be an important factor in producing top-down effects on both benthic and planktonic food webs.     

Matching consumer feeding behaviours and resource traits: a fourth‐corner problem in food‐web theory

For decades, food web theory has proposed phenomenological models for the underlying structure of ecological networks. Generally, these models rely on latent niche variables that match the feeding behaviour of consumers with their resource traits. In this paper, we used a comprehensive database to evaluate different hypotheses on the best dependency structure of trait‐matching patterns between consumers and resource traits. We found that consumer feeding behaviours had complex interactions with resource traits; however, few dimensions (i.e. latent variables) could reproduce the trait‐matching patterns. We discuss our findings in the light of three food web models designed to reproduce the multidimensionality of food web data; additionally, we discuss how using species traits clarify food webs beyond species pairwise interactions and enable studies to infer ecological generality at larger scales, despite potential taxonomic differences, variations in ecological conditions and differences in species abundance between communities.     

Herbivore functional traits and macroinvertebrate food webs have different responses to leaf chemical compounds of two macrophyte species in a tropical lake’s littoral zone

This research addressed the question of whether invertebrate food web structure varied between a native and an invasive macrophyte leaf species in the littoral zone of a tropical reservoir. We compared macroinvertebrate herbivore functional trait diversity composition with food web structure on the two macrophyte leaves, the invasive white ginger lily (Hedichium coronarium—Zingiberaceae) and the native pickerelweed (Pontederia cordata—Pontederiaceae). We predicted that the herbivore macroinvertebrate trait indices would decrease with macrophyte leaf species due to a lower resource quality with the flow-on effects in the food web structure. We calculated the number of functionally singular species (sing.sp) and herbivore functional trait richness (FRic) indices. For the macroinvertebrate food webs, we calculated the total number of trophic links (L), link density (L/S), connectance (C) and predator–prey ratios using a predator–prey matrix. We analysed the relationship between chemical traits of the macrophyte species’ leaves herbivore traits and food web indices using multivariate regression and Pearson’s correlation. Hedichium coronarium leaves had higher biomass and higher nitrogen content than the native P. cordata, which had higher phosphorus and carbohydrate content. Pontederia cordata leaves were associated with specialist macroinvertebrate species which primarily feed on biofilms (e.g. Ulmeritrus and Scirtidae) and plant leaves (e.g. Beardius). Food webs on P. cordata had lower numbers of trophic links (L), links per species (L/S) and predator–prey ratios. Connectance, which represents food web complexity, was similar between macroinvertebrate assemblages on the two leaf types. Our study suggests that chemical compounds of macrophyte leaves quality may have potential flow-on effects on food web structure.     

Omnivory and stability of food webs

The role and prevalence of omnivory, defined as feeding on more than one trophic level, are critical to understand food web structure and dynamics. Whether omnivory stabilizes or destabilizes food webs depends on the assumptions of theoretical models. Recently, Tanabe and Namba [Tanabe, K., Namba, T., 2005. Omivory creates chaos in simple food web models. Ecology 86, 3411–3414] found that omnivory can create chaos in a simple food web model with linear functional responses and 12 model parameters. In this paper, first we numerically examined bifurcation diagrams with all the parameters as bifurcation parameters, including self-limitation of the intermediate consumer and predator. Chaos spontaneously appears when the intraguild predator’s consumption rates are low for nutrient-rich intraguild prey and high for nutrient-poor basal resource and the intraguild prey reproduces efficiently feeding on the basal resource. Second, we investigated effects of the addition of a species into the basic model food web which exhibits chaos. The additional species is assumed to consume only one of the basal resource, intermediate consumer, or omnivorous predator. Consequences of the addition greatly depend on the trophic level on which the additional species feeds. While the increased diversity of predators feeding on the intermediate consumer stabilizes the web, the increased diversity of prey feeding on the basal resource induces collapse of the food web through exploitative competition for the basal resource. The food chain with the top predator feeding on the omnivorous predator is highly unstable unless the mortality of the top predator is extremely low. We discuss the possibility of real-world chaos and the reason why stability of food webs strongly depends on the topological structure of the webs. Finally, we consider the implications of our results for food web theory and resource management.     

The Probabilistic Niche Model Reveals the Niche Structure and Role of Body Size in a Complex Food Web

The niche model has been widely used to model the structure of complex food webs, and yet the ecological meaning of the single niche dimension has not been explored. In the niche model, each species has three traits, niche position, diet position and feeding range. Here, a new probabilistic niche model, which allows the maximum likelihood set of trait values to be estimated for each species, is applied to the food web of the Benguela fishery. We also developed the allometric niche model, in which body size is used as the niche dimension. About 80% of the links in the empirical data are predicted by the probabilistic niche model, a significant improvement over recent models. As in the niche model, species are uniformly distributed on the niche axis. Feeding ranges are exponentially distributed, but diet positions are not uniformly distributed below the predator. Species traits are strongly correlated with body size, but the allometric niche model performs significantly worse than the probabilistic niche model. The best-fit parameter set provides a significantly better model of the structure of the Benguela food web than was previously available. The methodology allows the identification of a number of taxa that stand out as outliers either in the model''s poor performance at predicting their predators or prey or in their parameter values. While important, body size alone does not explain the structure of the one-dimensional niche.     

Evolutionary responses of foraging-related traits in unstable predator–prey systems

The evolutionary responses of predators to prey and of prey to predators are analysed using models for the dynamics of a quantitative trait that determines the capture rate of prey by an average searching predator. Unlike previous investigations, the analysis centres on models and/or parameter values for which the two-species equilibrium is locally unstable. The instability in some models is driven by the predators non-linear functional response to prey; in other models, the cycles are a direct consequence of evolutionary response to selection acting on the trait. When the values of predator and prey traits combine multiplicatively to determine the capture rate, the predators trait shows only a transient response to changes in the preys trait in stable systems. However, when the population densities exhibit sustained oscillations, predators often evolve an increased long-term mean capture rate in response to an increased prey escape ability. Under the multiplicative model, prey in stable systems always evolve increased escape ability in response to an increased predator capture a     

Predator diet breadth influences the relative importance of bottom-up and top-down control of prey biomass and diversity

We investigated the effects of predator diet breadth on the relative importance of bottom-up and top-down control of prey assemblages, using microbial food webs containing bacteria, bacterivorous protists and rotifers, and two different top predators. The experiment used a factorial design that independently manipulated productivity and the presence or absence of two top predators with different diet breadths. Predators included a "specialist" predatory ciliate Euplotes aediculatus, which was restricted to feeding on small prey, and a "generalist" predatory ciliate Stentor coeruleus, which could feed on the entire range of prey sizes. Both total prey biomass and prey diversity increased with productivity in the predator-free control and specialist predator treatments, a pattern consistent with bottom-up control, but both remained unchanged by productivity in the generalist predator treatment, a pattern consistent with top-down control. Linear food chain models adequately described responses in the generalist predator treatment, whereas food web models incorporating edible and inedible prey (which can coexist in the absence of predators) adequately described responses in the specialist predator treatment. These results suggest that predator diet breadth can play an important role in modulating the relative strength of bottom-up and top-down forces in ecological communities.     

Effect of scavenging on predation in a food web

Scavenging can have important consequences for food web dynamics, for example, it may support additional consumer species and affect predation on live prey. Still, few food web models include scavenging. We develop a dynamic model that includes two facultative scavenger species, which we refer to as the predator or scavenger species according to their natural scavenging propensity, as well as live prey, and a carrion pool to show ramifications of scavenging for predation in simple food webs. Our modeling suggests that the presence of scavengers can both increase and decrease predator kill rates and overall predation in model food webs and the impact varies (in magnitude and direction) with context. In particular, we explore the impact of the amount of dynamics (exploitative competition) allowed in the predator, scavenger, and prey populations as well as the direction and magnitude of interference competition between predators and scavengers. One fundamental prediction is that scavengers most likely increase predator kill rates, especially if there are exploitative feedback effects on the prey or carrion resources like is normally observed in natural systems. Scavengers only have minimal effects on predator kill rate when predator, scavenger, and prey abundances are kept constant by management. In such controlled systems, interference competition can greatly affect the interactions in contrast to more natural systems, with an increase in interference competition leading to a decrease in predator kill rate. Our study adds to studies that show that the presence of predators affects scavenger behavior, vital rates, and food web structure, by showing that scavengers impact predator kill rates through multiple mechanisms, and therefore indicating that scavenging and predation patterns are tightly intertwined. We provide a road map to the different theoretical outcomes and their support from different empirical studies on vertebrate guilds to provide guidance in wildlife management.