Size-dependent interactions inhibit coexistence in intraguild predation systems with life-history omnivory

Growth in body size during ontogeny often results in changes in diet, leading to life-history omnivory. In addition, growth is often dependent on food density. Using a physiologically structured population model, we investigated the effects of these two aspects of individual growth in a system consisting of two size-structured populations, an omnivorous top predator and an intermediate consumer. With a single shared resource for both populations, we found that life-history omnivory decreases the likelihood of coexistence between top predator and intermediate consumer in this intraguild predation (IGP) system. This result contrasts with previous unstructured models and stage-structured models without food-dependent development. Food-dependent development and size-dependent foraging abilities of the predator resulted in a positive feedback between foraging success on the shared resource at an early life stage and foraging success on the intermediate consumer later in life. By phenomenologically incorporating this feedback in an unstructured IGP model, we show that it also demotes coexistence in this simple setting, demonstrating the robustness of the negative effect of this feedback.     

Environmental constraint of intraguild predation: Inorganic turbidity modulates omnivory in fairy shrimps

1. Omnivory is widespread in food webs, with an important stabilising effect. The strength of omnivorous trophic interactions may change considerably with changes in the local environment.
2. Shallow temporary waters are often characterised by high levels of inorganic turbidity that may directly limit the food uptake of filter-feeding organisms, but there is little evidence on how it might affect omnivorous species. Anostracans are key species of temporary waters and recent evidence suggests that these organisms are omnivorous consumers of both phyto- and zooplankton.
3. Using Branchinecta orientalis as a model species, our aim was to test how turbidity affects the feeding of an omnivorous anostracan. To do this, we used short-term feeding experiments and stable isotope analyses, with animals collected from soda pans in eastern Austria. In the feeding experiments, algae and zooplankton were offered as food either separately or in combination. The prey type treatments were crossed with turbidity levels in a factorial design.
4. There was a pronounced decrease in the ingested algal biomass with increasing turbidity. Conversely, ingestion rates on zooplankton were less affected by turbidity. Stable isotope analyses from field material supported our experimental results by showing a positive relationship of the trophic position of anostracans and the trophic niche of the communities with turbidity.
5. Our results show that turbidity modulates the intraguild trophic relationship between anostracans and their prey by shifting the diet of anostracans from more herbivorous in transparent to more carnivorous in turbid waters. Thus, inorganic turbidity might also have a community-shaping role in plankton communities of temporary waters through altering trophic relationships.

     

Prey persistence and abundance in systems with intraguild predation and type-2 functional responses

The apparent prevalence of intraguild predation in productive environments has been regarded as puzzling because some simple models suggest that the intraguild prey species is often either reduced in abundance or driven extinct at high resource productivity. While various theoretical mechanisms that avoid this prediction have been uncovered, they have often been viewed as being narrowly applicable. This article examines the fate of the intraguild prey in models in which consumer species may have type-2 functional responses; these are usually characterized by sustained fluctuations in population density at high enough resource productivities. The models also include adaptive, but imperfect diet choice by the top predator. We concentrate on two situations: (1) the prey exhibits less saturation in its functional response to the resource than does the predator and (2) the predator is unable to persist on the basal resource alone. The reasons given by previous studies for discounting these cases are re-examined. The present analysis shows that prey abundance often increases with increasing productivity in both cases, as does the range of prey parameters that allows prey persistence. It is also possible for the prey to coexist with the predator in spite of having a larger equilibrium requirement for the resource. Different assumptions about the dynamics of diet choice can have a large impact on population responses to enrichment. We argue that the persistence and/or increase in abundance of intraguild prey at higher productivity should not be regarded as puzzling because observations are consistent with a range of theoretical models that reflect commonly observed mechanisms.     

Trophic omnivory across a productivity gradient: intraguild predation theory and the structure and strength of species interactions

Intraguild predation theory centres on two predictions: (i) for an omnivore and an intermediate predator (IG-prey) to coexist on shared resources, the IG-prey must be the superior resource competitor, and (ii) increasing resource productivity causes the IG-prey''s equilibrium abundance to decline. I tested these predictions with a series of species-rich food webs along New Zealand''s rocky shores, focusing on two predatory whelks, Haustrum haustorium, a trophic omnivore, and Haustrum scobina, the IG-prey. In contrast to theory, the IG-prey''s abundance increased with productivity. Furthermore, feeding rates and allometric considerations indicate a competitive advantage for the omnivore when non-shared prey are considered, despite the IG-prey''s superiority for shared prey. Nevertheless, clear and regular cross-gradient changes in network structure and interaction strengths were observed that challenge the assumptions of current theory. These insights suggest that the consideration of consumer-dependent functional responses, non-equilibrium dynamics, the dynamic nature of prey choice and non-trophic interactions among basal prey will be fruitful avenues for theoretical development.     

Coexistence of predator and prey in intraguild predation systems with ontogenetic niche shifts

In basic intraguild predation (IGP) systems, predators and prey also compete for a shared resource. Theory predicts that persistence of these systems is possible when intraguild prey is superior in competition and productivity is not too high. IGP often results from ontogenetic niche shifts, in which the diet of intraguild predators changes as a result of growth in body size (life-history omnivory). As a juvenile, a life-history omnivore competes with the species that becomes its prey later in life. Competition can hence limit growth of young predators, while adult predators can suppress consumers and therewith neutralize negative effects of competition. We formulate and analyze a stage-structured model that captures both basic IGP and life-history omnivory. The model predicts increasing coexistence of predators and consumers when resource use of stage-structured predators becomes more stage specific. This coexistence depends on adult predators requiring consumer biomass for reproduction and is less likely when consumers outcompete juvenile predators, in contrast to basic IGP. Therefore, coexistence occurs when predation structures the community and competition is negligible. Consequently, equilibrium patterns over productivity resemble those of three-species food chains. Life-history omnivory thus provides a mechanism that allows intraguild predators and prey to coexist over a wide range of resource productivity.     

Prey life-history and bioenergetic responses across a predation gradient

To evaluate the importance of non-consumptive effects of predators on prey life histories under natural conditions, an index of predator abundance was developed for naturally occurring populations of a common prey fish, the yellow perch Perca flavescens, and compared to life-history variables and rates of prey energy acquisition and allocation as estimated from mass balance models. The predation index was positively related to maximum size and size at maturity in both male and female P. flavescens, but not with life span or reproductive investment. The predation index was positively related to size-adjusted specific growth rates and growth efficiencies but negatively related to model estimates of size-adjusted specific consumption and activity rates in both vulnerable (small) and invulnerable (large) size classes of P. flavescens. These observations suggest a trade-off between growth and activity rates, mediated by reduced activity in response to increasing predator densities. Lower growth rates and growth efficiencies in populations with fewer predators, despite increased consumption suggests either 1) a reduction in prey resources at lower predator densities or 2) an intrinsic cost of rapid prey growth that makes it unfavourable unless offset by a perceived threat of predation. This study provides evidence of trade-offs between growth and activity rates induced by predation risk in natural prey fish populations and illustrates how behavioural modification induced through predation can shape the life histories of prey fish species.     

Alternative stable states in communities with intraguild predation

Intraguild predation (IGP) is a widespread ecological phenomenon in which two consumers that share a resource also engage in a predator-prey interaction. Theory on IGP predicts the occurrence of alternative stable states, but empirical evidence of such states is scarce. This raises the question of whether alternative states are a rare phenomenon that is unlikely to be observed in nature. Here we analyze a model in which the resource exhibits logistic or chemostat dynamics and consumers have saturating (Type II) functional responses. We show that alternative states can arise for a wide range of biological scenarios and that environmental constraints can make their detection difficult. Our analysis identifies three possible combinations of alternative states: (i) IG prey or IG predator, (ii) coexistence or IG predator, and (iii) coexistence or IG prey. Bifurcation diagrams reveal that alternative states are possible over large regions of the parameter space. However, they can be limited to narrow ranges along the resource productivity axis, which may make it difficult to observe the occurrence of alternative states in communities with IGP. Microcosm experiments provide a promising avenue for detecting combinations of asymptotically stable states along a productivity gradient.     

Using mean first passage times to quantify equilibrium resilience in perturbed intraguild predation systems

Regime shift inducibility depends on equilibrium resilience, which depends on species interactions. When species interactions include intraguild predation (IGP), integrated pest management may induce regime shifts because enhancing the abundance of intraguild predators simultaneously increases competition with, and predation on, invasive prey. To explore the dynamical consequences of such manipulations, we use a bistable, deterministic IGP model with stochastic removals that perturb invader density from the high-density equilibrium. We quantify the combined effects of IGP and such perturbations in terms of mean first passage times (MFPTs) to target invader densities such as thresholds between regimes. Analytical MFPTs compare favorably with those generated by Monte Carlo numerical solutions of the stochastically perturbed IGP model. MFPTs can therefore usefully quantify equilibrium resilience in terms of perturbation schedules. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Emergent impacts of cannibalism and size refuges in prey on intraguild predation systems

Many organisms undergo ontogenetic niche shifts due to considerable changes in size during their development. These ontogenetic shifts can alter the trophic position of individuals, the type and strength of ecological interactions across species, and allow for cannibalism within species. In this study we ask if and how the interaction of a size refuge and cannibalism in the prey alters the dynamics of intraguild predation (IGP) systems. By manipulating the composition of large cannibalistic (Aeshna umbrosa) and predatory (Anax junius) dragonfly larvae in mesocosms we show that the interaction of cannibals and predators was non-linear and increased the survival of prey. The structure of the final resource community shared by prey and predator differed between small and large dragonfly treatments but not within size classes across species. In general, the small prey stage showed similar shifts in microhabitat use and refuge use when exposed to either conspecific cannibals or predators, while large cannibals showed no clear anti-predator response. However, further behavioral experiments revealed that specific behavioral components, such as distances between individuals or number of movements, differed when individuals were exposed to either cannibals or predators. This indicates that individuals discriminated between conspecific or heterospecific predators. Furthermore, in similar experiments large cannibals and predators showed different behaviors when exposed to conspecifics rather than to each other. These changes in behavior are consistent with the observed increase in prey survival. In general, the results indicate that cannibalism and ontogenetic niche shifts can result in behavior-mediated indirect interactions that reduce the impact of the predator on the mortality of its prey and alter the interactions of IGP systems. However, they also indicate that size is not the sole determinant and that we also need to account for the species identity when predicting the dynamics of communities.     

Habitat selection by predators and prey in communities with asymmetrical intraguild predation

Competition and predation have broad ecological consequences as they may influence individual behavior and community structure. In some cases, they are linked and predator and prey are also competitors (intraguild predation). I present a game theoretic model of habitat use by predators and prey under conditions of asymmetrical intraguild predation. This model predicts that when the diet of intraguild predators is restricted to intraguild prey and the resource for which predators and prey compete (the basal resource), co-occurrence is only stable when dietary overlap is low and productivity of the basal resource is not high. The addition of alternative resources for predators results in co-occurrence under all conditions. Variation in alternative resource productivity produces a continuum of intraguild prey distributions from matching relative habitat safety, to one that reflects both food and predation risk. When there is a substantial alternative resource for predators, the distribution of predators matches that of alternative resource availability while the distribution of prey is influenced by both habitat riskiness and food availability. The density and distribution of the predator's alternative resource thus influence habitat selection by the intraguild prey. This stresses the importance of indirect interactions in structuring habitat use in communities and the need to view habitat selection in a community context.     

Species coexistence of communities with intraguild predation: The role of refuges used by the resource and the intraguild prey

In this paper, we develop a three-species intraguild predation model which incorporates refuges used by the resource and the intraguild prey, and focus on the effects of refuges on the three species coexistence. The invasion condition and parameter region for coexistence are obtained using invasion analysis. The new invasion condition requires that all boundary states with one missing species can be invaded by the missing species. Numerical simulations show that refuges have a major influence on species coexistence of intraguild predation system, and the results strongly depend on the types of refuges introduced into the model. Our study also shows that prey's refuges are detrimental to species coexistence except the resource using refuges. In contrast to previous research, we find that spatial structure may play an important role in effects of refuges on species coexistence of intraguild predation systems. Our results may shed new light on understanding the mechanisms and the persistence of multi-species predators-prey system.     

Cannibalism prevents evolutionary suicide of ontogenetic omnivores in life‐history intraguild predation systems

The majority of animal species are ontogenetic omnivores, that is, individuals of these species change or expand their diet during life. If small ontogenetic omnivores compete for a shared resource with their future prey, ecological persistence of ontogenetic omnivores can be hindered, although predation by large omnivores facilitates persistence. The coupling of developmental processes between different life stages might lead to a trade‐off between competition early in life and predation later in life, especially for ontogenetic omnivores that lack metamorphosis. By using bioenergetic modeling, we study how such an ontogenetic trade‐off affects ecological and evolutionary dynamics of ontogenetic omnivores. We find that selection toward increasing specialization of one life stage leads to evolutionary suicide of noncannibalistic ontogenetic omnivores, because it leads to a shift toward an alternative community state. Ontogenetic omnivores fail to re‐invade this new state due to the maladaptiveness of the other life stage. Cannibalism stabilizes selection on the ontogenetic trade‐off, prevents evolutionary suicide of ontogenetic omnivores, and promotes coexistence of omnivores with their prey. We outline how ecological and evolutionary persistence of ontogenetic omnivores depends on the type of diet change, cannibalism, and competitive hierarchy between omnivores and their prey.     

Size structure and substitutability in an odonate intraguild predation system

Interactions between different size classes of predator species have the potential to influence survival of prey species in intraguild predation (IGP) systems, but few studies test for these effects. Using a substitutive design in a field setting, I measured the effects of two size classes of IG predators (large and small larvae of the dragonfly Anax junius) on the mortality of IG prey (larvae of the dragonfly Pachydiplax longipennis). I also examined whether combinations of large A. junius and P. longipennis and small A. junius and P. longipennis had substitutable effects on shared prey (larvae of the damselfly Ischnura verticalis). The presence of both size classes of A. junius, when alone and in combination with P. longipennis, significantly increased mortality of I. verticalis. In the presence of P. longipennis, large and small A. junius had similar effects on the mortality of I. verticalis, and effects of size-structured assemblages of A. junius were similar to the effects of each size class alone at the same density. The effects of the two size classes of A. junius on P. longipennis differed, and P. longipennis mortality was lower when exposed to size structured assemblages of A. junius than when exposed to only large A. junius at the same density. Results were similar to those in a laboratory study, although the effect of P. longipennis on I. verticalis was much lower in the field setting. These results demonstrate that interactions between different size classes of IG predators promote the survival of IG prey and highlight the importance of within-species size structure as a characteristic that may promote the coexistence of predators in IGP systems.     

Spatial dynamics of communities with intraguild predation: the role of dispersal strategies

I investigate the influence of dispersal strategies on intraguild prey and predators (competing species that prey on each other). I find an asymmetry between the intraguild prey and predator in their responses to each other's dispersal. The intraguild predator's dispersal strategy and dispersal behavior have strong effects on the intraguild prey's abundance pattern, but the intraguild prey's dispersal strategy and behavior have little or no effect on the intraguild predator's abundance pattern. This asymmetry arises from the different constraints faced by the two species: the intraguild prey has to acquire resources while avoiding predation, but the intraguild predator only has to acquire resources. It leads to puzzling distribution patterns: when the intraguild prey and predator both move away from areas of high density, they become aggregated to high-density habitats, but when they both move toward areas of high resource productivity, they become segregated to resource-poor and resource-rich habitats. Aggregation is more likely when dispersal is random or less optimal, and segregation is more likely as dispersal becomes more optimal. The crucial implication is that trophic constraints dictate the fitness benefits of using dispersal strategies to sample environmental heterogeneity. A strategy that affords greater benefits to an intraguild predator can lead to a more optimal outcome for both the intraguild predator and prey than a strategy that affords greater benefits to an intraguild prey.     

Two protagonists on aphidophagous patches: effects of learning and intraguild predation

In aphidophagous systems, trophic interactions between parasitoids and predators, termed intraguild predation, are frequently asymmetric. To mitigate predation risk for themselves and their offspring, intraguild prey may exploit associative learning to gain accurate information about patch quality. Therefore, costs of unnecessary escape behavior are avoided. We used sweet pepper patches (Capsicum annuum L., cv. ‘Mazurka’) (Solanaceae), sustaining Macrosiphum euphorbiae (Thomas) or Myzus persicae (Sulzer) (Homoptera: Aphididae) aphids, as a model system to quantify the foraging behaviors of the parasitoid Aphelinus abdominalis (Dalman) (Hymenoptera: Aphelinidae), when confronted with predatory second instar Chrysopa carnea (Stephens) (Neuroptera: Chrysopidae). The behavior of predator‐naive or predator‐experienced A. abdominalis foraging in a patch with or without C. carnea was recorded and analyzed using a multiple video observation system. We investigated (i) whether A. abdominalis could learn to detect the presence of a predator in a patch, (ii) the impact of the predator presence on the learning and motor learning of the parasitoid, and (iii) the effects of the aphid species on the guild interactions. Results showed that the presence of, or experience with the predator does not affect A. abdominalis learning or motor learning. We discuss the behavioral and ecological implications of our finding. Overall, predator‐induced aphid mobility increased the frequency and allocation time of Aphelinus oviposition activities, especially when Ma. euphorbiae was the host. The predator imposed indirect fitness costs on the parasitoid. Aphelinus abdominalis searched more often and longer, resulting in a tendency towards reduced Ma. euphorbiae parasitism rate in patches harboring C. carnea.     

Short-term responses to elevated predator densities: noncompetitive intraguild interactions and behavior

We investigated the short-term response of an arthropod assemblage to elevated generalist predator densities by introducing Chinese mantids (Tenodera sinensis) to field plots in a replicated, controlled experiment. Abundances of carnivorous arthropods were reduced by mantids to a greater extent than herbivores, and cursorial spiders emigrated from treatment plots in greater numbers than from controls. Initially, this emigration consisted only of small spiders that were demonstrated in the laboratory to be prey for mantids. Thus, the initial response of an arthropod assemblage to increased predators, densities was increased interactions among predators, which caused decline in predator population densities in a shorter time than competition for prey would require. Predator avoidance behavior must be considered together with intraguild predation and competition when interpreting the outcome of predator manipulations. Shortterm experiments may be more valuable than longer term studies in detecting this effect.     

Effect of emigration on cannibalism and intraguild predation in aphidophagous ladybirds

Abstract.  1. The incidence and timing of emigration, cannibalism, and intraguild predation of larvae of three aphidophagous ladybirds (Coleoptera: Coccinellidae), Harmonia axyridis Pallas, Coccinella septempunctata brucki Mulsant, and Propylea japonica Mulsant, relative to the presence of prey was determined in the laboratory in single- and mixed-species populations.
2. In single-species populations, 80% of the larvae of C. s. brucki emigrated prior to the extinction of the aphid population and no larvae were lost due to cannibalism; however > 80% of the larvae of the other two species were still present when the aphid became extinct and the losses due to cannibalism for H. axyridis and P. japonica were 25% and 14% respectively. Finally, 28% of the P. japonica larvae completed their development, whereas no larvae of the other two species became adult.
3. In mixed-species populations, mortality of P. japonica attributable to cannibalism or intraguild predation increased greatly to 60%, whereas that of the other two species remained about the same. Consequently, survival of H. axyridis larvae improved and survival of P. japonica worsened; however the survival of C. s. brucki larvae was not affected by the other two species. Early emigration by C. s. brucki larvae may have enabled them to escape intraguild predation by H. axyridis in this system.     

Spatial refuge from intraguild predation: implications for prey suppression and trophic cascades

The ability of predators to elicit a trophic cascade with positive impacts on primary productivity may depend on the complexity of the habitat where the players interact. In structurally-simple habitats, trophic interactions among predators, such as intraguild predation, can diminish the cascading effects of a predator community on herbivore suppression and plant biomass. However, complex habitats may provide a spatial refuge for predators from intraguild predation, enhance the collective ability of multiple predator species to limit herbivore populations, and thus increase the overall strength of a trophic cascade on plant productivity. Using the community of terrestrial arthropods inhabiting Atlantic coastal salt marshes, this study examined the impact of predation by an assemblage of predators containing Pardosa wolf spiders, Grammonota web-building spiders, and Tytthus mirid bugs on herbivore populations (Prokelisia planthoppers) and on the biomass of Spartina cordgrass in simple (thatch-free) and complex (thatch-rich) vegetation. We found that complex-structured habitats enhanced planthopper suppression by the predator assemblage because habitats with thatch provided a refuge for predators from intraguild predation including cannibalism. The ultimate result of reduced antagonistic interactions among predator species and increased prey suppression was enhanced conductance of predator effects through the food web to positively impact primary producers. Behavioral observations in the laboratory confirmed that intraguild predation occurred in the simple, thatch-free habitat, and that the encounter and capture rates of intraguild prey by intraguild predators was diminished in the presence of thatch. On the other hand, there was no effect of thatch on the encounter and capture rates of herbivores by predators. The differential impact of thatch on the susceptibility of intraguild and herbivorous prey resulted in enhanced top-down effects in the thatch-rich habitat. Therefore, changes in habitat complexity can enhance trophic cascades by predator communities and positively impact productivity by moderating negative interactions among predators.     

Short-term responses of phytoplankton to nutrient enrichment and planktivorous fish predation in a temperate South American mesotrophic reservoir

The benthic macroinvertebrate community is an important component of stream diversity, because its members are fundamental connectors among the different trophic levels of running waters. In this study, we assessed alpha and beta diversities of benthic macroinvertebrates in three stream sites and four microhabitats: (i) moss in the air-water interface; (ii) submerged roots of terrestrial plants; (iii) leaf litter deposited in pools; (iv) stones in riffles. We constructed rarefaction curves and compared species richness among microhabitats for each stream site. Additionally, we evaluated which factor, stream site, or microhabitat, was most important in determining variation in assemblage structure, i.e., beta diversity. There was no significant difference among microhabitats in terms of taxa richness evaluated by rarefaction curves. Using partial Constrained Correspondence Analysis (pCCA), we found that microhabitat was most important in determining community composition, accounting for 42.02% of the total variation. Stream sites accounted for 22.27%. In accordance with the pCCA, exploratory multivariate methods (ordination and classification) revealed four distinct groups, corresponding to the four microhabitats, independent of stream sites. Our results indicated that differences among environmental conditions are much more important in the determination of stream assemblage structure than are differences in spatial location. Accordingly, adjacent microhabitats in a single stream site harbor macroinvertebrate assemblages more dissimilar than those found in a single microhabitat at different stream sites. Handling editor: D. Dudgeon     

Evolutionary responses to harvesting in ungulates

1. We investigate the evolutionary responses to harvesting in ungulates using a state-dependent, stochastic, density-dependent individual-based model of red deer Cervus elaphus (L.) females subject to different harvesting regimes. 2. The population's mean weight at first reproduction shifts towards light weights as harvesting increases, and its distribution changes from a single peak distribution under very low or high harvest rates, to a bimodal distribution under intermediate harvest rates. 3. These results suggest that, consistent with previous studies on aquatic species, harvesting-induced mortality may drive adaptive responses in ungulates by reducing the fitness benefits from adult survival and growth in favour of early and lightweight reproduction. 4. Selective harvesting for heavy animals has no additional effect on the evolutionarily stable strategy, suggesting that harvest rate is more important than the degree of selectivity in driving adaptive responses. However, selective harvesting of light females is positively associated with maturation weights even higher than those of a nonharvested population, probably due to the reduction in the fitness value of the offspring. 5. The average number of weight at maturation strategies in the population declines but the total number of strategies across all simulations increases with harvest rate, suggesting that harvesting-induced selection on weight at maturity overcomes the increase in strategy diversity expected from density-dependent release. 6. Yield initially increases with harvesting due to enhanced productivity of light females experiencing density-dependent release. However, it crashes under intense harvesting resulting in a population skewed to light, young and, therefore, less reproductive animals.