Intraguild Predation Research Articles

Adaptive Reproductive Strategies of an Ectoparasitoid Sclerodermus guani under the Stress of Its Entomopathogenic Fungus Beauveria bassiana.

Complex interspecific relationships between parasites and their insect hosts involve multiple factors and are affected by their ecological and evolutionary context. A parasitoid Sclerodermus guani (Hymenoptera: Bethylidae) and an entomopathogenic fungus Beauveria bassiana (Hypocreales: Cordycipitaceae) shared the same host in nature, Monochamus alternatus (Coleoptera: Cerambycidae). They often encountered the semi-enclosed microhabitat of the host larvae or pupae. We tested the survival and reproduction of the parasitoid's parent and its offspring fitness under different concentrations of B. bassiana suspension. The results show that S. guani parent females carrying higher concentrations of the pathogen shorten the pre-reproductive time and regulate their own fertility and their offspring's survival and development. This minimal model of the interspecific interactions contains three dimensionless parameters, vulnerability (θ), dilution ratio (δ), and PR, which were used to evaluate the mortality effect of the parasitoid S. guani on its host M. alternatus under the stress of the entomopathogenic fungus B. bassiana. We compared the infection and lethal effect of the fungus B. bassiana with different concentrations to the parasitoid S. guani and the host larvae M. alternatus. At higher concentrations of the pathogen, the parasitoid parent females shorten the pre-reproductive time and regulate their own fertility and their offspring's survival and development. At moderate concentrations of the pathogen, however, the ability of the parasitoid to exploit the host is more flexible and efficient, possibly reflecting the potential interspecific interactions between the two parasites which were able to coexist and communicate with their hosts in ecological contexts (with a high overlap in time and space) and cause interspecific competition and intraguild predation.

Size-Dependent Intraguild Predation, Cannibalism, and Resource Allocation Determine the Outcome of Species Coexistence.

AbstractIntraguild predation (IGP), a system in which species compete for resources and prey on each other, is more common than existing theory predicts. In theory, an IG predator and its prey can coexist if the IG predator is a weaker competitor for a shared resource and the predator directly benefits from consuming the prey. However, many species that are IG predators also consume members of their own species (cannibalism). Here, we ask whether cannibalism can help resolve the paradox of IGP systems. Our approach differs from previous work on IGP and cannibalism by explicitly considering the size dependence of predatory interactions and how the benefits of predation are allocated to survival, growth, and fecundity of the predator or cannibal. Our results show that cannibalism facilitates coexistence under conditions that are opposite of those predicted by standard IGP theory: species can coexist when the cannibal is a better competitor on the shared resources, directly benefits little from consuming conspecifics, and allocates resources from predation more toward growth and fecundity over survival. Because the effects of IGP and cannibalism are opposite, when an IGP predator is also a cannibal, coexistence between the IGP predator and its prey is not possible and instead depends on the operation of other coexistence mechanisms (e.g., resource partitioning). These results point to the importance of understanding the relative rates of IGP and cannibalism as well as the resource allocation strategy of the IG predator in determining the likelihood of species coexistence.

Effect of Larval Instar on Intraguild Predation and Cannibalization in Herbivorous Scarab Beetles

Effect of Larval Instar on Intraguild Predation and Cannibalization in Herbivorous Scarab Beetles

Intraguild predation is increased in areas of low prey diversity in a generalist predator community.

Niche differentiation and intraguild predation (IGP) can allow ecologically similar species to coexist, although it is unclear which coexistence mechanism predominates in consumer communities. Until now, a limited ability to quantify diets from metabarcoding data has precluded the use of sequencing data to determine the relative importance of these mechanisms. Here, we pair a recent metabarcoding quantification approach with stable isotope analysis to examine diet composition in a wolf spider community. We compare the prevalence of resource partitioning and IGP in these spiders and test whether factors that influence foraging performance, including individual identity, morphology, prey community and environmental conditions, can explain variation in diet composition and IGP. Extensive IGP is likely the primary coexistence mechanism in this community, and other factors to which foraging variation is often attributed do not explain diet composition and IGP here. Rather, IGP increases as prey diversity decreases. Foragers are driven to IGP where resource niches are limited. We highlight the need to examine how drivers of predator-prey interaction strengths translate into foraging in natural systems.

A Case for the "Competitive Exclusion-Tolerance Rule" as a General Cause of Species Turnover along Environmental Gradients.

AbstractClosely related, ecologically similar species often segregate their distributions along environmental gradients of time, space, and resources, but previous research suggests diverse underlying causes. Here, we review reciprocal removal studies in nature that experimentally test the role of interactions among species in determining their turnover along environmental gradients. We find consistent evidence for asymmetric exclusion coupled with differences in environmental tolerance causing the segregation of species pairs, where a dominant species excludes a subordinate from benign regions of the gradient but is unable to tolerate challenging regions to which the subordinate species is adapted. Subordinate species were consistently smaller and performed better in regions of the gradient typically occupied by the dominant species compared with their native distribution. These results extend previous ideas contrasting competitive ability with adaptation to abiotic stress to include a broader diversity of species interactions (intraguild predation, reproductive interference) and environmental gradients, including gradients of biotic challenge. Collectively, these findings suggest that adaptation to environmental challenge compromises performance in antagonistic interactions with ecologically similar species. The consistency of this pattern across diverse organisms, environments, and biomes suggests generalizable processes structuring the segregation of ecologically similar species along disparate environmental gradients, a phenomenon that we propose should be named the competitive exclusion-tolerance rule.

Associations between a range‐shifting damselfly (Erythromma viridulum) and the UK's resident Odonata suggest habitat sharing is more important than antagonism

Abstract Species shifting their ranges under climate change are a conservation dilemma. Range‐shifters may be threatened by climate change in their historic range. However, range‐shifters are likely to be generalist opportunists, which could mean they could harm aspects of biodiversity in their new ecosystems. Therefore, we need approaches to rapidly assess how range‐shifters may integrate into the community of historically resident species. The small red‐eyed damselfly (Erythromma viridulum) has shifted into the United Kingdom since 1999 and may affect resident Odonata via intraguild predation. We asked whether the damselfly's arrival is associated with a decline in resident Odonata. We harnessed the British Dragonfly Society's dataset, using records from 49,788 site visits between 2000 and 2015 to construct dynamic species occupancy models for 17 resident UK Odonata. We estimated the potential effect of E. viridulum presence on the probability that each species would persist at a given site, while controlling for potential effects of climate and recording effort. On average, dragonflies (Anisoptera) persisted more frequently at sites where E. viridulum had established, while damselflies (Zygoptera) showed no change in persistence. Nevertheless, two resident damselflies, including E. viridulum's congener, disappeared more frequently when the range‐shifter established. We suggest that E. viridulum poses minimal risk to most UK resident Odonata. Rather, E. viridulum may be differentially establishing in areas with good habitat quality, where many species of historically resident Odonata are also found. Therefore, high quality, biodiverse sites may become home to increasing numbers of range‐shifters in future. Our approach permits rapid detection of how range‐shifters are integrating into resident biota.

Spider mites avoid caterpillar traces to prevent intraguild predation

The phytophagous spider mites Tetranychus kanzawai and Tetranychus urticae can be as small as < 0.5 mm; thus, they are often incidentally consumed along with food plant leaves by voracious lepidopteran larvae (hereafter, ‘caterpillars’). Therefore, the ability to avoid such intraguild predation should confer a selective advantage to mites. We experimentally demonstrated that adult females of both mite species avoided settling on food plant leaves with traces of all tested caterpillar species (Bombyx mori, Papilio xuthus, Spodoptera litura and Theretra oldenlandiae). We examined additional interactions using B. mori and T. kanzawai and found that B. mori trace avoidance by T. kanzawai lasted for more than 48 h. Tetranychus kanzawai also avoided B. mori traces on plant stems, along which mites access leaves. Moreover, T. kanzawai avoided acetone extracts of B. mori traces applied to filter paper, indicating that chemical substances of caterpillar traces are responsible for the avoidance. This study is the first demonstration of a repellent effect of herbivore trace chemicals on heterospecific herbivores. Although spider mites have developed resistance against many synthetic pesticides, these results predict that natural compounds simulating caterpillar traces may repel spider mites from agricultural crops.

Intraguild Predation of an American Kestrel Fledgling by Crested Caracaras in Northern Patagonia, Argentina

Intraguild Predation of an American Kestrel Fledgling by Crested Caracaras in Northern Patagonia, Argentina

Dances with wolves: The demographic consequence of asymmetric competition and intraguild predation in a native‐invasive skink system

Abstract Currently, we lack enough knowledge to fully explain how the impacts of species invasion on native communities are attributed to multifaceted, individual‐based behavioural outcomes. Here, we illustrate the long‐term population dynamics of the native long‐tailed sun skink (Eutropis longicaudata) before and after the invasion of the common sun skink (Eutropis multifasciata). We conducted diet investigation, morphological measurement, and a series of behavioural experiments both in the field and laboratory. We explained how the impacts of the invasive skink on the native skink can cascade towards the population level based on these individual‐level behavioural data. We present evidence of competition exclusion of the native skink population resulting from the invasion of the common sun skink. The drastic decline found in the native skink population was largely accounted for by low recruitment, as shown by the decrease in its clutch numbers correspondingly. We also found dominance of the invasive skink in both exploitation competition and intraguild predation. Considering the highly overlapping morphological and dietary niches between the two species, our findings imply that the native skink has undergone strong food competition and predation pressure on its eggs and juveniles. Interestingly, the native skink started to display parental care behaviour 2 years after the invasion event, and its clutch survival rate has recovered since then. The shift in parental care behaviour may help the native skink cope with this new predation pressure from the invasive skink. Overall, the two competitive skinks showed low chances of coexisting. The negative population growth of this native skink species may be primarily derived from poor reproductive performance, given a sharp decline in its clutch numbers and its inferiority in exploitation competition, despite rebounding clutch survival rates. Read the free Plain Language Summary for this article on the Journal blog.

An experimental framework for quantifying the degree of intraguild predation in omnivorous food webs in the field

AbstractIntraguild predation (IGP) is common in natural and human‐managed systems and plays a critical role in food web dynamics. Although studies have documented the occurrence of IGP across a wide range of predator taxa, quantitative understanding regarding the degree/intensity of IGP remains lacking. I propose an experimental framework combining controlled feeding trials and stable isotope analysis to quantify the degree of IGP in an omnivorous food web in the field consisting of a top predator, a mesopredator, and a shared prey. The degree of IGP is defined as the proportion (in number) of mesopredators consumed in the total diet (shared prey + mesopredator) of top predators. Feeding trials along with stable isotope analysis are used to construct a standard curve of the relationship between the diet composition of top predator and its nitrogen isotope signatures. The nitrogen isotope signatures of field‐collected top predator individuals are then analyzed and interpolated to the standard curve to estimate the degree of IGP in the field. The proposed framework leverages the strengths of different experimental approaches to study trophic interactions, providing a practical tool for quantifying IGP in a more accurate (controlled feeding trials and standard IGP curve) and realistic (stable isotope analysis of field samples) fashion. The current framework can be further extended to food webs involving more complex interactions (e.g., multiple shared prey) and complemented with other approaches (e.g., molecular gut content analysis) to capture a more complete picture of IGP dynamics in the field.

When the red-lined carrion beetle disrupts successional dynamics on large vertebrate carcasses

In a field study of insect colonization on domestic pig carcasses, the typical colonization sequence took a different turn midway through decomposition when Necrodes surinamensis (Fabricius) (Coleoptera: Silphidae) dramatically increased in abundance on some carcasses. This provided an opportunity to test the prediction that N. surinamensis would aggregate at clumped carcasses but not as much at dispersed carcasses, thus leaving enough resources in less heavily colonized habitat patches to support weaker competitors, as predicted by the aggregation model of coexistence. Larger aggregations of this silphine beetle resulted in the collapse of blow fly (Diptera: Calliphoridae) maggot populations due to intraguild predation, and a decline or exclusion of late-successional insect species. This phenomenon has been reported in a European Necrodes species but it is the first time it is documented with N. surinamensis, a widespread species in North America. Substantial increases in adult and larval populations of N. surinamensis were first documented on clumped carcasses and were not as pronounced on dispersed carcasses. The specifics of N. surinamensis aggregations are discussed with reference to ecological and forensic implications, including the fact that feeding by N. surinamensis larvae makes the remains appear to have been altered by scavengers and decomposing for longer than they have.

Stoichiometry and environmental change drive dynamical complexity and unpredictable switches in an intraguild predation model

We incorporate stoichiometry (the balance of key elements) into an intraguild predation (IGP) model. Theoretical and numerical results show that our system exhibits complex dynamics, including chaos and multiple types of both bifurcations and bistability. Types of bifurcation present include saddle-node, Hopf, and transcritical bifurcations, and types of bistability present include node-node, node-cycle, and cycle-cycle bistability; cycle-cycle bistability has never been observed in IGP ordinary differential equation models. Stoichiometry can stabilize or destabilize the system via the disappearance or appearance of chaos. The species represented in the model can coexist for moderate levels of light intensity and nutrient availability. When the amount of light or nutrients present is extremely high or low, coexistence of the species becomes impossible, potentially harming biodiversity. Interestingly, stoichiometry can facilitate the re-emergence of severely endangered species as light intensity increases. In a temporally changing environment, the system can jump between different unstable states following changes in light intensity, with the trajectory followed depending strongly on initial conditions.

Intraguild Predation of Hippodamia variegata on Aphid Mummies in Cotton Field.

Intraguild predation among arthropod predators in agricultural ecosystems may have a negative impact on biological control. At present, there are few direct reports on trophic relationships among participants of predation in field groups. In this study, we measured the feeding choices of Hippodamia variegata (Goeze) towards mummies with different densities of Aphis gossypii Glover. The dynamics of the occurrence of mummies in the cotton field were investigated over 2017-2019. Singleplex PCR and multiplex PCR were used to detect the predation of 2090 H. variegata individuals on aphids and mummies in Xinjiang cotton field, which revealed the intraguild predation frequency between H. variegata and various parasitoids. There was no obvious feeding preference of H. variegata towards live aphids or mummies, which mainly depended on the relative density of prey. Among the four species of aphids detected in H. variegata, A. gossypii had a high detection rate and was the main prey source of the ladybeetle in the cotton filed. Mostly, ladybeetles consumed parasitoids through mummies, with 6.39% directly feeding on adult parasitoids. H. variegata had strong trophic links to both parasitoids and aphids. We established a food web of aphids-primary parasitoids-hyperparasitoids-H. variegata, which can be used to evaluate the pest control ability of H. variegata from a new perspective.

Trait adaptation enhances species coexistence and reduces bistability in an intraguild predation module.

Disentangling how species coexist in an intraguild predation (IGP) module is a great step toward understanding biodiversity conservation in complex natural food webs. Trait variation enabling individual species to adjust to ambient conditions may facilitate coexistence. However, it is still unclear how coadaptation of all species within the IGP module, constrained by complex trophic interactions and trade-offs among species-specific traits, interactively affects species coexistence and population dynamics. We developed an adaptive IGP model allowing prey and predator species to mutually adjust their species-specific defensive and offensive strategies to each other. We investigated species persistence, the temporal variation of population dynamics, and the occurrence of bistability in IGP models without and with trait adaptation along a gradient of enrichment represented by carrying capacity of the basal prey for different widths and speeds of trait adaptation within each species. Results showed that trait adaptation within multiple species greatly enhanced the coexistence of all three species in the module. A larger width of trait adaptation facilitated species coexistence independent of the speed of trait adaptation at lower enrichment levels, while a sufficiently large and fast trait adaptation promoted species coexistence at higher enrichment levels. Within the oscillating regime, increasing the speed of trait adaptation reduced the temporal variability of biomasses of all species. Finally, species coadaptation strongly reduced the presence of bistability and promoted the attractor with all three species coexisting. These findings resolve the contradiction between the widespread occurrence of IGP in nature and the theoretical predictions that IGP should only occur under restricted conditions and lead to unstable population dynamics, which broadens the mechanisms presumably underlying the maintenance of IGP modules in nature. Generally, this study demonstrates a decisive role of mutual adaptation among complex trophic interactions, for enhancing interspecific diversity and stabilizing food web dynamics, arising, for example, from intraspecific diversity.

Comparison of dynamic behavior between continuous- and discrete-time models of intraguild predation.

Intraguild predation is a common ecological phenomenon that manifests itself by the aggression of one predator by another to obtain a shared prey species. In this paper, we develop a discrete analog of a stoichiometric continuous-time intraguild predation model. We analyze the dynamics of the discrete-time model, such as boundedness and invariance, stability of equilibria, and features of ecological matrices. The dynamic behavior of the two models is compared and analyzed through numerical analysis. We observe the same coexistence region of populations and stoichiometric effects of food quality of the shared prey in both models. Obvious differences between the discrete- and continuous-time models can be observed with intermediate and high levels of light intensity. The multistability characteristics and the existence interval of chaos differ among the different time scale models. This study provides evidence of the importance of time scales on intraguild predation.

Predatory capacity and intraguild interaction between aphidophagous predators in the control of rose bush aphids

Chrysoperla externa (Hagen) and Hippodamia convergens (Guérin-Meneville) are voracious generalist predators, and important aphid control agents. In an environment containing a complex of species, the occurrence of intraguild interactions can interfere in the predator behavior and consumption. The aim of this work was to know the number of nymphs of Rhodobium porosum (Sanderson) and Macrosiphum rosae (Linnaeus) consumed by larvae of C. externa and H. convergens, and the interaction between these predators when confined together. First, second and third instar nymphs of R. porosum and M. rosae were provided in Petri dishes containing rose leaflets and second instar larvae of the predators. Intraguild interaction was studied in Petri dishes containing first instar nymphs of both aphid species and a second instar larva of C. externa plus one of H. convergens. A third treatment consisted of dishes containing a second instar larva of both predators maintained in the absence of prey. The evaluations took place throughout the entire instar of the predators. C. externa consumed a greater number of R. porosum nymphs and H. convergens a greater number of M. rosae nymphs. For both species of prey, the highest consumption was verified on the last day of evaluation. There was a positive interaction when the predator’s larvae were confined in the presence of aphid nymphs, with no mortality observed for any of them. In the absence of prey, there was 70% mortality of H. convergens larvae due to intraguild predation.

Effect of diet composition and temperature on the gastric evacuation rate of European sardine: implication for egg predation estimates

Cannibalism and intraguild predation of fish eggs are frequently observed for small and medium pelagic fish and can be an important cause of natural mortality. The European sardine Sardina pilchardus is the major predator of pelagic fish eggs in Atlantic Iberian waters. Estimates of egg mortality due to predation rely on a number of parameters that are frequently unknown for most species, such as gastric evacuation rate (GER) and feeding periodicity, and rates obtained for other fish species are generally used. These assumptions can severely affect egg mortality estimates. We conducted laboratory experiments to estimate the GER of European sardine that were fed diets composed of different proportions of fish eggs and other food types, such as Artemia franciscana nauplii, Brachionus plicatilis and microalgae, at different temperatures experienced by sardine in the wild (15, 17 and 21°C). Temperature, predator size and sex did not influence the gastric rates. Prey type significantly affected the GER of sardines, with slower evacuation when offered diets containing a higher concentration of fish eggs rather than microalgae, rotifers and Artemia nauplii. Fish eggs are more nutritionally rich compared to microalgae, rotifers and Artemia nauplii, and therefore more difficult to digest. GERs obtained here for S. pilchardus were similar to those obtained for Sardinops sagax in South Africa. This study provides important information that allows for improving estimates of daily feeding rates and egg mortality by predation, thus increasing our understanding of small pelagic fish population dynamics.

Spatial and temporal cooccurrence among Neotropical native coccinellids and the exotic Harmonia axyridis

Coccinellids are important biological control agents and aphid predators in horticultural crops around the world. Neotropical Cycloneda sanguinea, Eriopis connexa and Coleomegilla quadrifasciata octodecimpustulata, and the exotic Harmonia axyridis (all Coleoptera: Coccinellidae), are predators that mainly feed on aphids. In this work we described the abundance of these coccinellid species and their spatial and temporal cooccurrence in agroecological eggplant crop of Argentina. We also estimate the intensity and symmetry of the intraguild predation between C. quadrifasciata octodecimpustulata and the other species in laboratory experiments. Both temporal and spatial segregation was observed. H. axyridis was the strongest intraguild predator in the interaction with C. quadrifasciata octodecimpustulata, and this latter was the strongest intraguild predator in interaction with C. sanguinea and E. connexa. In this context, native coccinellid species would be vulnerable to the exotic and invasive H. axyridis; however, the lack of cooccurrence of this species with the native ones, under conditions of low density of extra-guild prey would indicate that spatial segregation could be the mechanism by which these species coexist in the eggplant crop.

Direct and Indirect Competitive Interactions between Ooencyrtus nezarae and Paratelenomus saccharalis Parasitizing Megacopta cribraria Egg Patches.

The present study investigated egg parasitoid interspecific interactions between a generalist, Ooencyrtus nezarae Ishii (Hymenoptera: Encyrtidae) and a specialist, Paratelenomus saccharalis Dodd (Hymenoptera: Platygastridae) in a laboratory setting using kudzu bug (Megacopta cribraria Fabricius, (Hemiptera: Plataspidae)) eggs as their shared host. Three experiments were conducted to evaluate the emergence of wasps from parasitized hosts after the simultaneous and sequential release of wasps, monitor aggressive behavior of P. saccharalis, and quantify intraguild predation of O. nezarae larvae on heterospecific P. saccharalis larvae. Results showed that total host egg parasitism was higher when both wasps were released simultaneously than if wasps were released sequentially. Ooencyrtus nezarae produced more total offspring than P. saccharalis in all sequential/simultaneous treatments but produced male offspring in most cases. In the aggressive behavioral experiment, specialist, P. saccharalis used head butting to fight O. nezarae, but no other aggressions were observed. In an experiment examining intraguild predation, O. nezarae was able to develop in host eggs parasitized by P. saccharalis four days earlier, acting as a superior larval competitor. These findings shed light on the potential interspecific interactions between O. nezarae and P. saccharalis, which may determine their relative abundance and influence their compatibility in kudzu bug biological control programs.

Two Better Than One? Potential Effects of Intraguild Predation on the Biological Control of Ceratitis capitata (Diptera: Tephritidae) by the Parasitoid Aganaspis daci (Hymenoptera: Figitidae) and the Predator Pseudoophonus rufipes (Coleoptera: Carabidae)

The use of more than one species to manage a single insect pest is a common practice among biological control programs. However, the beneficial effects of natural enemies are not always additive, which in many cases may be attributed to interspecific interactions such as intraguild predation (IGP). Herein, we investigated the potential IGP between two relevant natural enemies of the Medfly (Ceratitis capitata), the predator Pseudoophonus rufipes and the parasitoid Aganaspis daci, as well as the possible implications of this phenomenon in their efficiency as biocontrol agents. To this end, we assessed their functional responses and different demographic parameters when acting alone and together against C. capitata under laboratory conditions. Coexistence led to a switch in the functional response of both species, from type III to type II in A. daci and the opposite in P. rufipes. Regarding demographic parameters, coexistence resulted in higher parasitoidism and population reduction by A. daci only at low host densities, probably due to competition pressure. In the same circumstances, P. rufipes reduced its predatory activity, rejecting those larvae that were presumably parasitized and causing negligible IGP. At high Medfly densities, A. daci efficiency decreased, and the reduced encounter probability enhanced the predatory activity by P. rufipes. As a result of these trends, Medfly population reduction reached almost 100% at all densities, which suggests an additive effect of both natural enemies and recommends combined releases of these agents as a strategy for the control of the Medfly.