Symbiont-conferred immunity interacts with effects of parasitoid genotype and intraguild predation to affect aphid immunity in a clone-specific fashion

Disentangling multiple predator effects in biodiversity and ecosystem functioning research

Community genomics: a community-wide perspective on within-species genetic diversity.

Intraguild predation is claimed to be ubiquitous in nature. It also occurs among natural enemies in biological control systems, where one natural enemy (the intraguild predator) attacks another species of natural enemy (the intraguild prey), whereas they also compete for the same pest. We review the theory of intraguild predation and its consequences for biological control for two different scenarios. 1. The intraguild predator is the superior natural enemy ($i.e.$ reduces the pest population the most). In this case, the intraguild predator will exclude the intraguild prey, thus there will be no intraguild predation in the long term. 2. The intraguild prey is the superior natural enemy. In this case, the intraguild predator and intraguild prey may coexist or the intraguild predator can exclude the intraguild prey. Theory predicts for this scenario that pest numbers will always be lowest when only the intraguild prey is present. Hence, the occurrence of intraguild predation in cropping systems would never result in increased control, but can result in decreased control. We subsequently review experimental tests of the effect of intraguild predation among natural enemies on the population dynamics of pests. Contrary to expectations, we find that intraguild predation often did not result in an increase of pest populations, even when the intraguild predator was the inferior natural enemy. Often, the presence of the intraguild predator had no effect or even resulted in a decrease of pest populations. Although the number of studies was limited, we scanned the literature to identify possible causes for the discrepancy of experimental results with theoretical predictions. We specifically evaluated trends in the effects with respect to the length of the study period, the spatial scale at which experiments were carried out, the number of species involved in the studies and the spatial complexity of the experimental arenas. There was a slight trend towards experiments of longer duration showing less positive effects on pest densities, but no clear effect of spatial scale. All studies that showed positive effects on pest densities were studies with 3 species, but the number of studies with more than 3 species was small. Spatial complexity had mixed effects on experimental results. In conclusion, it is clear that intraguild predation most often does not increase pest densities as was predicted from theory, but more research is needed to reveal why theory does not meet practice.

Most biological control systems involve a diverse community of natural enemies. We investigated how specialist and generalist natural enemies differ as biological control agents of pea aphids (Acyrthosiphon pisum), and how interactions among natural enemies affect successful control. In alfalfa, pea aphids are attacked by a specialist parasitoid wasp, Aphidius ervi, and a guild of generalist predators primarily made up of Nabis and Orius bugs, coccinellid and carabid beetles, and web-building spiders. In three field experiments, we manipulated the parasitoid, then the generalist predator guild, and finally both classes of natural enemy, and recorded resulting impacts on pea aphid population control. The parasitoid caused little immediate reduction in aphid population growth but caused a large decline after a delay corresponding to the generation time of the parasitoid. In contrast, the generalist guild caused an immediate decline in the aphid population growth rate. However, the generalists did not exert density-dependent control, so aphid densities continued to increase throughout the experiment. The third field experiment in which we simultaneously manipulated parasitoids and predators investigated the possibility of “nonadditive effects” on aphid control. Densities of parasitoid pupae were 50% lower in the presence of generalist predators, indicating intraguild predation. Nonetheless, the ratio of parasitoids to aphids was not changed, and the impact of the two types of natural enemies was additive. We constructed a stage-structured model of aphid, parasitoid, and predator dynamics and fit the model to data from our field experiments. The model supports the additivity of parasitoid and predator effects on aphid suppression but suggests that longer-term experiments (32 d rather than 20 d) would likely reveal nonadditive effects as predation removes parasitoids whose response to aphid densities occurs with a delay. The model allowed us to explore additional factors that could influence the additivity of parasitoid and predator effects. Aphid density-dependent population growth and predator immigration in response to aphid density would likely have little influence on the additivity between parasitism and predation. However, if a parasitoid were to show a strong Type II functional response, in contrast to A. ervi whose functional response is nearly Type I, interactions with predators would likely be synergistic. These analyses reveal factors that should be investigated in other systems to address whether parasitism and predation act additively on host densities. Corresponding Editor: E. Evans.

Generalist predators are often used in biological control programs, although they can be detrimental for pest control through interference with other natural enemies. Here, we assess the effects of generalist natural enemies on the control of two major pest species in sweet pepper: the green peach aphid Myzus persicae (Sulzer) and the western flower thrips Frankliniella occidentalis (Pergande). In greenhouses, two commonly used specialist natural enemies of aphids, the parasitoid Aphidius colemani Viereck and the predatory midge Aphidoletes aphidimyza (Rondani), were released together with either Neoseiulus cucumeris Oudemans, a predator of thrips and a hyperpredator of A. aphidimyza, or Orius majusculus (Reuter), a predator of thrips and aphids and intraguild predator of both specialist natural enemies. The combined use of O. majusculus, predatory midges and parasitoids clearly enhanced the suppression of aphids and consequently decreased the number of honeydew-contaminated fruits. Although intraguild predation by O. majusculus on predatory midges and parasitoids will have affected control of aphids negatively, this was apparently offset by the consumption of aphids by O. majusculus. In contrast, the hyperpredator N. cucumeris does not prey upon aphids, but seemed to release aphids from control by consuming eggs of the midge. Both N. cucumeris and O. majusculus did not affect rates of aphid parasitism by A. colemani. Thrips were also controlled effectively by O. majusculus. A laboratory experiment showed that adult predatory bugs feed on thrips as well as aphids and have no clear preference. Thus, the presence of thrips probably promoted the establishment of the predatory bugs and thereby the control of aphids. Our study shows that intraguild predation, which is potentially negative for biological control, may be more than compensated by positive effects of generalist predators, such as the control of multiple pests, and the establishment of natural enemies prior to pest invasions. Future work on biological control should focus on the impact of species interactions in communities of herbivorous arthropods and their enemies.

Theory and empirical evidence show that intraspecific competition can drive selection favouring the use of novel resources (i.e. niche expansion). The evolutionary response to such selection depends on genetic variation for resource use. However, while genetic variation might facilitate niche expansion, genetically diverse groups may also experience weaker competition, reducing density-dependent selection on resource use. Therefore, genetic variation for fitness on different resources could directly facilitate, or indirectly retard, niche expansion. To test these alternatives, we factorially manipulated both the degree of genetic variation and population density in flour beetles (Tribolium castaneum) exposed to both novel and familiar food resources. Using stable carbon isotope analysis, we measured temporal change and individual variation in beetle diet across eight generations. Intraspecific competition and genetic variation acted on different components of niche evolution: competition facilitated niche expansion, while genetic variation increased individual variation in niche use. In addition, genetic variation and competition together facilitated niche expansion, but all these impacts were temporally variable. Thus, we show that the interaction between genetic variation and competition can also determine niche evolution at different time scales.

Intraguild predation among natural enemies is common in food webs with insect herbivores at their base. Though intraguild predation may be reciprocal, typically one species suffers more than the other and frequently exhibits behavioural strategies to lessen these effects. How such short-term behaviours influence population dynamics over several generations has been little studied. We worked with a model insect community consisting of two species of aphid feeding on different host plants (Acyrthosiphon pisum on Vicia and Sitobion avenae on Triticum), a parasitoid (Aphidius ervi) that attacks both species, and a dominant intraguild predator (Coccinella septempunctata) that also feeds on both aphids (whether parasitized or not). As reported previously, we found A. ervi avoided chemical traces of C. septempunctata. In population cages in the laboratory, application of C. septempunctata extracts to Vicia plants reduced parasitism on A. pisum. This did not increase parasitism on the other aphid species, our predicted short-term trait-mediated effect. However, a longer term multigenerational consequence of intraguild predator avoidance was observed. In cages where extracts were applied in the first generation of the study, parasitoid recruitment was reduced leading to higher population densities of both aphid species. S. avenae thus benefits from the presence of a dominant intraguild predator foraging on another species of aphid (A. pisum) on a different food plant, a long-term, trait-mediated example of apparent mutualism. The mechanism underlying this effect is hypothesized to be the reduced searching efficiency of a shared parasitoid in the presence of cues associated with the dominant predator.

Interactions between natural enemies can be crucial for determining their overall control of pest species, yet the mechanisms that govern such interactions are often poorly understood. The risk of negative effects such as intraguild predation and the possibility of mitigating such risks are important components for ultimately determining the compatibility of biological control agents. We performed a group of experiments to determine whether the coccinellid Harmonia axyridis Pallas (Coleoptera: Coccinellidae) poses an intraguild threat to the parasitoid Aphidius ervi Haliday (Hymenoptera: Braconidae) and to see whether A. ervi is able to avoid predation by responding to the chemical tracks deposited by H. axyridis. We show that although H. axyridis does not readily consume A. ervi mummies, it preferentially consumes parasitized aphids over unparasitized aphids. We also show that A. ervi can defend against this threat by avoiding oviposition in the presence of H. axyridis chemical tracks. Aphidius ervi parasitized far fewer pea aphids Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) on plants [Vicia faba L. (Fabaceae)] with H. axyridis chemical tracks in a no-choice environment at a single-plant scale. Similarly, when parasitoids could move freely between plants with and without tracks, A. ervi parasitism was higher on plants without tracks. Behavioral observations of A. ervi foraging suggested that this might be because of reduced A. ervi attack rates and patch residence times in the presence of H. axyridis tracks. Despite a risk of intraguild predation by H. axyridis, our study suggests that A. ervi may be able to mitigate this risk by altering its behavior in response to chemical cues.

Influence du risque du a la presence de predateurs et a au jeune subit sur le taux d'accouplement et sur sa duree

A synthesis is underway between ecology and evolution, partly brought about by the realization that evolutionary change can take place on ecological timescales (Hairston et al., 2005; Whitham et al., 2006; Carroll et al., 2007). This synthesis attempts to understand the dynamic interplay of ecological and evolutionary processes that results from natural or anthropogenic selective forces (Lankau & Strauss, 2007). Moreover, this synthesis represents an integration of several ‘genes to ecosystems’ approaches, including ‘ecological stochiometry’, ‘community genetics’ (Whitham et al., 2006) and ‘niche construction’. United under the framework of ‘eco-evolutionary dynamics’, these ideas seek to link genetic and phenotypic variation to population dynamics, biodiversity and ecosystem function, and place these disciplines in a dynamic evolutionary framework (i.e. understanding the ecological consequences of evolutionary processes and the evolutionary consequences of ecological interactions). This is not an easy endeavor because any such synthesis needs to be broadly multidisciplinary and integrative (Whitham et al., 2006). And yet the potential pay offs are large given that genetic variation across plant and animal systems can have extended consequences at the population, community and ecosystem levels. These consequences can come in the form of the vital rates of survival, reproduction and migration, as well as arthropod and aquatic macroinvertebrate diversity, soil microbial communities, trophic interactions, carbon storage, soil nitrogen availability, dissolved organic nitrogen and production of primary producers (Whitham et al., 2006; Bailey et al., 2009; Ezard et al., 2009; Harmon et al., 2009; Johnson et al., 2009; Palkovacs et al., 2009; Post & Palkovacs, 2009). The effects of genetic or phenotypic variation are not limited to single systems or to ecologically important species (i.e. keystone species, dominant species, foundation species, ecosystem engineers), although these are excellent places to start looking. Instead, genetic variation seems to have effects that are broadly distributed across plant and animal systems - and these effects can be similar in magnitude to those of nonevolutionary ecological variables, such as climate, species invasion and habitat quality (Hairston et al., 2005; Bailey et al., 2009; Ezard et al., 2009; Palkovacs et al., 2009; Post & Palkovacs, 2009).

The experimental literature on the effects of intraguild predation on population growth rates of herbivorous arthropod prey has expanded substantially in the last decade, creating a body of results that can be used to test hypotheses relevant to biological control. Here we present a formal meta-analysis of the published experimental literature to assess two hypotheses: (1) intraguild predation causes an increase in the density of the shared herbivore prey, and (2) ‘coincidental intraguild predation’, in which a predatory arthropod (the ‘intraguild predator’) consumes a herbivore that harbors a developing parasitoid (the ‘intermediate predator’), is less likely to disrupt biological control than is ‘omnivorous intraguild predation’, in which the intermediate predator is consumed directly. The meta-analysis reveals that intraguild predation does not universally cause an increase in the density of the shared prey; instead, the mean effect size viewed across all studies is not significantly different from zero, and there is strong variability in effects across studies. The meta-analysis also reveals a marginally significant difference between the effects of coincidental and omnivorous intraguild predation: inclusion of a coincidental intraguild predator significantly enhances biological control, at least in the short-term trials included in our database, whereas inclusion of an omnivorous intraguild predator has little overall effect. Thus, our analysis highlights the diversity of effects generated by intraguild predators within arthropod communities. The discrepancy between theory and empirics appears likely to stem from their different time-frames, with theory often emphasizing equilibria and experimentation examining instead short-term transients, and also with the artificial simplification of arthropod communities depicted in theoretical treatments. More work, both theoretical and empirical, is needed to bridge the gap between theory and observation and to develop a deeper understanding of factors generating the observed diversity of intraguild predator effects.

A greater diversity of natural enemies can in some cases disrupt prey suppression, particularly when natural enemies engage in intraguild predation, where natural enemies compete with and prey upon each other. However, empirical studies have often demonstrated enhanced prey suppression despite intraguild predation. A recent theoretical study proposed the hypothesis that, when the intermediate predator is cannibalistic, intraguild predation can reduce cannibalism within the intermediate predator population, leading to little change in intermediate predator mortality and thus enhanced prey suppression. The goal of this study was to examine this hypothesis empirically. Two summer-long field enclosure experiments were conducted in cotton fields. We investigated the effects of adding an intraguild predator, Zelus renardii, on (1) the abundance of a cannibalistic intermediate predator, Geocoris pallens, (2) the abundance of a herbivore, Lygus hesperus, and (3) cotton plant performance. G. pallens adult abundance did not increase, even when food availability was high and natural enemies were absent, suggesting that density-dependent cannibalism imposes an upper limit on its densities. Furthermore, although Z. renardii is an intraguild predator of G. pallens, G. pallens long-term densities were unaffected by Z. renardii. In the presence of the intermediate predator, the addition of the intraguild predator Z. renardii enhanced suppression of L. hesperus, and there were suggestions that Z. renardii and G. pallens partitioned the L. hesperus population. Effects of herbivore suppression cascaded to the plant level, improving plant performance. In conclusion, we provide empirical support for the hypothesis that the addition of an intraguild predator may enhance prey suppression if the intermediate predator expresses density-dependent cannibalism. Intraguild predation and cannibalism co-occur in many communities; thus their joint effects may be broadly important in shaping predator effects on herbivores and plant performance.

An experiment was conducted to test whether parasitoid resistance within a single clonal line of pea aphid (Acyrthosiphon pisum) might increase after exposure to the parasitoid wasp Aphidius ervi. Any change in resistance was expected to occur through an increase in the density of protective symbiotic bacteria rather than genetic change within the aphid or the bacterial symbiont. Six aphid lineages were exposed to high parasitoid attack rates over nine generations, each line being propagated from individuals that had survived attack; a further six lineages were maintained without parasitoids as a control. At the end of the experiment the strength of resistance of aphids from treatment and control lines were compared. No differences in resistance were found.

Evidence for a genetic basis for delayed dispersal in a cooperatively breeding canid

Genetic variation in a single species can have predictable and heritable effects on associated communities and ecosystem processes, however little is known about how genetic variation of a dominant species affects plant community assembly. We characterized the genetic structure of a dominant grass (Sorghastrum nutans) and two subordinate species (Chamaecrista fasciculata, Silphium integrifolium), during the third growing season in grassland communities established with genetically distinct (cultivated varieties or local ecotypes) seed sources of the dominant grasses. There were genetic differences between subordinate species growing in the cultivar versus local ecotype communities, indicating that intraspecific genetic variation in the dominant grasses affected the genetic composition of subordinate species during community assembly. A positive association between genetic diversity of S. nutans, C. fasciculata, and S. integrifolium and species diversity established the role of an intraspecific biotic filter during community assembly. Our results show that intraspecific variation in dominant species can significantly modulate the genetic composition of subordinate species.