Cascading effects of predator diversity and omnivory in a marine food web

Over‐harvesting, habitat loss and exotic invasions have altered predator diversity and composition in a variety of communities which is predicted to affect other trophic levels and ecosystem functioning. We tested this hypothesis by manipulating predator identity and diversity in outdoor mesocosms that contained five species of macroalgae and a macroinvertebrate herbivore assemblage dominated by amphipods and isopods. We used five common predators including four carnivores (crabs, shrimp, blennies and killifish) and one omnivore (pinfish). Three carnivorous predators each induced a strong trophic cascade by reducing herbivore abundance and increasing algal biomass and diversity. Surprisingly, increasing predator diversity reversed these effects on macroalgae and altered algal composition, largely due to the inclusion and performance of omnivorous fish in diverse predator assemblages. Changes in predator diversity can cascade to lower trophic levels; the exact effects, however, will be difficult to predict due to the many complex interactions that occur in diverse 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.     

Stepping in Elton's footprints: a general scaling model for body masses and trophic levels across ecosystems

Despite growing awareness of the significance of body-size and predator-prey body-mass ratios for the stability of ecological networks, our understanding of their distribution within ecosystems is incomplete. Here, we study the relationships between predator and prey size, body-mass ratios and predator trophic levels using body-mass estimates of 1313 predators (invertebrates, ectotherm and endotherm vertebrates) from 35 food-webs (marine, stream, lake and terrestrial). Across all ecosystem and predator types, except for streams (which appear to have a different size structure in their predator-prey interactions), we find that (1) geometric mean prey mass increases with predator mass with a power-law exponent greater than unity and (2) predator size increases with trophic level. Consistent with our theoretical derivations, we show that the quantitative nature of these relationships implies systematic decreases in predator-prey body-mass ratios with the trophic level of the predator. Thus, predators are, on an average, more similar in size to their prey at the top of food-webs than that closer to the base. These findings contradict the traditional Eltonian paradigm and have implications for our understanding of body-mass constraints on food-web topology, community dynamics and stability.     

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.     

The effect of predation pressure and predator adaptive foraging on the relative importance of consumptive and non‐consumptive predator net effects in a freshwater model system

An important challenge in community ecology is identifying the functional characteristics capable of predicting the nature and strength of predator effects on food webs. We developed an individual‐based model, based on a shallow lake model system, to evaluate the total, consumptive, and non‐consumptive indirect effect that predators have on basal resources when the predators differ in their foraging types (active adaptive foraging or sedentary foraging). Overall, both predator types caused similar total indirect effects on lower trophic levels. However, the nature net effects of predators diverged between predator foraging types. Active predators caused larger non‐consumptive effects, relative to the total indirect effect, irrespective of predation pressure levels. On the other hand, sedentary predators caused larger non‐consumptive effects for lower predation pressure levels, but consumptive effects became more important as predation pressure increased. Our simulations showed that the reliance on a particular mechanism driving consumer–resource interactions is altered by predator foraging behavior and highlight the importance of both prey and predator foraging behaviors to predict the causes and consequences of cascading effects observed in food webs.     

Terrestrial trophic cascades: how much do they trickle?

Although more consensus is now emerging on the magnitude and frequency of cascading trophic effects in aquatic communities, the debate over their terrestrial counterparts continues. We used meta-analysis to analyze field experiments on trophic cascades in terrestrial arthropod-dominated food webs to evaluate the overall magnitude of trophic cascades and conditions affecting their occurrence and strength. We found extensive support for the presence of trophic cascades in terrestrial communities. In the majority of experiments, predator removal led to increased densities of herbivorous insects and higher levels of plant damage. Cascades in which removing predators led to decreased herbivory also were detected but were less frequent and weaker, suggesting a predominantly three-trophic-level behavior of arthropod-dominated terrestrial food webs. Despite the clear evidence that cascades often decreased plant damage, residual effects of predation produced either no or only minimal changes in overall plant biomass. Agricultural systems and natural communities exhibited similarly strong effects of predation on herbivore abundance. However, resulting effects on plant damage and community-wide effects of trophic cascades on plant biomass usually were highly variable, and only in the managed agricultural systems did predators occasionally have strong indirect effects on plant biomass. Our meta-analysis suggests that the effects of trophic cascades on the biomass of primary producers are weaker in terrestrial than aquatic food webs.     

Evaluating the effects of trophic complexity on a keystone predator by disassembling a partial intraguild predation food web

1. Many taxa can be found in food webs that differ in trophic complexity, but it is unclear how trophic complexity affects the performance of particular taxa. In pond food webs, larvae of the salamander Ambystoma opacum occupy the intermediate predator trophic position in a partial intraguild predation (IGP) food web and can function as keystone predators. Larval A. opacum are also found in simpler food webs lacking either top predators or shared prey. 2. We conducted an experiment where a partial IGP food web was simplified, and we measured the growth and survival of larval A. opacum in each set of food webs. Partial IGP food webs that had either a low abundance or high abundance of total prey were also simplified by independently removing top predators and/or shared prey. 3. Removing top predators always increased A. opacum survival, but removal of shared prey had no effect on A. opacum survival, regardless of total prey abundance. 4. Surprisingly, food web simplification had no effect on the growth of A. opacum when present in food webs with a low abundance of prey but had important effects on A. opacum growth in food webs with a high abundance of prey. Simplifying a partial IGP food web with a high abundance of prey reduced A. opacum growth when either top predators or shared prey were removed from the food web and the loss of top predators and shared prey influenced A. opacum growth in a non-additive fashion. 5. The non-additive response in A. opacum growth appears to be the result of supplemental prey availability augmenting the beneficial effects of top predators. Top predators had a beneficial effect on A. opacum populations by reducing the abundance of A. opacum present and thereby reducing the intensity of intraspecific competition. 6. Our study indicates that the effects of food web simplification on the performance of A. opacum are complex and depend on both how a partial IGP food web is simplified and how abundant prey are in the food web. These findings are important because they demonstrate how trophic complexity can create variation in the performance of intermediate predators that play important roles in temporary pond food webs.     

Cascading predator control interacts with productivity to determine the trophic level of biomass accumulation in a benthic food web

Large-scale exploitation of higher trophic levels by humans, together with global-scale nutrient enrichment, highlights the need to explore interactions between predator loss and resource availability. The hypothesis of exploitation ecosystems suggests that top–down and bottom–up control alternate between trophic levels, resulting in a positive relationship between primary production and the abundance of every second trophic level. Specifically, in food webs with three effective trophic levels, primary producers and predators should increase with primary production, while in food webs with two trophic levels, only herbivores should increase. We provided short-term experimental support for these model predictions in a natural benthic community with three effective trophic levels, where the number of algal recruits, but not the biomass of gastropod grazers, increased with algal production. In contrast, when the food web was reduced to two trophic levels by removing larger predators, the number of algal recruits was unchanged while gastropod grazer biomass increased with algal production. Predator removal only affected the consumer-controlled early life-stages of algae, indicating that both the number of trophic levels and the life-stage development of the producer trophic level determine the propagation of trophic cascades in benthic systems. Our results support the hypothesis that predators interact with resource availability to determine food-web structure.     

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.     

Linearity in the aggregate effects of multiple predators in a food web

Theory in community ecology often assumes that predator species have similar indirect effects and thus can be treated mathematically as a single functional unit (e.g. guild or trophic level). This assumption is questionable biologically because predator species typically differ in their effects, creating the potential for nonlinearities when they coexist. We evaluated the nature of indirect effects caused by three species of hunting spider predators, singly and in multiple species combinations, on grass and herb plants in experimental old-field food webs. Despite the potential for nonlinearity, indirect effects in different multiple predator combinations consistently did not differ significantly from the respective means of the single species effects. Thus, for this experimental system, the whole was simply the average of the parts. Consequently, models which abstract predator species as single trophic levels would successfully predict indirect effects in this system regardless of the composition of the predator fauna.     

Trickle-down effects of aboveground trophic cascades on the soil food web

Trophic cascades are increasingly being regarded as important features of aboveground and belowground food webs, but the effects of aboveground cascades on soil food webs, and vice versa, remains essentially unexplored. We conducted an experiment consisting of model synthesised communities containing grassland plant and invertebrate species, in which treatments included soil only, soil+plants, soil+plants+aphids, and soil+plants+aphids+predators; predator treatments consisted of the lacewing Micromus tasmaniae and ladybird beetle Coccinella undecimpunctata added either singly or in combination. Addition of Micromus largely reversed the negative effects of aphids on plant biomass, while both of the predator species caused large changes in the relative abundances of dominant plant species. Predators of aphids also affected several components of the belowground subsystem. Micromus had positive indirect effects on the primary consumer of the soil decomposer food web (microflora), probably through promoting greater input of basal resources to the decomposer subsystem. Predator treatments also influenced densities of the tertiary consumers of the soil food web (top predatory nematodes), most likely through inducing changes in plant community composition and therefore the quality of resource input to the soil. The secondary consumers of the soil food web (microbe‐feeding nematodes) were, however, unresponsive. The fact that some trophic levels of the soil food web but not others responded to aboveground manipulations is explicable in terms of top‐down and bottom‐up forces differentially regulating different belowground trophic levels. Addition of aphids also influenced microbial community structure, promoted soil bacteria at the expense of fungi, and enhanced the diversity of herbivorous nematodes; in all cases these effects were at least partially reversed by addition of Micromus. These results in tandem point to upper level consumers in aboveground food webs as a potential driver of the belowground subsystem, and provide evidence that predator‐induced trophic cascades aboveground can have effects that trickle through soil food webs.     

Effects of evolutionary changes in prey use on the relationship between food web complexity and stability

The relationship between food web complexity and stability has been the subject of a long-standing debate in ecology. Although rapid changes in the food web structure through adaptive foraging behavior can confer stability to complex food webs, as reported by Kondoh (Science 299:1388–1391, 2003), the exact mechanisms behind this adaptation have not been specified in previous studies; thus, the applicability of such predictions to real ecosystems remains unclear. One mechanism of adaptive foraging is evolutionary change in genetically determined prey use. We constructed individual-based models of evolution of prey use by predators assuming explicit population genetics processes, and examined how this evolution affects the stability (i.e., the proportion of species that persist) of the food web and whether the complexity of the food web increased the stability of the prey–predator system. The analysis showed that the stability of food webs decreased with increasing complexity regardless of evolution of prey use by predators. The effects of evolution on stability differed depending on the assumptions made regarding genetic control of prey use. The probabilities of species extinctions were associated with the establishment or loss of trophic interactions via evolution of the predator, indicating a clear link between structural changes in the food web and community stability.     

Pyramids of species richness: the determinants and distribution of species diversity across trophic levels

How species richness is distributed across trophic levels determines several dimensions of ecosystem functioning, including herbivory, predation, and decomposition rates. We perform a meta‐analysis of 72 large published food webs to investigate their trophic diversity structure and possible endogenous, exogenous, and methodological causal variables. Consistent with classic theory, we found that published food webs can generally be described as ‘pyramids of species richness’. The food webs were more predator‐poor, prey‐rich and hierarchical than is expected by chance or by the niche or cascade models. The trophic species richness distribution also depended on centrality, latitude, ecosystem‐type and methodological bias. Although trophic diversity structure is generally pyramidal, under many conditions the structure is consistently uniform or inverse‐pyramidal. Our meta‐analysis adds nuance to classic assumptions about food web structure: diversity decreases with trophic level, but not under all conditions, and the decrease may be scale‐dependent. Synthesis The distribution of species richness across trophic levels has not been evaluated in recent decades, despite improvement in food web resolution and the relevance of biodiversity distribution to ecosystem function. Our meta‐analysis of 72 large, recent food webs, illustrates that published food webs can generally be described as basal‐rich, top‐poor ‘pyramids of species richness’, consistent with classic theory. Although trophic diversity structure is generally pyramidal, under some environmental and ecological conditions the structure is uniform or inverse‐pyramidal. Our meta‐analysis confirms classic theory about food web structure, while adding nuance by describing conditions under which classic pyramid structure is not observed.     

Productivity,Disturbance and Ecosystem Size Have No Influence on Food Chain Length in Seasonally Connected Rivers

The food web is one of the oldest and most central organising concepts in ecology and for decades, food chain length has been hypothesised to be controlled by productivity, disturbance, and/or ecosystem size; each of which may be mediated by the functional trophic role of the top predator. We characterised aquatic food webs using carbon and nitrogen stable isotopes from 66 river and floodplain sites across the wet-dry tropics of northern Australia to determine the relative importance of productivity (indicated by nutrient concentrations), disturbance (indicated by hydrological isolation) and ecosystem size, and how they may be affected by food web architecture. We show that variation in food chain length was unrelated to these classic environmental determinants, and unrelated to the trophic role of the top predator. This finding is a striking exception to the literature and is the first published example of food chain length being unaffected by any of these determinants. We suggest the distinctive seasonal hydrology of northern Australia allows the movement of fish predators, linking isolated food webs and potentially creating a regional food web that overrides local effects of productivity, disturbance and ecosystem size. This finding supports ecological theory suggesting that mobile consumers promote more stable food webs. It also illustrates how food webs, and energy transfer, may function in the absence of the human modifications to landscape hydrological connectivity that are ubiquitous in more populated regions.     

Context-dependent effects of predator removal from experimental microcosm communities

The loss of a predator from an ecological community can cause large changes in community structure and ecosystem processes, or have very little consequence for the remaining species and ecosystem. Understanding when and why the loss of a predator causes large changes in community structure and ecosystem processes is critical for understanding the functional consequences of biodiversity loss. We used experimental microbial communities to investigate how the removal of a large generalist predator affected the extinction frequency, population abundance and total biomass of its prey. We removed this predator in the presence or absence of an alternative, more specialist, predator in order to determine whether the specialist predator affected the outcome of the initial species removal. Removal of the large generalist predator altered some species' populations but many were unaffected and no secondary extinctions were observed. The specialist predator, though rare, altered the response of the prey community to the removal of the large generalist predator. In the absence of the specialist predator, the effects of the removal were only measurable at the level of individual species. However, when the specialist predator was present, the removal of the large generalist predator affected the total biomass of prey species. The results demonstrate that the effect of species loss from high trophic levels may be very context-dependent, as rare species can have disproportionately large effects in food webs.     

Disease-induced stabilization of predator-prey oscillations

Parasites are an integral part of virtually all food webs and species communities. Here we consider the invasion of a resident predator-prey system by an infectious disease with frequency-dependent transmission spreading within the predator population. We derive biologically plausible and insightful quantities (demographic and epizootiological reproduction numbers) that allow us to completely determine community composition. Successful disease invasion can have two contrary effects in driving its host population to extinction or in stabilizing predator-prey cycles. Our findings contradict predictions from previous models suggesting a destabilizing effect of parasites. We show that predator infection counteracts the paradox of enrichment. In turn, parasite removal from food webs can have catastrophic effects. We discuss the implications for biological control and resource management on more than one trophic level.     

Connectance determines invasion success via trophic interactions in model food webs

Human induced global change has greatly altered the structure and composition of food webs through the invasion of non‐native species and the extinction of native species. Much attention has been paid to the effects of species deletions on food web structure and stability. However, recent empirical evidence suggests that for most taxa local species richness has increased as successful invasions outpace extinctions at this scale. This pattern suggests that food webs, which represent feeding interactions at the local scale, may be increasing in species richness. Knowledge of how food web structure relates to invasive species establishment and the effect of successful invaders on subsequent food web structure remains an unknown but potentially important aspect of global change. Here we explore the effect of food web topology on invasion success in model food webs to develop hypotheses about how the distribution of biodiversity across trophic levels affects the success of invasion at each trophic level. Our results suggest a connectance (C) based framework for predicting invasion success in food webs due to the way that C constrains the number of species at each trophic level and thus the number of potential predators and prey for an invader at a given trophic level. We use the relationship between C and the proportion of species at each trophic level in 14 well studied food webs to make the following predictions; 1) the success of basal invaders will increase as C increases due to the decrease in herbivores in high C webs, 2) herbivore invasion success will decrease as C increases due to the decrease in the proportion of basal species and increase in intermediate species and omnivores in high C webs. 3) Top predator invasion success will increase as C increases due to the increase in intermediate prey species. However, it is not clear how the relative influence of trophic structure compares to empirically known predictors of invasion success such as invader traits, propagule pressure, and resource availability.     

Bottom-up trophic cascades and material transfer in terrestrial food webs

In contrast to top-down trophic cascades, few reviews have appeared of bottom-up trophic cascades. We review the recent development of research on bottom-up cascades in terrestrial food webs, focusing on tritrophic systems consisting of plants, herbivorous insects, and natural enemies, and attempt to integrate bottom-up cascade and material transfer among trophic levels. Bottom-up cascades are frequently reported in various tritrophic systems, and are important to determine community structure, population dynamics, and individual performance of higher trophic levels. In addition, we highlight several features of bottom-up cascades. Accumulation or dilution of plant nutritional and defensive materials by herbivorous insects provides a mechanistic base for several bottom-up cascades. Such a stoichiometric approach has the potential to improve our understanding of bottom-up cascading effects in terrestrial food webs. We suggest a future direction for research by integration of bottom-up cascades and material transfer among trophic levels.