Genetic variation, predator-prey interactions and food web structure

Food webs are networks of species that feed on each other. The role that within-population phenotypic and genetic variation plays in food web structure is largely unknown. Here, I show via simulation how variation in two key traits, growth rates and phenology, by influencing the variability of body sizes present through time, can potentially affect several structural parameters in the direction of enhancing food web persistence: increased connectance, decreased interaction strengths, increased variation among interaction strengths and increased degree of omnivory. I discuss other relevant traits whose variation could affect the structure of food webs, such as morphological and additional life-history traits, as well as animal personalities. Furthermore, trait variation could also contribute to the stability of food web modules through metacommunity dynamics. I propose future research to help establish a link between within-population variation and food web structure. If appropriately established, such a link could have important consequences for biological conservation, as it would imply that preserving (functional) genetic variation within populations could ensure the preservation of entire communities.     

Size-based predictions of food web patterns

We employ size-based theoretical arguments to derive simple analytic predictions of ecological patterns and properties of natural communities: size-spectrum exponent, maximum trophic level, and susceptibility to invasive species. The predictions are brought about by assuming that an infinite number of species are continuously distributed on a size–trait axis. It is, however, an open question whether such predictions are valid for a food web with a finite number of species embedded in a network structure. We address this question by comparing the size-based predictions to results from dynamic food web simulations with varying species richness. To this end, we develop a new size- and trait-based food web model that can be simplified into an analytically solvable size-based model. We confirm existing solutions for the size distribution and derive novel predictions for maximum trophic level and invasion resistance. Our results show that the predicted size-spectrum exponent is borne out in the simulated food webs even with few species, albeit with a systematic bias. The predicted maximum trophic level turns out to be an upper limit since simulated food webs may have a lower number of trophic levels, especially for low species richness, due to structural constraints. The size-based model possesses an evolutionary stable state and is therefore un-invadable. In contrast, the food web simulations show that all communities, irrespective of number of species, are equally open to invasions. We use these results to discuss the validity of size-based predictions in the light of the structural constraints imposed by food webs.     

Weaving animal temperament into food webs: implications for biodiversity

Recent studies into community level dynamics are revealing processes and patterns that underpin the biodiversity and complexity of natural ecosystems. Theoretical food webs have suggested that species‐rich and highly complex communities are inherently unstable, but incorporating certain characteristics of empirical communities, such as allometric body size scaling and non‐random interaction distributions, have been shown to enhance stability and facilitate species coexistence. Incorporating individual level traits and variability into food web theory is seen as a future pathway for this research and our growing knowledge of individual behaviours, in the form of temperament (or personality) traits, can inform the direction of this research. Temperament traits are consistent differences in behaviour between individuals, which are repeatable across time and/or across ecological contexts, such as aggressive or boldness behaviours that commonly differ between individuals of the same species. These traits, under the framework of behavioural reaction norms, show both individual consistency as well as contextual and phenotypic plasticity. This is likely to contribute significantly to the effects of individual trait variability and adaptive trophic behaviour on the structure and dynamics of food webs, which are apparently stabilizing. Exploring the role of temperament in the context of community ecology is a unique opportunity for cross‐pollination between ecological fields, and can provide new insights into community stability and biodiversity.     

Re-evaluating the omnivory–stability relationship in food webs

Under equilibrium conditions, previous theory has shown that the presence of omnivory destabilizes food webs. Correspondingly, omnivory ought to be rare in real food webs. Although, early food web data appeared to verify this, recently many ecologists have found omnivory to be ubiquitous in food web data gathered at a high taxonomic resolution. In this paper, we re-investigate the role of omnivory in food webs using a non-equilibrium perspective. We find that the addition of omnivory to a simple food chain model (thus a simple food web) locally stabilizes the food web in a very complete way. First, non-equilibrium dynamics (e.g. chaos) tend to be eliminated or bounded further away from zero via period-doubling reversals invoked by the omnivorous trophic link. Second, food chains without interior attractors tend to gain a stable interior attractor with moderate amounts of omnivory.     

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 dynamics of multispecies, multi-life-stage models of aquatic food webs

We investigated the dynamics of models of aquatic food webs using stability analysis methods previously applied to other types of food web models. Our models expanded traditional Lotka-Volterra models of predator-prey interactions in several ways. We added life history structure to these models in order to investigate its effects. Life history omnivory is different life history stages of a species feeding in trophically different positions in a food web. Such a species might appear omnivorous, integrating across all stages, but the individual stage might not be. Other important additions to the basic models included stock-recruitment relationships between adults and young and food-dependent maturation rates for early life history stages. Complex models of multispecies interactions were built from basic ones by adding new features sequentially. Our analysis revealed five major features of our multispecies, multi-life-stage models. Omnivory reduces stability, as it does in food web models without life history structure. However, life history omnivory reduces stability much less than single life stage omnivory does. Stock recruitment relationships affect the likelihood of finding stable models. If the maturation rate of young varies with their food supply, the chance of finding stable models decreases. Finally, predation loops of the type A eats B, B eats A, or A eats B, B eats C, C eats A greatly reduce model stability. We present both biological and mathematical explanations for these findings. We also discuss their implications for management of marine resources.     

Food Web Assembly Rules for Generalized Lotka-Volterra Equations

In food webs, many interacting species coexist despite the restrictions imposed by the competitive exclusion principle and apparent competition. For the generalized Lotka-Volterra equations, sustainable coexistence necessitates nonzero determinant of the interaction matrix. Here we show that this requirement is equivalent to demanding that each species be part of a non-overlapping pairing, which substantially constrains the food web structure. We demonstrate that a stable food web can always be obtained if a non-overlapping pairing exists. If it does not, the matrix rank can be used to quantify the lack of niches, corresponding to unpaired species. For the species richness at each trophic level, we derive the food web assembly rules, which specify sustainable combinations. In neighboring levels, these rules allow the higher level to avert competitive exclusion at the lower, thereby incorporating apparent competition. In agreement with data, the assembly rules predict high species numbers at intermediate levels and thinning at the top and bottom. Using comprehensive food web data, we demonstrate how omnivores or parasites with hosts at multiple trophic levels can loosen the constraints and help obtain coexistence in food webs. Hence, omnivory may be the glue that keeps communities intact even under extinction or ecological release of species.     

High‐resolution food webs based on nitrogen isotopic composition of amino acids

Food webs are known to have myriad trophic links between resource and consumer species. While herbivores have well‐understood trophic tendencies, the difficulties associated with characterizing the trophic positions of higher‐order consumers have remained a major problem in food web ecology. To better understand trophic linkages in food webs, analysis of the stable nitrogen isotopic composition of amino acids has been introduced as a potential means of providing accurate trophic position estimates. In the present study, we employ this method to estimate the trophic positions of 200 free‐roaming organisms, representing 39 species in coastal marine (a stony shore) and 38 species in terrestrial (a fruit farm) environments. Based on the trophic positions from the isotopic composition of amino acids, we are able to resolve the trophic structure of these complex food webs. Our approach reveals a high degree of trophic omnivory (i.e., noninteger trophic positions) among carnivorous species such as marine fish and terrestrial hornets.This information not only clarifies the trophic tendencies of species within their respective communities, but also suggests that trophic omnivory may be common in these 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.     

Food‐web structure varies along environmental gradients in a high‐latitude marine ecosystem

Large‐scale patterns in species diversity and community composition are associated with environmental gradients, but the implications of these patterns for food‐web structure are still unclear. Here, we investigated how spatial patterns in food‐web structure are associated with environmental gradients in the Barents Sea, a highly productive shelf sea of the Arctic Ocean. We compared food webs from 25 subregions in the Barents Sea and examined spatial correlations among food‐web metrics, and between metrics and spatial variability in seawater temperature, bottom depth and number of days with ice cover. Several food‐web metrics were positively associated with seawater temperature: connectance, level of omnivory, clustering, cannibalism, and high variability in generalism, while other food‐web metrics such as modularity and vulnerability were positively associated with sea ice and negatively with temperature. Food‐web metrics positively associated with habitat heterogeneity were: number of species, link density, omnivory, path length, and trophic level. This finding suggests that habitat heterogeneity promotes food‐web complexity in terms of number of species and link density. Our analyses reveal that spatial variation in food‐web structure along the environmental gradients is partly related to species turnover. However, the higher interaction turnover compared to species turnover along these gradients indicates a consistent modification of food‐web structure, implying that interacting species may co‐vary in space. In conclusion, our study shows how environmental heterogeneity, via environmental filtering, influences not only turnover in species composition, but also the structure of food webs over large spatial scales.     

Omnivory as a stabilizing feature of natural communities

Abstract Omnivory-defined broadly as feeding on more than one trophic level-occupies a prominent position in discussions of food web architecture and dynamics, due in large part to an enduring conflict regarding omnivory's role in community dynamics. According to classical results from mathematical food web theory, omnivory destabilizes ecological communities, whereas more recent conceptual syntheses suggest that omnivory should be a strongly stabilizing factor in food webs. Working with an arthropod assemblage at Mount Saint Helens, I experimentally addressed this controversy using a two-way factorial design that crossed a manipulation of the degree of omnivory with another "disturbance" manipulation that targeted a specific component of the assemblage. In this statistical design, significant interaction effects (i.e., how the community impacts of the disturbance varied with the degree of omnivory) identified key stabilizing or destabilizing influences of omnivory. Overall, my experimental results indicated that increasing the degree of omnivory stabilized community dynamics, in keeping with recent conceptual syntheses.     

Topological properties of food webs: from real data to community assembly models

We explore patterns of trophic connections between species in the largest and highest-quality empirical food webs to date, introducing a new topological property called the link distribution frequency (i.e. degree distribution), defined as the frequency of species S _L with L links. Non-trivial differences are shown in link distribution frequencies between species-rich and species-poor communities, which might have important consequences for the responses of ecosystems to disturbances. Coarse-grained topological properties observed, as species richness-connectance and number of links-species richness relationships, provide no support for the theory of links-species scaling law or constant connectance across empirical food webs investigated. We further explore these observations by means of simulated food webs resulting from multitrophic assembly models using different functional responses between species. Species richness-connectance and links-species richness relationships of empirical food webs are reproduced by our models, but degree distributions are not properly predicted, suggesting the need of new theoretical approximations to food web assembly. The best agreement between empirical and simulated webs occurs for low values of interaction strength between species, corroborating previous empirical and theoretical findings where weak interactions govern food web dynamics.     

Omnivory and the stability of simple food webs

Traditional ecological theory predicts that the stability of simple food webs will decline with an increasing number of trophic levels and increasing amounts of omnivory. These ideas have been tested using protozoans in laboratory microcosms. However, the results are equivocal, and contrary to expectation, omnivory is common in natural food webs. Two recent developments lead us to re-evaluate these predictions using food webs assembled from protists and bacteria. First, recent modelling work suggests that omnivory is actually stabilizing, providing that interactions are not too strong. Second, it is difficult to evaluate the degree of omnivory of some protozoan species without explicit experimental tests. This study used seven species of ciliated protozoa and a mixed bacterial flora to assemble four food webs with two trophic levels, and four webs with three trophic levels. Protist species were assigned a rank for their degree of omnivory using information in the literature and the results of experiments that tested whether the starvation rate of predators was influenced by the amount of bacteria on which they may have fed and whether cannibalism (a form of omnivory) occurred. Consistent with recent modelling work, both bacterivorous and predatory species with higher degrees of omnivory showed more stable dynamics, measured using time until extinction and the temporal variability of population density. Systems with two protist species were less persistent than systems with one protist species, supporting the prediction that longer food chains will be less stable dynamically. Received: 28 December 1997 / Accepted: 22 June 1998     

The consequences of size dependent foraging for food web topology

A general question in biology is how processes at one scale, for example that of individual organisms, influence patterns at larger scales, for example communities of interacting individuals. Here we ask how changing the size‐dependence of the foraging behaviour of individuals can influence the structure of food webs. We assembled communities using a model in which species interactions are determined by allometric foraging rules of (1) handling time and (2) attack rates, and also (3) the distribution of body sizes. We systematically varied these three factors and examined their effects on three community level, food web allometries: the generality ‐ mass correlation, the vulnerability ‐ mass correlation and the trophic height ‐ mass correlation. The results demonstrate how allometries of individual foraging behaviour (handling time and attack rates) are linked across scales of organisation: different community level allometries are influenced by different individual level allometries. For example, generality allometries in the community are most affected by the individual allometric relationships of the attack rate, whereas trophic level allometries in the community are more strongly influenced by variation in individual handling time allometries. Importantly, we also find that the shape of the body size distribution from which species are drawn has a substantial influence on how these links between scales operate. This study suggests that understanding the variation of size structure among ecological networks requires knowledge about the causes of variation in individual foraging behaviour and determinants of the regional body size distribution.     

Persistence despite omnivory: benthic communities and the discrepancy between theory and observation

Omnivory is omnipresent in natural communities. However, most theoretical models predict that omnivory should be rare, especially at high basal productivity. To address this incongruity, we consider as an example benthic food webs with omnivory. We present a mathematical analysis of simple benthic food webs in which a number of mechanisms promote persistence of omnivory. As a model system, we focus on the interaction between detritus, bacteria and deposit feeders that feed on both bacteria and detritus. Biomass patterns change with increasing basal productivity, triggering mechanisms that weaken the interactions between components of omnivorous interactions. Consequently, these mechanisms extend the range of organic input rates at which omnivorous interactions persist, and prevent exclusion, promoting omnivorous interactions in productive environments. These mechanisms give potential explanations for the high incidence of omnivory in benthic communities and shed insight on the persistence of omnivory in other communities.     

Potential consequences of climate change for primary production and fish production in large marine ecosystems

Existing methods to predict the effects of climate change on the biomass and production of marine communities are predicated on modelling the interactions and dynamics of individual species, a very challenging approach when interactions and distributions are changing and little is known about the ecological mechanisms driving the responses of many species. An informative parallel approach is to develop size-based methods. These capture the properties of food webs that describe energy flux and production at a particular size, independent of species'' ecology. We couple a physical–biogeochemical model with a dynamic, size-based food web model to predict the future effects of climate change on fish biomass and production in 11 large regional shelf seas, with and without fishing effects. Changes in potential fish production are shown to most strongly mirror changes in phytoplankton production. We project declines of 30–60% in potential fish production across some important areas of tropical shelf and upwelling seas, most notably in the eastern Indo-Pacific, the northern Humboldt and the North Canary Current. Conversely, in some areas of the high latitude shelf seas, the production of pelagic predators was projected to increase by 28–89%.     

Native richness and species level trophic traits predict establishment of alien freshwater fishes

Community level ecological traits are thought to affect invasibility as more diverse communities with complex trophic interactions may be associated with greater biotic resistance. Elucidation of the nature of this relationship is often hampered by difficulties in characterising food webs, particularly where field data are lacking. We attempted to overcome this by coupling food web modelling with information-theoretic analysis of the modelled webs. In addition, we also investigated the possibility that species level trends in trophic traits of established aliens might reflect exploitation of empty niches. We constructed hypothetical food webs of 26 natural and artificial lentic habitats from a data set consisting of 370 fish species representing 71 families. Using these food webs, we investigated associations at the community level between food web traits and network topology and number of alien fish species using an information-theoretic approach based on a set of competing a priori hypotheses. At the species level, we similarly tested for trends in trophic traits of established alien fishes using the information-theoretic approach in addition to nMDS of diet data. We found that native species richness in a community was the most important determinant of the number of alien fish taxa, displaying an inverse relationship. Our data also show that alien fish generally feed lower down the food web. Our findings suggest that the biotic resistance hypothesis, though scale dependent, can result in observable effects in animal communities. Moreover, we also found that the ability to exploit low energy yield food sources could favour the establishment of alien species via avoidance of resistive forces from native taxa.     

Species loss and the structure and functioning of multitrophic aquatic systems

Experiments and theory in single trophic level systems dominate biodiversity and ecosystem functioning research and recent debates. All natural ecosystems contain communities with multiple trophic levels, however, and this can have important effects on ecosystem structure and functioning. Furthermore, many experiments compare assembled communities, rather than examining loss of species directly. We identify three questions around which to organise an investigation of how species loss affects the structure and functioning of multitrophic systems. 1) What is the distribution of species richness among trophic levels; 2) from which trophic levels are species most often lost; and 3) does loss of species from different trophic levels influence ecosystem functioning differently? Our analyses show that: 1) Relatively few high‐quality data are available concerning the distribution of species richness among trophic levels. A new data‐set provides evidence of a decrease in species richness as trophic height increases. 2) Multiple lines of evidence indicate that species are lost from higher trophic levels more frequently than lower trophic levels. 3) A theoretical model suggests that both the structure of food webs (occurrence of omnivory and the distribution of species richness among trophic levels) and the trophic level from which species are lost determines the impact of species loss on ecosystem functioning, which can even vary in the sign of the effect. These results indicate that, at least for aquatic systems, models of single trophic level ecosystems are insufficient for understanding the functional consequences of extinctions. Knowledge is required of food web structure, which species are likely to be lost, and also whether cascading extinctions will occur.