Plant population size and isolation affect herbivory of <Emphasis Type="Italic">Silene latifolia</Emphasis> by the specialist herbivore <Emphasis Type="Italic">Hadena bicruris</Emphasis> and parasitism of the herbivore by parasitoids

Habitat fragmentation can affect levels of herbivory in plant populations if plants and herbivores are differentially affected by fragmentation. Moreover, if herbivores are top–down controlled by predators or parasitoids, herbivory may also be affected by differential effects of fragmentation on herbivores and their natural enemies. We used natural Silene latifolia populations to examine the effects of plant population size and isolation on the level of herbivory by the seed predating noctuid Hadena bicruris and the rate of parasitism of the herbivore by its parasitoids. In addition, we examined oviposition rate, herbivory and parasitism in differently sized experimental populations. In natural populations, the level of herbivory increased and the rate of parasitism decreased with decreasing plant population size and increasing degree of isolation. The number of parasitoid species also declined with decreasing plant population size. In the experimental populations, the level of herbivory was also higher in smaller populations, in accordance with higher oviposition rates, but was not accompanied by lower rates of parasitism. Similarly, oviposition rate and herbivory, but not parasitism rate, increased near the edges of populations. These results suggests that in this system with the well dispersing herbivore H. bicruris, habitat fragmentation increases herbivory of the plant through a behavioural response of the moth that leads to higher oviposition rates in fragmented populations with a reduced population size, increased isolation and higher edge-to-interior ratio. Although the rate of parasitism and the number of parasitoid species declined with decreasing population size in the natural populations, we argue that in this system it is unlikely that this decline made a major contribution to increased herbivory.     

Do distances among host patches and host density affect the distribution of a specialist parasitoid?

The effect of spatial habitat structure and patchiness may differ among species within a multi-trophic system. Theoretical models predict that species at higher trophic levels are more negatively affected by fragmentation than are their hosts or preys. The absence or presence of the higher trophic level, in turn, can affect the population dynamics of lower levels and even the stability of the trophic system as a whole. The present study examines different effects of spatial habitat structure with two field experiments, using as model system the parasitoid Cotesia popularis which is a specialist larval parasitoid of the herbivore Tyria jacobaeae. One experiment examines the colonisation rate of the parasitoid and the percentage parasitism at distances occurring on a natural scale; the other experiment examines the dispersal rate and the percentage parasitism in relation to the density of the herbivore and its host plant. C. popularis was able to reach artificial host populations at distances up to the largest distance created (at least 80 m from the nearest source population). Also, the percentage parasitism did not differ among the distances. The density experiment showed that the total number of herbivores parasitised was higher in patches with a high density of hosts, regardless of the density of the host plant. The percentage parasitism, however, was not related to the density of the host. The density of the host plant did have a (marginally) significant effect on the percentage parasitism, probably indicating that the parasitoid uses the host plant of the herbivore as a cue to find the herbivore itself. In conclusion, the parasitoid was not affected by the spatial habitat structure on spatial scales that are typical of local patches.     

Host plant genotype determines bottom‐up effects in an aphid‐parasitoid‐predator system

Plant genotypes are known to affect performance of insect herbivores and the community structure of both herbivores and higher trophic levels. Still, only a limited number of studies demonstrate differences in the performance of predators and parasitoids because of plant genotypic effects and most of these focus on gall formers. We designed a greenhouse experiment to investigate the effects of host plant genotype on fitness components in a grass‐aphid‐carnivore system. We used clones of quackgrass [Elytrigia repens (L.) Desv. ex Nevski (Poaceae)], the aphid Rhopalosiphum padi (L.) (Hemiptera: Aphididae), the parasitoid wasp Aphidius colemani (Viereck) (Hymenoptera: Braconidae), and the predatory lacewing Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). The number of aphid offspring differed considerably among plant genotypes. These differences were only in part because of differences in the production of biomass among host genotypes. Therefore, genotypes may differ in their nutritional value for phytophages. The number of aphids attacked by the parasitoid also differed among genotypes and aphid numbers only partly accounted for this effect. Moreover, pupal development time of female parasitoids was affected by plant genotype. We found no differences in mortality, body size, or sex ratio of hatching wasps between genotypes of quackgrass. Development time of the larvae and larval weight of the predatory lacewings differed among genotypes, but not weight of pupae and adults. Generally, the proportion of the total variance explained by the plant genotype was smaller for parasitoids and predators than for aphids. Overall, our experiments indicated that the plant genotype affects tri‐trophic interactions, but also that the strength of these effects decreases along the food chain.     

The impact of habitat fragmentation on trophic interactions of the monophagous butterfly <Emphasis Type="Italic">Polyommatus coridon</Emphasis>

Theory predicts that habitat fragmentation, including reduced area and connectivity of suitable habitat, changes multitrophic interactions. Species at the bottom of trophic cascades (host plants) are expected to be less negatively affected than higher trophic levels, such as herbivores and their parasitoids or predators. Here we test this hypothesis regarding the effects of habitat area and connectivity in a trophic system with three levels: first with the population size of the larval food plant Hippocrepis comosa, next with the population density of the monophagous butterfly species Polyommatus coridon and finally with its larval parasitism rate. Our results show no evidence for negative effects of habitat fragmentation on the food plant or on parasitism rates, but population density of adult P. coridon was reduced with decreasing connectivity. We conclude that the highly specialized butterfly species is more affected by habitat fragmentation than its larval food plant because of its higher trophic position. However, the butterfly host species was also more affected than its parasitoids, presumably because of lower resource specialization of local parasitoids which also frequently occur in alternative hosts. Therefore, conservation efforts should focus first on the most specialized species of interaction networks and second on higher trophic levels.     

Floral diversity, parasitoids and hyperparasitoids – A laboratory approach

Adding floral resources to agro-ecosystems to improve biological control can enhance the survival, egg load, and parasitism rate of insect parasitoids. However, this may not always be the case because the herbivore may benefit from the added resource as much as, or more than the third-trophic level. In addition, the natural enemies of those in the third-trophic level may also derive improved fitness from the added resources. Both these processes will dampen trophic cascades, leading to less-effective biological control. In this study, the effect of adding different flowering plants on the longevity, egg load, aphid parasitism rates and hyperparasitism of Aphidius ervi Haliday (Hymenoptera: Braconidae) by its hyperparasitoid Dendrocerus aphidum Rondani (Hymenoptera: Megaspilidae) were investigated, using the pea aphid Acyrthosiphon pisum Harris (Homoptera: Aphididae) as the herbivore. Parasitoids exposed to buckwheat survived, on average, between four to five times as long as those in the control (water) and those in phacelia, alyssum and coriander treatments survived three to four times as long. Hyperparasitoids exposed to buckwheat survived five to six times as long as those in the control and three to five times longer with the other plants compared with the control. Almost all flower species significantly increased parasitoid and hyperparasitoid egg loads and the number of parasitised aphids and parasitised mummies compared with control. Understanding the factors influencing the dynamics of multitrophic interactions involving flowering plants, herbivores, parasitoids and hyperparasitoids is a fertile area for future research. One of the most challenging areas in contemporary ecology concerns the relative importance of different types of biodiversity mediating trophic interactions and thereby influencing the structure of communities and food webs. This paper begins to explore this using an experimental, laboratory-based approach.     

The role of host plant species in the phenotypic differentiation of sympatric populations of Aleiodes nolophanae and Cotesia marginiventris

The ecology of parasitoids is strongly influenced by their host plant species. Parasitoid fitness can be affected by a variety of plant traits that could promote phenotypic differentiation among populations of parasitoids. Generalist parasitoids are expected to be more affected by plant traits (e.g., plant defensive traits) than specialist parasitoids. Data are presented on phenotypic differences of two braconid parasitoid wasps ovipositing on the same insect host species on two different host plant species. Adult mass, adult longevity, and percent parasitism are compared for the generalist parasitoid Cotesia marginiventris Cresson and the specialist parasitoid Aleiodes nolophanae Ashmead (both Hymenoptera: Braconidae) emerging from green cloverworms, Hypena scabra Fabricius (Lepidoptera: Noctuidae), feeding on two host plant species, alfalfa (Medicago sativa L.) and soybean (Glycine max L. Merr.) (both Fabaceae), at three locations. Specialist wasps that parasitized the green cloverworm on alfalfa had a significantly larger mass than the ones that parasitized the green cloverworm on soybean at the three study sites. Generalist wasps that parasitized green cloverworms on alfalfa had a larger mass than wasps parasitizing green cloverworms on soybean only at one of the study sites (i.e., Prince George's County, MD, USA). Similarly, both specialist and generalist wasps lived longer when parasitizing green cloverworms on alfalfa than when parasitizing them on soybean at only one of the study sites (i.e., Prince George's County). In Prince George's County, percent parasitism on alfalfa by the specialist parasitoid was higher than on soybean for three consecutive years and percent parasitism by the generalist parasitoid was the same on alfalfa and soybean every year. Thus, phenotypic differences among populations associated with different host plant species vary geographically (i.e., parasitoid phenotype associated with different host plant species differ at some sites while it is the same at other sites). The implications of geographic variation for biological control are discussed.     

Life history plasticity and fitness in a caddisfly in response to proximate cues of pond-drying

The majority of plants are involved in symbioses with arbuscular mycorrhizal fungi (AMF), and these associations are known to have a strong influence on the performance of both plants and insect herbivores. Little is known about the impact of AMF on complex trophic chains, although such effects are conceivable. In a greenhouse study we examined the effects of two AMF species, Glomus intraradices and G. mosseae on trophic interactions between the grass Phleum pratense, the aphid Rhopalosiphum padi, and the parasitic wasp Aphidius rhopalosiphi. Inoculation with AMF in our study system generally enhanced plant biomass (+5.2%) and decreased aphid population growth (−47%), but there were no fungal species-specific effects. When plants were infested with G. intraradices, the rate of parasitism in aphids increased by 140% relative to the G. mosseae and control treatment. When plants were associated with AMF, the developmental time of the parasitoids decreased by 4.3% and weight at eclosion increased by 23.8%. There were no clear effects of AMF on the concentration of nitrogen and phosphorus in plant foliage. Our study demonstrates that the effects of AMF go beyond a simple amelioration of the plants’ nutritional status and involve rather more complex species-specific cascading effects of AMF in the food chain that have a strong impact not only on the performance of plants but also on higher trophic levels, such as herbivores and parasitoids.     

ECOLOGICAL VERSUS PHYLOGENETIC DETERMINANTS OF TROPHIC ASSOCIATIONS IN A PLANT–LEAFMINER–PARASITOID FOOD WEB

Specialized trophic interactions in plant–herbivore–parasitoid food webs can spur “bottom–up” diversification if speciation in plants leads to host‐shift driven divergence in insect herbivores, and if the effect then cascades up to the third trophic level. Conversely, parasitoids that search for victims on certain plant taxa may trigger “top–down” diversification by pushing herbivores into “enemy‐free space” on novel hosts. We used phylogenetic regression methods to compare the relative importance of ecology versus phylogeny on associations between Heterarthrinae leafmining sawflies and their parasitoids. We found that: (1) the origin of leafmining led to escape from most parasitoids attacking external‐feeding sawflies; (2) the current enemies mainly consist of generalists that are shared with other leafmining taxa, and of more specialized lineages that may have diversified by shifting among heterarthrines; and (3) parasitoid–leafminer associations are influenced more by the phylogeny of the miners’ host plants than by relationships among miner species. Our results suggest that vertical diversifying forces have a significant—but not ubiquitous—role in speciation: many of the parasitoids have remained polyphagous despite niche diversification in the miners, and heterarthrine host shifts also seem to be strongly affected by host availability.     

Trophic cascades initiated by fungal plant endosymbionts impair reproductive performance of parasitoids in the second generation

Variation in plant quality can transmit up the food chain and may affect herbivores and their antagonists in the same direction. Fungal endosymbionts of grasses change the resource quality by producing toxins. We used an aphid-parasitoid model system to explore how endophyte effects cascade up the food chain and influence individual parasitoid performance. We show that the presence of an endophyte in the grass Lolium perenne has a much stronger negative impact on the performance of the parasitoid Aphidius ervi than on its aphid host Metopolophium festucae. Although the presence of endophytes did not influence the parasitism rate of endophyte-naïve parasitoids or their offspring’s survival to adulthood, most parasitoids developing within aphids from endophyte-infected plants did not reproduce at all. This indicates a delayed but very strong effect of endophytes on parasitoid performance, which should ultimately affect plant performance negatively by releasing endophyte-tolerant herbivores from top-down limitations.     

Plant‐mediated indirect effects and the persistence of parasitoid–herbivore communities

We have examined the effects of herbivore diversity on parasitoid community persistence and stability, mediated by nonspecific information from herbivore‐infested plants. First, we investigated host location and patch time allocation in the parasitoid Cotesia glomerata in environments where host and/or nonhost herbivores were present on Brassica oleracea leaves. Parasitoids were attracted by infochemicals from leaves containing nonhost herbivores. They spent considerable amounts of time on such leaves. Thus, when information from the plant is indistinct, herbivore diversity is likely to weaken interaction strengths between parasitoids and hosts. In four B. oleracea fields, all plants contained herbivores, often two or more species. We modelled parasitoid–herbivore communities increasing in complexity, based on our experiments and field data. Increasing herbivore diversity promoted the persistence of parasitoid communities. However, at a higher threshold of herbivore diversity, parasitoids became extinct due to insufficient parasitism rates. Thus, diversity can potentially drive both persistence and extinctions.     

Distribution and colonisation ability of three parasitoids and their herbivorous host in a fragmented landscape

Habitat fragmentation can disrupt communities of interacting species even if only some of the species are directly affected by fragmentation. For instance, if parasitoids disperse less well than their herbivorous hosts, habitat fragmentation may lead to higher herbivory in isolated plant patches due to the absence of the third trophic level. Community-level studies suggest that parasitoids tend to have limited dispersal abilities, on the order of tens of metres, much smaller than that of their hosts, while species-oriented studies document dispersal by parasitoids on the scale of kilometres. In this study the distribution patterns of three parasitoid species with different life histories and their moth host, Hadena bicruris, a specialist herbivore of Silene latifolia, were compared in a large-scale network of natural fragmented plant patches along the rivers Rhine and Waal in the Netherlands. We examined how patch size and isolation affect the presence of each species. Additionally, experimental plots were used to study the colonisation abilities of the species at different distances from source populations.In the natural plant patches the presence of the herbivore and two of the parasitoids, the gregarious specialist Microplitis tristis and the gregarious generalist Bracon variator were not affected by patch isolation at the scale of the study, while the solitary specialist Eurylabus tristis was. In contrast to the herbivore, the presence of all parasitoid species declined with plant patch size. The colonisation experiment confirmed that the herbivore and M. tristis are good dispersers, able to travel at least 2 km within a season. B. variator showed intermediate colonisation ability and E. tristis showed very limited colonisation ability at this spatial scale. Characteristics of parasitoid species that may contribute to differences in their dispersal abilities are discussed.     

Multitrophic web of insects associated with <Emphasis Type="Italic">Piptadenia gonoacantha</Emphasis> (Mart.) Macbr. (Fabaceae) and their relationship with resource traits

We describe for the first time the food web of insects associated with fruits and seed of Piptadenia gonoacantha (Fabaceae), and analyze their relationships with resource traits, such as biomass and fruit area. A total of 440 fruits of P. Gonoacantha were sampled in the city of Lavras, Minas Gerais, Brazil. We found twenty-one species of insects distributed in three trophic levels. The most widely sampled species was Acanthoscelides clitellarius (Coleoptera, Chrysomelidae, Bruchinae), the main consumer species of seeds. It was also verified the presence of Lepidoptera larvae consuming both seeds and the internal fruit tissue. Other species of herbivorous insects were found in low numbers. The food web was subdivided into one sub-web of 10 parasitoid species and one hyperparasitoid species associated to A. clitellarius and another one sub-web of four parasitoid species associated with Lepidoptera. For the parasitism rates, we obtained the following: 19.11% for the total food web, 17.93% for the A. clitellarius parasitism, and 36% for the Lepidoptera parasitism. The resource traits had influence on the oviposition behavior of A. clitellarius, where fruits with larger area showed more eggs of this species. Fruits with higher biomass showed greater abundance and richness of insects as well as more interactions. Seeds with higher biomass were more often used by herbivorous insects. The larval forms of Lepidoptera caused the greatest damage in seed biomass among herbivores. Seeds with parasitoids did not show a significant difference in biomass when compared to predated seeds.     

Organic and conventional fertilizer effects on a tritrophic interaction: parasitism,performance and preference of Cotesia vestalis

Interest in sustainable farming methods that rely on alternatives to conventional synthetic fertilizers and pesticides is increasing. Sustainable farming methods often utilize natural populations of predatory and parasitic species to control populations of herbivores, which may be potential pest species. We investigated the effects of several types of fertilizer, including those typical of sustainable and conventional farming systems, on the interaction between a herbivore and parasitoid. The effects of fertilizer type on percentage parasitism, parasitoid performance, parasitoid attack behaviour and responses to plant volatiles were examined using a model Brassica system, consisting of Brassica oleracea var capitata, Plutella xylostella (Lepidoptera) larvae and Cotesia vestalis (parasitoid). Percentage parasitism was greatest for P. xylostella larvae feeding on plants that had received either a synthetic ammonium nitrate fertilizer or were unfertilized, in comparison to those receiving a composite fertilizer containing hoof and horn. Parasitism was intermediate on plants fertilized with an organically produced animal manure. Male parasitoid tibia length showed the same pattern as percentage parasitism, an indication that offspring performance was maximized on the treatments preferred by female parasitoids for oviposition. Percentage parasitism and parasitoid size were not correlated with foliar nitrogen concentration. The parasitoids did not discriminate between hosts feeding on plants in the four fertilizer treatments in parasitoid behaviour assays, but showed a preference for unfertilized plants in olfactometer experiments. The percentage parasitism and tibia length results provide support for the preference–performance hypothesis.     

Parasitoid pressure and the radiation of a gallforming group (Cecidomyiidae: Asphondylia spp.) on creosote bush (Larrea tridentata)

Summary We tested the Enemy Impact Hypothesis, which predicts that communities of one tropic level are organized by the tropic level above. In the case of gallforming insect communities, the hypothesis predicts that gall morphology will diverge, minimizing the number of parasitoids shared among species. We used the monophyletic group of gallforming cecidomyiids (Asphondylia spp.) on creosote bush (Larrea tridentata) to test this hypothesis, predicting that species with thicker gall walls should exclude species of parasitoids with shorter ovipositors and have lower levels of parasitism. Of 17 parasitoid species reared from Asphondylia galls on creosote bush, 9 accounted for over 98% of parasitism. Seven of these 9 species had ovipositors long enough to penetrate 10 of 13 gall morphs measured. There was no significant relationship between gall wall thickness and number of associated parasitoid species (r ²=0.01, P>0.05, n=13). There was no relationship between gall wall thickness and types of parasitoid species colonizing galls: parasitoids with the shortest ovipositors colonized all types of gall morphs and were dominant members of the parasitoid assemblages in galls with the thickest walls. Ultimately, there were no significant differences in percent parasitism among Asphondylia species, regardless of gall wall thickness. We found no difference in numbers of associated parasitoids or percent parasitism in galls with different textures (e.g. hairy versus smooth), different locations on the plant or different phenologies. Our results suggest that enemy impact has not influenced the diversity of this gall community. Gall wall thickness, phenology, location on the plant and surface structure do not appear to influence the distribution of parasitoid species. Other explanations are offered to account for diversity in gall morphology among these species.     

The spitting image of plant defenses: Effects of plant secondary chemistry on the efficacy of caterpillar regurgitant as an anti‐predator defense

In the arms race between plants, herbivores, and their natural enemies, specialized herbivores may use plant defenses for their own benefit, and variation in plant traits may affect the benefits that herbivores derive from these defenses. Pieris brassicae is a specialist herbivore of plants containing glucosinolates, a specific class of defensive secondary metabolites. Caterpillars of P. brassicae are known to actively spit on attacking natural enemies, including their main parasitoid, the braconid wasp Cotesia glomerata. Here, we tested the hypothesis that variation in the secondary metabolites of host plants affects the efficacy of caterpillar regurgitant as an anti‐predator defense. Using a total of 10 host plants with different glucosinolate profiles, we first studied natural regurgitation events of caterpillars on parasitoids. We then studied manual applications of water or regurgitant on parasitoids during parasitization events. Results from natural regurgitation events revealed that parasitoids spent more time grooming after attack when foraging on radish and nasturtium than on Brassica spp., and when the regurgitant came in contact with the wings rather than any other body part. Results from manual applications of regurgitant showed that all parameters of parasitoid behavior (initial attack duration, attack interruption, grooming time, and likelihood of a second attack) were more affected when regurgitant was applied rather than water. The proportion of parasitoids re‐attacking a caterpillar within 15 min was the lowest when regurgitant originated from radish‐fed caterpillars. However, we found no correlation between glucosinolate content and regurgitant effects, and parasitoid behavior was equally affected when regurgitant originated from a glucosinolate‐deficient Arabidopsis thaliana mutant line. In conclusion, host plant affects to a certain extent the efficacy of spit from P. brassicae caterpillars as a defense against parasitoids, but this is not due to glucosinolate content. The nature of the defensive compounds present in the spit remains to be determined, and the ecological relevance of this anti‐predator defense needs to be further evaluated in the field.     

Tri-trophic consequences of UV-B exposure: plants,herbivores and parasitoids

In this paper we demonstrate a UV-B-mediated link between host plants, herbivores and their parasitoids, using a model system consisting of a host plant Brassica oleracea, a herbivore Plutella xylostella and its parasitoid Cotesia plutellae. Ultraviolet-B radiation (UV-B) is a potent elicitor of a variety of changes in the chemistry, morphology and physiology of plants and animals. Recent studies have demonstrated that common signals, such as jasmonic acid (JA), play important roles in the mechanisms by which plants respond to UV-B and to damage by herbivores. Plant responses elicited by UV-B radiation can affect the choices of ovipositing female insects and the fitness of their offspring. This leads to the prediction that, in plants, the changes induced as a consequence of UV damage will be similar to those elicited in response to insect damage, including knock-on effects upon the next trophic level, predators. In our trials female P. xylostella oviposited preferentially on host plants grown in depleted UV-B conditions, while their larvae preferred to feed on tissues from UV-depleted regimes over those from UV-supplemented ones. Larval feeding patterns on UV-supplemented tissues met the predictions of models which propose that induced defences in plants should disperse herbivory; feeding scars were significantly smaller and more numerous – though not significantly so – than those on host plant leaves grown in UV-depleted conditions. Most importantly, female parasitoids also showed a clear pattern of preference when given the choice between host plants and attendant larvae from the different UV regimes; however, in the case of the female parasitoids, the choice was in favour of potential hosts foraging on UV-supplemented tissues. This study demonstrates the potential for UV-B to elicit a variety of interactions between trophic levels, most likely mediated through effects upon host plant chemistry.     

Does a Specialist Parasitoid Adapt to its Host on a New Host Plant?

The host plant expansion of a diamondback moth, Plutella xylostella (L.) (DBM) strain to snowpea (Pisum sativum L.) raised the question whether a specialist parasitoid Diadegma semiclausum (DS) could be conditioned to locate and parasitize its host on the new host plant. In a specialist parasitoid a behavioural change towards a plant outside the normal host plant range of its host due to developmental experience is not expected. The responsive behaviour, parasitism rates and fitness of three subsequent DS generations were investigated on the snowpea-strain of DBM. After three generations of DS on the pea 62.5% of females chose an DBM-infested pea plant over DBM infested cabbage. Only 16.4% of cabbage-reared DS was attracted to infested pea. Rearing of the parasitoid in host larvae on peas significantly increased the number of larvae parasitized on this host plant in the first generation; however, there was no further increase in generations 2 and 3. Larval mortality was similar for all parasitoid/DBM combinations on both host plants, but significantly higher mortality occurred in parasitoid pupae from peas. Development time of the parasitoid was slightly prolonged on the pea strain of DBM. The number of females produced by parasitoids reared on the pea strain of DBM was significantly reduced as compared to D. semiclausum reared on the cabbage strain on both host strains. Results show that DS has the potential to change its responsive behaviour in order to locate its host on a new host plant. According to the current view, a specialist parasitoid is not expected to change its reaction to a plant outside the normal host plant range of its host. Within 3 generations, responsive behaviour towards snowpea could be increased. However, fitness trade-offs, especially an extreme shift in sex ratio to males reduced reproductive success.     

The role of natural enemy guilds in Aphis glycines suppression

Generalist natural enemy guilds are increasingly recognized as important sources of mortality for invasive agricultural pests. However, the net contribution of different species to pest suppression is conditioned by their biology and interspecific interactions. The soybean aphid, Aphis glycines (Hemiptera: Aphididae), is widely attacked by generalist predators, but the relative impacts of different natural enemy guilds remains poorly understood. Moreover, low levels of A. glycines parasitism suggest that resident parasitoids may be limited through intraguild predation. During 2004 and 2005, we conducted field experiments to test the impact of different guilds of natural enemies on A. glycines. We contrasted aphid abundance on field cages with ambient levels of small predators (primarily Orius insidiosus) and parasitoids (primarily Braconidae), sham cages and open controls exposed to large predators (primarily coccinellids), and cages excluding all natural enemies. We observed strong aphid suppression (86- to 36-fold reduction) in treatments exposed to coccinellids, but only minor reduction due to small predators and parasitoids, with aphids reaching rapidly economic injury levels when coccinellids were excluded. Three species of resident parasitoids were found attacking A. glycines at very low levels (<1% parasitism), with no evidence that intraguild predation by coccinellids attenuated parasitoid impacts. At the plant level, coccinellid impacts resulted in a trophic cascade that restored soybean biomass and yield, whereas small natural enemies provided only minor protection against yield loss. Our results indicate that within the assemblage of A. glycines natural enemies in Michigan, coccinellids are critical to maintain aphids below economic injury levels.     

Plant species variation in bottom‐up effects across three trophic levels: a test of traits and mechanisms

1. An increasing number of studies have addressed the mechanisms by which plant inter‐specific variation influence interactions at higher trophic levels, but little is known about the underlying plant traits driving these dynamics. 2. Here we investigated the effects of host plant species on herbivore‐parasitoid interactions and the underlying traits driving such effects. For this, we measured the abundance of seed‐eating bruchids and their parasitoids across seven sympatric populations of the bean species Phaseolus coccineus and Phaseolus vulgaris in Central Mexico. To investigate the mechanisms underlying differences between bean species in bruchid‐parasitoid interactions, we carried out two laboratory experiments to test whether bruchid and parasitoid performance differed between plant species. We also measured seed size and phenolic compounds to investigate if seed traits mediate bruchid‐parasitoid interactions by influencing herbivore susceptibility or resistance to parasitoids. 3. Field surveys revealed that the rate of parasitoid recruitment to bruchids was significantly higher on P. vulgaris than on P. coccineus. Subsequent laboratory bioassays indicated that bruchids developed more slowly and exhibited lower fitness on P. vulgaris seeds than on P. coccineus seeds. Accordingly, we found that bean species differed in seed size, with P. vulgaris having smaller (less nutritious) seeds, which explains why bruchid development was slower on this plant species. 4. These results provide a mechanism for why bruchids exhibited higher parasitism rates on seeds of P. vulgaris in the field which could be due to Slow‐Growth/High‐Mortality effects, a smaller physical refuge provided by the seed, or both factors. The roles of these mechanisms remain inconclusive without further study.     

Serratia marcescens as a rapid indicator of Microctonus hyperodae oviposition activity in Listronotus maculicollis and potential application of the technique to host-specificity testing

Listronotus maculicollis (Dietz) (Coleoptera: Curculionidae) is a potential novel host of the braconid parasitoid Microctonus hyperodae Loan, but initial studies have shown that levels of parasitism are lower than in the natural host L. bonariensis (Kuschel). A novel bacterial indicator test was used to determine whether the lower level of parasitism was due to behavioural factors, lack of oviposition, or host resistance. The incidence of ovipositor penetration by the parasitoid M. hyperodae into adult L. maculicollis was measured by immersing the ovipositor of the parasitoid in the facultative pathogen, Serratia marcescens Bizio. Adult weevils were then exposed to parasitoids for up to 72 h and rapid mortality used as an indicator of oviposition penetration. Survival was assessed after six days and surviving weevils were dissected and examined for parasitoid larvae. Mortality among L. maculicolis exposed to parasitoids treated with S. marcescens was significantly higher (P<0.001) than the controls but significantly lower (P<0.001) than in the natural host, L. bonariensis. Dissection of weevils exposed to uncontaminated parasitoids revealed that parasitism in L. maculicolis was significantly (P<0.001) less than parasitism in L. bonariensis. Serratia marcescens-induced mortality plus parasitism of surviving weevils in the parasitoid plus bacteria treatments produced a similar overall effect. Application of bacteria to the parasitoid ovipositor provided a rapid, simple test for ovipositor penetration, which shows potential for separation of behavioural and physiological defence mechanisms in parasitoid/host range studies.