Food web associations and effect of trophic resources and environmental factors on parasitoids expanding their host range into non‐native hosts

Trophic interactions and environmental conditions determine the structure of food webs and the host expansion of parasitoids into novel insect hosts. In this study, we investigate plant–insect–parasitoid food web interactions, specifically the effect of trophic resources and environmental factors on the presence of the parasitoids expanding their host range after the invasion of Chrysodeixis chalcites (Esper) (Lepidoptera: Noctuidae). We also consider potential candidates for biological control of this non‐native pest. A survey of larval stages of Plusiinae (Lepidoptera: Noctuidae) and their larval parasitoids was conducted in field and vegetable greenhouse crops in 2009 and 2010 in various locations of Essex and Chatham‐Kent counties in Ontario, Canada. Twenty‐one plant–host insect–host parasitoid associations were observed among Trichoplusia ni (Hübner) (Lepidoptera: Noctuidae), C. chalcites, and larval parasitoids in three trophic levels of interaction. Chrysodeixis chalcites, an old‐world species that had just arrived in the region, was the most common in our samples. The larval parasitoids Campoletis sonorensis (Cameron) (Hymenoptera: Ichneumonidae), Cotesia vanessae (Reinhard), Cotesia sp., Microplitis alaskensis (Ashmead), and Meteorus rubens (Nees) (all Hymenoptera: Braconidae) expanded their host range into C. chalcites changing the structure of the food web. Copidosoma floridanum (Ashmead) (Hymenoptera: Encyrtidae) was the most common parasitoid of T. ni that was not found in the invasive species. Plant species, host abundance, and agro‐ecosystem were the most common predictors for the presence of the parasitoids expanding their host range into C. chalcites. Our results indicate that C. sonorensis, C. vanessae, and C. floridanum should be evaluated for their potential use in biological control of C. chalcites and T. ni.     

Noncrop flowering plants restore top‐down herbivore control in agricultural fields

Herbivore populations are regulated by bottom‐up control through food availability and quality and by top‐down control through natural enemies. Intensive agricultural monocultures provide abundant food to specialized herbivores and at the same time negatively impact natural enemies because monocultures are depauperate in carbohydrate food sources required by many natural enemies. As a consequence, herbivores are released from both types of control. Diversifying intensive cropping systems with flowering plants that provide nutritional resources to natural enemies may enhance top‐down control and contribute to natural herbivore regulation. We analyzed how noncrop flowering plants planted as “companion plants” inside cabbage (Brassica oleracea) fields and as margins along the fields affect the plant–herbivore–parasitoid–predator food web. We combined molecular analyses quantifying parasitism of herbivore eggs and larvae with molecular predator gut content analysis and a comprehensive predator community assessment. Planting cornflowers (Centaurea cynanus), which have been shown to attract and selectively benefit Microplitis mediator, a larval parasitoid of the cabbage moth Mamestra brassicae, between the cabbage heads shifted the balance between trophic levels. Companion plants significantly increased parasitism of herbivores by larval parasitoids and predation on herbivore eggs. They furthermore significantly affected predator species richness. These effects were present despite the different treatments being close relative to the parasitoids’ mobility. These findings demonstrate that habitat manipulation can restore top‐down herbivore control in intensive crops if the right resources are added. This is important because increased natural control reduces the need for pesticide input in intensive agricultural settings, with cascading positive effects on general biodiversity and the environment. Companion plants thus increase biodiversity both directly, by introducing new habitats and resources for other species, and indirectly by reducing mortality of nontarget species due to pesticides.     

Invasive insect herbivores as disrupters of chemically-mediated tritrophic interactions: effects of herbivore density and parasitoid learning

Invasive insect herbivores have the potential to interfere with native multitrophic interactions by affecting the chemical cues emitted by plants and disrupting the attraction of natural enemies mediated by herbivore-induced plant volatiles (HIPVs). In a previous study, we found that the presence of the exotic herbivore Spodoptera littoralis on Brassica rapa plants infested by the native herbivore Pieris brassicae makes these dually-infested plants unattractive to the main parasitoid of P. brassicae, the braconid wasp Cotesia glomerata. Here we show that this interference by S. littoralis is strongly dependent on the relative densities of the two herbivores. Parasitoids were only deterred by dually-infested plants when there were more S. littoralis larvae than P. brassicae larvae on a plant. Furthermore, the blend of HIPVs emitted by dually-infested plants differed the most from HIPVs emitted by Pieris-infested plants when S. littoralis density exceeded P. brassicae density. We further found that associative learning by the parasitoid affected its preferences: attraction to dually-infested plants increased after parasitoids were presented a P. brassicae caterpillar (rewarding experience) in presence of the odor of a dually-infested plant, but not when presented a S. littoralis caterpillar (non-rewarding experience). A non-rewarding experience prior to the bioassays resulted in a general decrease in parasitoid motivation to respond to plant odors. We conclude that herbivore density and associative learning may play an important role in the foraging behavior of natural enemies in communities, and such effects should not be overlooked when investigating the ecological impact of exotic species on native food webs.     

Trophic consequences of a biological invasion: do plant invasions increase predator abundance?

As invasive species become integrated into existing communities, they engage in a wide variety of trophic interactions with other community members. Many of these interactions are direct (e.g. predator–prey interactions or interference competition), but invasive species also can affect native community members indirectly, by influencing the abundances of intermediary species in trophic webs. Observational studies suggest that invasive plant species affect herbivorous arthropod communities and that these effects may flow up trophic webs to influence the abundance of predators. However, few studies have experimentally manipulated the presence of invasive plants to quantify the effects of plant invasion on higher trophic levels. Here, I use comparisons across sites that have or have not been invaded by the invasive plant Medicago polymorpha, combined with experimental removals of Medicago and insect herbivores, to investigate how a plant invasion affects the abundance of predators. Both manipulative and observational experiments showed that Medicago increased the abundance of the exotic herbivore Hypera and predatory spiders, suggesting positive bottom–up effects of plant invasions on higher trophic levels. Path analyses conducted on data from natural habitats revealed that Medicago primarily increased spider abundance through herbivore‐mediated indirect pathways. Specifically, Medicago density was positively correlated with the abundance of the dominant herbivore Hypera, and increased Hypera densities were correlated with increased spider abundance. Smaller‐scale experimental studies confirmed that Medicago may increase spider abundance through herbivore‐mediated indirect pathways, but also showed that the effects of Medicago varied across sites, including having no effect or having direct effects on spider abundance. If effects of invasive species commonly flow through trophic webs, then invasive species have the potential to affect numerous species throughout the community, especially those species whose dynamics are tightly connected to highly‐impacted community members through trophic linkages.     

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.     

An exotic parasitoid provides an invasional lifeline for native parasitoids

The introduction of an exotic species may alter food webs within the ecosystem and significantly affect the biodiversity of indigenous species at different trophic levels. It has been postulated that recent introduction of the brown marmorated stinkbug (Halyomorpha halys (Stål)) represents an evolutionary trap for native parasitoids, as they accept H. halys egg masses as a host but produce no viable progeny. Interspecific interactions between European egg parasitoid, Trissolcus cultratus (Mayr), and an Asian parasitoid, Trissolcus japonicus (Ashmead), were assessed by providing egg masses to T. cultratus at various time intervals following the initial parasitization by T. japonicus. The suitability of the host for the parasitoid development was re‐assessed by providing T. cultratus with fresh and frozen egg masses of various ages. The likelihood of T. cultratus being able to attack previously parasitized egg masses was determined by assessing the duration of egg mass guarding behavior by T. japonicus following parasitization. The results of experiments examining the interspecific interactions between a native European egg parasitoid, T. cultratus, and an Asian parasitoid, T. japonicus (a candidate for the biological control of H. halys), showed that the native species can act as facultative hyperparasitoid of the exotic one. Although this is only possible during certain stages of T. japonicus development, the presence of the introduced parasitoid may reduce the impact of the evolutionary trap for indigenous parasitoid species. There is a possibility that the occurrence of facultative hyperparasitism between scelionid parasitoids associated with stinkbugs is common. This resulting intraguild predation could promote conservation and stabilization of natural communities by impacting the diversity and population dynamics of native stinkbugs and their parasitoids (e.g., by allowing native parasitoids to avoid wasting reproductive effort on unsuitable hosts), or reduce success of biological control programs (e.g., by reducing the population size of the exotic parasitoids).     

Field collection of egg parasitoids of Pentatomidae and Scutelleridae in Northwest Italy and their efficacy in parasitizing Halyomorpha halys under laboratory conditions

The invasion of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) has caused severe economic damage in crops in North America and Europe, motivating research to identify its natural enemies, both in native and invaded areas. In its Asian native range, the main natural enemies are egg parasitoids, among which the most effective are Trissolcus japonicus (Ashmead) and Trissolcus mitsukurii (Ashmead) (Hymenoptera: Scelionidae) in China and Japan, respectively. In Europe, biology, host range, and impact of most native scelionid species are not well‐known. The present study aimed to investigate (1) presence and abundance of scelionid species that parasitize native Pentatomidae and Scutelleridae eggs in Northwest Italy, and (2) their ability to develop on H. halys eggs. During 4‐year field surveys, egg masses were collected and reared until bug nymph or adult parasitoid emergence. Then, the obtained scelionid females were tested for their ability to parasitize H. halys eggs in laboratory no‐choice experiments. Egg masses of all collected bug species were parasitized, and Telenomus spp. (Hymenoptera: Scelionidae), Trissolcus belenus (Walker), and Anastatus bifasciatus (Geoffroy) (Hymenoptera: Eupelmidae) were the most common parasitoids. In the laboratory, Trissolcus kozlovi Rjachovskij was the only species to significantly produce offspring from fresh H. halys eggs, whereas all tested Trissolcus species significantly induced host egg abortion (non‐reproductive effects). This study provides knowledge of the parasitoid species associated with native bugs, and represents a starting point to investigate the intricate interactions between native and exotic parasitoids recently found in northern Italy. These egg parasitoids could potentially be effective biocontrol agents of H. halys.     

A tritrophic approach to the preference–performance hypothesis involving an exotic and a native plant

Exotic plants often generate physical and chemical changes in native plant communities where they become established. A major challenge is to understand how novel plants may affect trophic interactions in their new habitats, and how native herbivores and their natural enemies might respond to them. We compared the oviposition preference and offspring performance of the crucifer specialist, Pieris brassicae, on an exotic plant, Bunias orientalis, and on a related native plant, Sinapis arvensis. Additionally, we studied the response of the parasitoid, Cotesia glomerata to herbivore-induced plant volatiles (HIPV) and determined the volatile blend composition to elucidate which compound(s) might be involved in parasitoid attraction. On both host plants we also compared the parasitism rate of P. brassicae by C. glomerata. Female butterflies preferred to oviposit on the native plant and their offspring survival and performance was higher on the native plant compared to the exotic. Although, headspace analysis revealed qualitative and quantitative differences in the volatile blends of both plant species, C. glomerata did not discriminate between the HIPV blends in flight-tent bioassays. Nevertheless, parasitism rate of P. brassicae larvae was higher on the native plant under semi-field conditions. Overall, P. brassicae oviposition preference may be more influenced by bottom-up effects of the host plant on larval performance than by top-down pressure exerted by its parasitoid. The potential for dietary breadth expansion of P. brassicae to include the exotic B. orientalis and the role of top-down processes played by parasitoids in shaping herbivore host shifts are further discussed.     

Fungal Phyllosphere Communities are Altered by Indirect Interactions Among Trophic Levels

Trophic interactions involving predators, herbivores, and plants have been described in terrestrial systems. However, there is almost no information on the effect of trophic interactions on microbial phyllosphere community abundance, diversity, or structure. In this study, the interaction between a parasitoid, an insect herbivore, and the fungal phyllosphere community is examined. Parasitoid wasps have an indirect negative impact on fungal community diversity. On the citrus phyllosphere, the exotic wasp species, Amitus hesperidum and Encarsia opulenta, may parasitize the citrus blackfly (Aleurocanthus woglumi). If parasitism levels are low, the blackfly may produce significant amounts of honeydew secretions on the surface of the leaf. Honeydew deposition provides a carbon-rich substrate for the development of fungal growth persisting as sooty mold on the leaves. Leaves from sooty mold-infested grapefruit (Citrus paradisi) trees were collected from multiple orchards in south Texas. The effect of different levels of exotic parasite activity, citrus blackfly, and sooty mold infestation on phyllosphere mycobiota community structure and diversity was examined. Our results suggest the presence of the parasitoid may lead to a top–down trophic cascade affecting phyllosphere fungal community diversity and structure. Additionally, persistent sooty mold deposits that have classically been referred to as Capnodium citri (and related asexual morphological forms) actually comprise a myriad of fungal species including many saprophytes and potential fruit and foliar pathogens of citrus.     

Predators,fire or resources: What drives the distribution of herbivores in fragmented mesic forests?

Trophic interactions and disturbance events can shape the structure and function of ecosystems. However, the effects of drivers such as predation, fire and climatic variables on species distributions are rarely considered concurrently. We used a replicated landscape‐scale predator management experiment to compare the effects of red fox Vulpes vulpes control, time‐since‐fire, vegetation type and other environmental variables on native herbivore distributions. Occurrence data for four native herbivores and an invasive predator – the red fox – were collected from 240 sites across three baited (for lethal fox control) and three unbaited forest blocks (4659–9750 ha) in south‐western Victoria, Australia, and used to build species distribution models. The herbivore taxa were as follows: red‐necked wallaby Macropus rufogriseus, black wallaby Wallabia bicolour, grey kangaroo Macropus fuligenosus and Macropus giganteus and common brushtail possum Trichosurus vulpecula. Fox control and fire had little effect on herbivore occurrence, despite the literature suggesting it can influence abundance, while climate, proximity to farmland and topography were more influential. This may be because the region’s high productivity and agricultural pastures subsidise food resources for both predators and prey within the forest blocks and so dampen trophic interactions. Alternatively, these drivers may affect herbivore abundance, but not herbivore occurrence. Understanding the drivers of herbivore distributions is an important step in predicting the effects of herbivory on other species, particularly after management interventions such as predator control and prescribed burns.     

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.     

Can Invasive Species Enhance Competitive Ability and Restoration Potential in Native Grass Populations?

Native plant individuals often persist within communities dominated by exotics but the influence of this exposure on native populations is poorly understood. Selection for traits contributing to competitive ability may lead to native plant populations that are more tolerant of the presence of exotic invaders. In this way, long‐term coexistence with an exotic may confer competitive advantages to remnant (experienced) native populations and be potentially beneficial to restoration. In past studies we have documented genetic differentiation within native grass populations exposed to the exotic invader Russian knapweed (Acroptilon repens). Here, we examine populations of a cool‐season grass, needle‐and‐thread (Hesperostipa comata [Trin. & Rupr.]) and a warm season, alkali sacaton (Sporobolus airoides [Torr.]) collected from Russian knapweed‐invaded sites and adjacent noninvaded sites to assess their relative competitive ability against a novel exotic neighbor, Canada thistle (Cirsium arvense). Experienced S. airoides (from within A. repens invasions) appear to better tolerate (accumulate biomass, leaf nitrogen content, and to initiate new tillers) the presence of a novel competitor (C. arvense). Experienced and inexperienced H. comata genets differ in their response to the presence of C. arvense. Relative neighbor effects of native grasses on C. arvense were generally greater from experienced grasses. The ability to compete with novel neighbors may be driven by general competitive traits rather than species‐specific coevolutionary trajectories. Irrespective of competitive mechanisms, the conservation of native species populations within weed invasions may provide an important restoration tool by retaining unique components of native gene pools selected by competitive interactions with exotics.     

Do native and invasive herbivores have an effect on Brassica rapa pollination?

• Mutualistic (e.g. pollination) and antagonistic (e.g. herbivory) plant–insect interactions shape levels of plant fitness and can have interactive effects.
• By using experimental plots of Brassica rapa plants infested with generalist (Mamestra brassicae) and specialised (Pieris brassicae) native herbivores and with a generalist invasive (Spodoptera littoralis) herbivore, we estimated both pollen movement among treatments and the visiting behaviour of honeybees versus other wild pollinators.
• Overall, we found that herbivory has weak effects on plant pollen export, either in terms of inter‐treatment movements or of dispersion distance. Plants infested with the native specialised herbivore tend to export less pollen to other plants with the same treatment. Other wild pollinators preferentially visit non‐infested plants that differ from those of honeybees, which showed no preferences. Honeybees and other wild pollinators also showed different behaviours on plants infested with different herbivores, with the former tending to avoid revisiting the same treatment and the latter showing no avoidance behaviour. When taking into account the whole pollinator community, i.e. the interactive effects of honeybees and other wild pollinators, we found an increased avoidance of plants infested by the native specialised herbivore and a decreased avoidance of plants infested by the invasive herbivore.
• Taken together, our results suggest that herbivory may have an effect on B. rapa pollination, but this effect depends on the relative abundance of honeybees and other wild pollinators.

     

Identifying Native Vegetation for Reducing Exotic Species during the Restoration of Desert Ecosystems

There is currently much interest in restoration ecology in identifying native vegetation that can decrease the invasibility by exotic species of environments undergoing restoration. However, uncertainty remains about restoration's ability to limit exotic species, particularly in deserts where facilitative interactions between plants are prevalent. Using candidate native species for restoration in the Mojave Desert of the southwestern U.S.A., we experimentally assembled a range of plant communities from early successional forbs to late‐successional shrubs and assessed which vegetation types reduced the establishment of the priority invasive annuals Bromus rubens (red brome) and Schismus spp. (Mediterranean grass) in control and N‐enriched soils. Compared to early successional grass and shrub and late‐successional shrub communities, an early forb community best resisted invasion, reducing exotic species biomass by 88% (N added) and 97% (no N added) relative to controls (no native plants). In native species monocultures, Sphaeralcea ambigua (desert globemallow), an early successional forb, was the least invasible, reducing exotic biomass by 91%. However, the least‐invaded vegetation types did not reduce soil N or P relative to other vegetation types nor was native plant cover linked to invasibility, suggesting that other traits influenced native‐exotic species interactions. This study provides experimental field evidence that native vegetation types exist that may reduce exotic grass establishment in the Mojave Desert, and that these candidates for restoration are not necessarily late‐successional communities. More generally, results indicate the importance of careful native species selection when exotic species invasions must be constrained for restoration to be successful.     

Indirect competitive effects of stemborers on a gall community

Interspecific competition between phytophagous insects using the same host plant occurs frequently and can strongly affect population densities of competing species. Competition between gallmakers and stemborers could be especially intense because both types of herbivore are unable to avoid competition by relocation during their immature stages. For apical meristem gallmakers the main result of competition is likely to be the interruption of resources to the gall by the stemborers' devouring of stem contents. The proximate effect of such competition could be to reduce gall size, thereby increasing the number of chambers per gall unit volume, and reducing the size and potential reproductive output of the gallformer. In addition, smaller galls may be more susceptible to attack from size‐limited parasitoids, resulting in a second indirect effect of competition. Using a community of galling and stemboring insects on the saltmarsh shrub Iva frutescens L. (Asteraceae), we measured for indirect effects of competition. We examined the primary indirect effect of competition on gall midge crowding and the secondary effects on parasitism rates and parasitoid guild composition. Results indicated that galls co‐occurring with stemborers were smaller, crowding of gall inhabitants was 22% greater, and the composition of the parasitoid guild was altered relative to galls on unbored stems. The overall parasitism rate was not different between galls on bored vs. unbored stems. These results show that competition resulting from the presence of stemborers has the potential to affect the gall midge Asphondylia borrichiae Rossi & Strong (Diptera: Cecidomyiidae) and secondarily to affect its guild of hymenopteran parasitoids.     

A molecular tool to identify Anastatus parasitoids of the brown marmorated stink bug

Globally, Anastatus species (Hymenoptera: Eupelmidae) are associated with the invasive agricultural pest Halyomorpha halys (Stål) (Hemiptera: Pentatomidae). In Europe, the polyphagous Anastatus bifasciatus (Geoffroy) is the most prevalent native egg parasitoid on H. halys eggs and is currently being tested as a candidate for augmentative biological control. Anastatus bifasciatus frequently displays behavior without oviposition, and induces additional host mortality through oviposition damage and host feeding that is not measured with offspring emergence. This exacerbates accurate assessment of parasitism and host impact, which is crucial for efficacy evaluation as well as for pre‐ and post‐release risk assessment. To address this, a general Anastatus primer set amplifying a 318‐bp fragment within the barcoding region of the cytochrome oxidase I (COI) gene was developed. When challenged with DNA of three Anastatus species —A. bifasciatus, Anastatus japonicus Ashmead, and Anastatus sp.—, five scelionid parasitoid species that might be encountered in the same host environments and 11 pentatomid host species, only Anastatus DNA was successfully amplified. When applied to eggs of the target host, H. halys, and an exemplary non‐target host, Dendrolimus pini L. (Lepidoptera: Lasiocampidae), subjected to host feeding, no Anastatus amplicons were produced. Eggs of the two host species containing A. bifasciatus parasitoid stages, from 1‐h‐old eggs to pupae, and emerged eggs yielded Anastatus fragments. Confirmation of parasitoid presence with dissections and subsequent PCRs with the developed primer pair resulted in 95% success for 1‐h‐old parasitoid eggs. For both host species, field‐exposed sentinel emerged eggs stored dry for 6 months, 100% of the specimens produced Anastatus amplicons. This DNA‐based screening method can be used in combination with conventional methods to better interpret host‐parasitoid and parasitoid‐parasitoid interactions. It will help address ecological questions related to an environmentally friendly approach for the control of H. halys in invaded areas.     

Dose-dependent influence of Microplitis rufiventris factors on developmental rate and growth of last-instar Spodoptera littoralis larvae

The solitary endoparasitoid, Microplitis rufiventris, attacks and can develop in earlier instars of Spodoptera littoralis larvae with preference to third‐instar larvae. We used the last stadium (sixth instar), a stage which is not naturally parasitized. The newly moulted larvae (0–3 h old) of this stadium were more acceptable for parasitization by the wasp females than the older ones (24 h old). Parasitization by M. rufiventris wasp of last instar S. littoralis larvae leads to dose (no. of eggs + parasitoid factors)‐dependent effects which were more pronounced at 20°C than at 27°C. A single oviposition into a sixth instar host larva resulted in normal development of the host. However, superparasitization increased the proportions of developmentally arrested hosts and number of live wasp larvae. Development of supernumerary individuals of the parasitoid in the host larva leads to dose‐related adverse effects on host growth and development. The present study may provide interesting opportunities for studying the physiological bases of host–parasitoid interactions and parasitoid intra‐specific competition in the biological system considered.     

Effects of plant sex on insect abundance across three trophic levels in the perennial shrub Buddleja cordata

Although there is a growing interest in the effects of intra‐specific plant genetic variation on species interactions, the effects of plant sex, an important axis of genetic variation, have been less studied. In addition, previous work investigating plant sex effects on species interactions has frequently focused on bitrophic interactions (e.g., herbivory), usually ignoring plant sex effects on higher trophic levels (i.e., natural enemies). Here, we investigated the effects of plant sex on herbivore abundance and that of their natural enemies associated with the dioecious shrub Buddleja cordata Kunth (Scrophulariaceae). Furthermore, we measured a subset of plant traits frequently involved in herbivore resistance and the potentially underlying plant sex effects. To this end, we recorded the abundances of a specialist leaf‐chewing caterpillar [Acronyctodes mexicanaria Walker (Lepidoptera: Geometridae)] throughout an entire growing season. We also recorded information about the caterpillar’s parasitoids, as well as leaf water content, phenolic compounds, phosphorus, and nitrogen for male and female plants of B. cordata. Plant sex did not significantly influence caterpillar abundance but did have an effect on natural enemies, with parasitoid abundance being 2.4‐fold greater on female than on male plants. The effect of plant sex on parasitoids remained significant after accounting for caterpillar abundance, suggesting that it was underlain by a trait‐mediated (rather than density‐mediated) mechanism. Finally, we found that male plants had a higher concentration of phenolic compounds (other traits did not differ between plant sexes). These results provide valuable evidence for the extended effects of plant sex on the third trophic level and point at plant traits potentially mediating such effects.     

Landscape complexity differentially benefits generalized fourth,over specialized third,trophic level natural enemies

The differential loss of higher trophic levels in the face of natural habitat loss can result in the disruption of important trophic interactions, such as biological control. Natural enemies of herbivorous pests in cropping systems often benefit from the presence of natural habitats in surrounding landscapes, as they provide key resources such as alternative hosts. However, any benefits from a biological control perspective may be dampened if this also enhances enemies at the fourth trophic level. Remarkably, studies of the influence of landscape structure on diversity and interactions of fourth trophic‐level natural enemies are largely lacking. We carried out a large‐scale sampling study to investigate the effects of landscape complexity (i.e. the proportion of non‐crop habitat in the landscapes surrounding focal study areas) on the parasitoid communities of aphids in wheat and on an abundant extra‐field plant, stinging nettle. Primary parasitoid communities (3rd trophic level) attacking the cereal aphid, Sitobion avenae, had little overlap with the communities attacking the nettle aphid, Microlophium carnosum, while secondary parasitoids (4th trophic level) showed high levels of species overlap across these two aphids (25 vs 73% shared species respectively), resulting in significantly higher linkage density and lower specialization for secondary than primary parasitoid webs. In wheat, parasitoid diversity was not related to landscape complexity for either primary or secondary parasitoids. Rates of primary parasitism were generally low, while secondary parasitism rates were high (37–94%) and increased significantly with increasing landscape complexity, although this pattern was driven by a single secondary parasitoid species. Overall, our results demonstrate that extra‐field habitats and landscape complexity can differentially benefit fourth, over third, trophic level natural enemies, and thereby, could dampen biological control. Our results further suggest that fourth trophic‐level enemies may play an important, yet understudied, role in linking insect population dynamics across habitat types.