Biological Control Of Insect Pests Research Articles

Screening of liquid media and fermentation of an endophytic Beauveria bassiana strain in a bioreactor.

A novel approach for biological control of insect pests could be the use of the endophytic entomopathogenic Beauveria bassiana isolate ATP-02. For the utilization of the endophyte as a commercial biocontrol agent, the fungus has to be mass-produced. B. bassiana was raised in shake flask cultures to produce high concentrations of total spores (TS), which include blastospores (BS) and submerged conidiospores (SCS). The highest concentration of 1.33×109 TS/mL and the highest yield of 5.32×1010 TS/g sucrose was obtained in the TKI broth with 5% sugar beet molasses which consists of 50% sucrose as a carbon source. In spite of the lower sugar concentration (2.5%) the amount of TS could be increased up to 11-times in contrast to the cultivation with 5% sucrose. The scale-up to a 2 L stirred tank reactor was carried out at 25°C, 200–600 rpm and 1 vvm at pH 5.5. A TS yield of 5.2×1010 TS/g sucrose corresponding to a SCS yield of 0.2×1010 SCS/g sucrose was obtained after 216 h. With regards to the culture medium the cost of 1012 TS amounts to 0.24 €. Plutella xylostella larvae, which were fed with oilseed rape leaves treated with spores from fermentation resulted in 77 ± 5% mortality. Moreover, spores from submerged cultivation were able to colonize oilseed rape leaves via leaf application. This is the first report of fermentation of an endophytic B. bassiana strain in a low-cost culture medium to very high yields of TS.

Regulatory experience and challenges for the release of GM insects

Genetically modified (GM) insects are a potentially valuable new tool for the biological control of insect pests of humans, animals and plants. Considerable progress has been made recently in transfer of GM insects from the laboratory to release and evaluation in the environment. As with other new genetic technologies, regulatory agencies have often found it challenging to determine the regulatory regime under which they should be evaluated, and have either adapted existing regulatory frameworks or adopted new ones. No country has legislation specifically for GM insects. However, irrespective of the regulatory regime under which they are evaluated, the purpose of their regulation remains the same; to protect human health and the environment. Consequently there are evaluation themes common to their regulatory scrutiny, which are elucidated here. There have also been some challenges and issues encountered during the risk evaluation for field release of GM insects, and this paper will highlight some of these to assist others when considering policy, regulation and assessment of GM insects. Useful regulatory and policy precedents also exist from the regulation of biological control agents and the global protection of plants from pests under the International Standards for Phytosanitary Measures (ISPM) framework. Where countries do not have existing regulations, these evaluation instruments could have the potential to be adapted to form a suitable framework for the assessment of risk for GM insects. Finally, some considerations for future policy and regulation in this area are discussed.

A global review of arthropod-mediated ecosystem-services in Vaccinium berry agroecosystems

Native beneficial arthropods, including bees, predators, and parasitoids, provide valuable ecosystem services, which help to maintain agricultural productivity and reduce the need for pesticide inputs.Vacciniumberry species are somewhat unique compared to many of the world’s fruit crops in that, up until recently, most of the harvesting and culture of species for food occurred in the geographic regions of their origin. This suggests that insects involved in many of the ecosystem services for these berries are native species that have a shared co-evolutionary history. Due to the shared phylogenetic origins of theVacciniumspp. agroecosystems, the shared need for efficient pollination, and a number of shared agricultural pests, the potential exists for research from these related systems to closely apply to agroecosystems within the same genus. This review brings together research regarding arthropod-mediated ecosystem services from a number of prominentVacciniumagroecosystems worldwide. In total, thirty-nine ecosystem service studies are discussed. These studies quantified arthropod-mediated ecosystem services being provisioned toVacciniumagroecosystems. Additionally, thirty-nine surveys of arthropods closely associated and/or providing ecosystem services toVacciniumsystems are also reviewed. Studies took place almost exclusively in temperate regions with a heavy emphasis on insect pest biological control and pollination services. It is our hope that by synthesizing this body of literature, researchers and growers might be able to utilize research methods, results, and conservation recommendations despite differences in production practices and local arthropod fauna.

Microsatellite and Wolbachia analysis in Rhagoletis cerasi natural populations: population structuring and multiple infections.

Rhagoletis cerasi (Diptera: Tephritidae) is a major pest of sweet and sour cherries in Europe and parts of Asia. Despite its economic significance, there is a lack of studies on the genetic structure of R. cerasi populations. Elucidating the genetic structure of insects of economic importance is crucial for developing phenological-predictive models and environmental friendly control methods. All natural populations of R. cerasi have been found to harbor the endosymbiont Wolbachia pipientis, which widely affects multiple biological traits contributing to the evolution of its hosts, and has been suggested as a tool for the biological control of insect pests and disease vectors. In the current study, the analysis of 18 R. cerasi populations collected in Greece, Germany, and Russia using 13 microsatellite markers revealed structuring of R. cerasi natural populations, even at close geographic range. We also analyzed the Wolbachia infection status of these populations using 16S rRNA-, MLST- and wsp-based approaches. All 244 individuals screened were positive for Wolbachia. Our results suggest the fixation of the wCer1 strain in Greece while wCer2, wCer4, wCer5, and probably other uncharacterized strains were also detected in multiply infected individuals. The role of Wolbachia and its potential extended phenotypes needs a thorough investigation in R. cerasi. Our data suggest an involvement of this symbiont in the observed restriction in the gene flow in addition to a number of different ecological factors.

Effects of landscape complexity and habitat management on stemborer colonization, parasitism and damage to maize

Lepidopteran stemborers are a serious constraint to efficient production of maize in sub-Saharan Africa. One of the most effective ways of managing these pests is through a habitat management system called push–pull. Landscape complexity has been shown to enhance biological control of insect pests, and therefore may influence effectiveness of habitat management systems designed to control pests. We studied the relative importance of the push–pull cropping system as a local effect and proportional cover of grassland as a landscape effect on (i) stemborer population density and damage to maize, and (ii) parasitism and mortality of stemborer life stages in western Kenya. We found a significant interactive effect between cropping system and grassland cover on abundance of stemborer larvae and pupa, and a near significant interactive effect of these variables on rates of egg parasitism. Cropping system had the largest effect on larval and pupal abundance in more complex landscapes, whereas it affected egg parasitism most strongly in the simplest landscapes. Grasslands appeared to primarily function as a source for the pests, rather than for natural enemies. However, sites from landscapes with a larger range of grassland cover need to be studied to fully explore the combined effects of cropping system and landscape complexity on pest control in this system. The push–pull cropping system significantly suppressed stemborer colonization of the maize and enhanced activity of stemborer parasitoids, with significant reductions in crop damage and increase in grain yield.

露地ナス栽培における土着天敵保護を主眼とした選択性殺虫剤の利用による害虫防除体系

露地ナス栽培における土着天敵保護を主眼とした選択性殺虫剤の利用による害虫防除体系

Feeding Behaviour of the Predatory Reduviid,Rhynocoris kumarii(Hemiptera: Reduviidae)

The feeding behaviour of the predatory reduviids, which is highly prey specific and replete with evolving prey-capture strategies, is the sole reason for the abundance of these insects in hostile environments. Their search for nutrients can be efficiently put to beneficial use in agriculture. The utilisation of these insects in the biological control of insect pests increases their economic potential; hence, their extensive and varied feeding behaviour needs to be studied carefully in order to make better use of these insects in integrated pest management programmes.

Synopsis of Cotesia species, biological agents for pest control on vegetables in Vietnam, with description of one new species

The biology of four allied species of the genusCotesiaCameron is reviewed. All these species were reared from larvae of pest insects mainly belonging to the families Lymantriidae, Noctuidae, Pieridae and Plutellidae. They are larval endoparasitoids and considered as important agents for biological control of pest insects infesting different vegetable crops in Vietnam, such as cabbage, kohlrabi, small colza, cauliflower, peanut, soybeans, and various other legumes. Of those four species,Cotesia clethrogynaeLong sp. n., is described as new and illustrated; the biology and distribution of the other three allied species are given, they are illustrated and compared, and a key to four species is provided.This paper resulted from the identification of a new species ofCotesiareared from limantrid larvae ofClethrogynae turbataButler and the necessity to compare related species. The host is an important pest infestant on soybean, different beans, peas and peanut in Vietnam.

Native bark-foraging birds preferentially forage in infected ash (Fraxinus spp.) and prove effective predators of the invasive emerald ash borer (Agrilus planipennis Fairmaire)

Inadvertently introduced into North America in the 1990s, the invasive emerald ash borer (EAB, Agrilus planipennis) has been spreading across the Great Lakes Region resulting in widespread ash tree (Fraxinus spp.) mortality. Native woodpeckers and other bark-foraging insectivores represent one of the few potential natural predators of EAB in the U.S. In this study, we combined observational and destructive tree harvesting approaches to assess bark-foraging bird predation on EAB larvae in a deciduous forest of central Ohio. Results of our observational study show that in an EAB impacted forest, bark-foraging birds forage more heavily on ash trees than non-ash trees, and that they forage preferentially on ash trees that exhibit canopy decline symptoms relative those with healthy canopies. These patterns were further supported by the destructive sampling of 46 ash trees wherein predation by bark-foragers significantly reduced tree-level EAB densities by upwards of 85%. Bark-foraging predation intensity increased with increased EAB infestation levels, with bark-foragers harvesting ∼45% of EAB in trees with thinning canopies compared to ∼22% in ash trees with healthy canopies. Woodpeckers harvest EAB in a density-dependent pattern that could contribute to population control. Despite bark-forager predation, EAB had a high likelihood of successfully emerging from the heavily infested ash trees (∼30% or 35 EAB per m2). Our results suggest that woodpeckers and other bark-foragers may use visual canopy decline, and perhaps other cues, to target ash trees with increased EAB densities. Moreover, our results provide insight into the indirect effects of invasive species on biotic interactions in forest ecosystems highlighting potential shifts in bark-foraging and other bird behaviors in response to a novel forest pest. Bark-foragers respond to EAB infestation and may thus potentially help regulate EAB populations and their spread in a mixed deciduous forest. We suggest that maintaining snags and nesting sites during and after forest pest outbreaks may enhance populations of bark-foraging bird species and, thus, their biological control of pest insects in temperate deciduous forests.

Influences of the seminatural and natural matrix surrounding crop fields on aphid presence and aphid predator abundance within a complex landscape

The biological control of pest insects in farmlands is an important ecosystem service provided by natural enemies, a tenet that is frequently supported by natural ecosystems; however, natural ecosystems can sometimes serve as a source of pests and can maintain them as an ecosystem disservice. We examined the effects of the surrounding seminatural and natural matrix on aphid presence and aphid predator abundance in buckwheat fields. We specifically aimed to detect whether the seminatural and natural matrix causes a trade-off between pest and natural enemy abundances. We established buckwheat study fields in a region of central Japan, the landscape of which is quite complex. Our results showed that aphid presence was not affected by either the abundance of ladybirds and lacewings or the area of the surrounding seminatural and natural matrix. We also found that the abundance of ladybirds, but not of lacewings, was significantly affected by the area of the seminatural and natural matrix. These findings suggest that in a complex landscape, as the area of seminatural and natural lands increases, some assemblages of natural enemies could also increase, but their biological control services would have little effect or would be compensated for by larger pest migration, leading to no net difference in pest damage.

Does rearing an aphid parasitoid on one host affect its ability to parasitize another species?

Abstract Generalist parasitoids are commonly used for the biological control of insect pests; however, they are often reared on a single host species because this is more practical for commercial production. Few studies have investigated the consequences of rearing a generalist parasitoid on a single host species in terms of performance on other target pests. We investigated the impact of rearing the generalist parasitoid Praon unicum Smith (Hymenoptera: Braconidae, Aphidiinae) on an alternative aphid host Myzus persicae Sulzer (Hemiptera: Aphididae) with respect to its ability to perform on Ericaphis fimbriata Richards (Hemiptera: Aphididae), a pest of highbush blueberries. Parasitoids reared on the two aphid hosts did not differ in physical size measurements. Praon unicum reared on M. persicae had a lower oviposition success over 6 days compared with insects reared on E. fimbriata, mainly as a result of differences early in life. There was no difference in parasitoid egg size, lifetime fertility, age‐specific fertility, female offspring ratio, development time or calculated intrinsic rate of increase from the two aphid hosts. We conclude that there were no negative consequences of rearing P. unicum on M. persicae on its ability to parasitize E. fimbriata, although further field studies would need to be performed to investigate whether natal host influences parasitoid preference.

Spatial and temporal variation in sugar availability for insect parasitoids in agricultural fields and consequences for reproductive success

Our ability to improve biological control of insect pests depends on our understanding of factors that limit the reproductive success of their natural enemies in the field. Pest control by parasitoids in agricultural fields can be compromised by the availability of sugar resources. We studied sugar availability for Anagrus parasitoids that parasitize the eggs of leafhopper pests (genus Erythroneura) in vineyards in northern California. Laboratory assays indicated that parasitoids survive less than a day on average without feeding, and ∼3days when supplied with honey. We captured foraging parasitoids in five unsprayed vineyards in northern California and applied a simple chemical test to assay the presence of sugar in their abdomen. Parasitoid abundance decreased throughout the day (08:00–16:00h), suggesting that many parasitoids survive less than a day in the field. The proportion of feeding (sugar-positive) individuals was generally low (∼10% on average); it varied among field sites and decreased as the season progressed (from July to October). Parasitoids captured in the afternoon were more often found with sugar in their guts compared to those captured in the morning hours. This may be explained by a direct positive effect of sugar on parasitoid survival, but may also result from longer-lived parasitoids simply having more time to locate scarce sugar resources. The egg loads of female parasitoids were negatively related to sugar availability, suggesting that sugar increases oviposition success, although we could not rule out a causal role for other site-date specific factors. Overall, our results suggest that Anagrus parasitoids in vineyards may be limited by sugar availability, and that adding sugar resources such as flowering cover crops, especially towards the end of the season, could potentially improve their efficacy as biological control agents. However, this is only likely to be successful in combination with the elimination of other factors that compromise parasitoid success.

Biological control of insect pests in apple orchards in China

Apple is one of the most important fruits in China, and both yield and quality are greatly affected by insect pests. According to surveys, there are more than 200 species of natural enemies in apple orchards. Few, however, have been closely studied. Major natural enemies including parasitoids, predators and pathogens are briefly described in this review, especially focusing on two parasitoids of Trichogramma dendrolimi Matsumura and Aphelinus mali Haldeman, predatory mites and a pathogenic fungus of Beauveria bassiana (Balsamo) Vuillemin as case studies. Augmentation, one important strategy of biological control, supplements the natural control provided by the existing natural enemy community in apple orchards, and greatly increases their efficiency in controlling pests. Conservation biological control is also widely applied in four major apple-producing areas. Based on habitat manipulation, the ground cover planting system helps regulate the microclimate and enhance the biodiversity of apple orchards, effectively conserving the richness and diversity of beneficial insect species. Certain achievements have been made in the main biological control strategies including successful introduction of some exotic natural enemies such as A. mali and Typhlodromus occidentalis Nesbitt, augmentative production and application of biological control agents such as T. dendrolimi, B. bassiana and Bacillus thuringiensis, and further research in conservation of establishing adaptive ground cover planting patterns to local environment. Challenges, however, still exist. Biological control of insect pests in apple orchards is an important part of integrated pest management programs, requiring more research and application in China.

Mass rearing and release of Trichogramma for biological control of insect pests of corn in China

Corn (Zea mays L., Poaceae) is ranked first as food crop in planting area and in total yield production in China. Asian corn borer, Ostrinia furnacalis, is the most destructive pest of corn in China, causing 6–9 million tons of yield loss per year on average. Trichogramma has been released for control of Asian corn borer at large scale since the 1970’s, partly triggered by the fact that Trichogramma dendrolimi can be successfully mass reared on eggs of the Chinese oak silkworm, Antheraea pernyi. Eggs of different hosts, such as Eri-silkworm, Samia cynthia ricini, A. pernyi, the Rice moth, Corcyra cephalonica, the Angoumois grain moth, Sitotroga cerealella and also artificial host eggs were tested and successfully used to mass-rear various Trichogramma species in China since then. The mass production technology and release technique of Trichogramma have been greatly improved in recent years making Trichogramma production and field application more practical and cost efficient. Nowadays, nearly 4 million hectares of corn are treated with T. dendrolimi, Trichogramma chilonis and Trichogramma ostriniae annually, mainly in North-east China. Large ecological and economic benefits have been achieved in areas where Trichogramma have been released continuously for many years. This includes an increase of natural populations of Trichogramma and other natural enemies in cornfields, the avoidance of any insecticide treatments in corn, a reduction in mycotoxin contamination and overall higher yields. The release of Trichogramma for controlling Asian corn borer and other lepidopteran pests became one of the key measures in corn IPM in China. Trichogramma applications combined with other non-chemical control measures for corn insect pests IPM began a new era in China as the new concept of “Public Plant Protection, Green Plant Protection” was put forward in 2006 as the guideline for plant protection in China. The future prospects and challenges of Trichogramma application are also discussed in this review.

Biological control of insect pests in litchi orchards in China

This paper describes the current state of the biological control of insect pests in litchi orchards in China. Litchi is growing in importance as a fruit in China and the control of litchi stink bug, Tessaratoma papillosa (Drury) (Hemiptera: Pentatomidae) by the solitary egg endoparasitoid Anastatus japonicus (Ashmead) (Hymenoptera: Eulophidae) is an example of successful classical biological control. This review will cover the current economic status of litchi production in China, the challenges faced in litchi pest management, and possible solutions. The review will also focus on research activities and experiences drawn from many years of experimentation and field work by researchers in an attempt to promote biological control and reduce insecticide use to produce healthier food and a safer environment. Studies on the biology and ecology of T. papillosa and its egg parasitoid A. japonicas will be summarized. The adult longevity and long oviposition period, in combination with the short life cycle, high fecundity, and resistance to harsh environmental conditions make this parasitoid ideal for biological control. The straightforwardness of mass-rearing and easy access to high quality factitious host eggs have made it possible to control T. papillosa with this parasitoid in litchi orchards over large areas in China. Both pest and parasitoid have been thoroughly studied, and A. japonicus has been used in the field for control since late 1960s. The introduction of techniques for mass-rearing of A. japonicus and the parasitoid’s efficacy in controlling T. papillosa once released will be discussed. Finally, we will address the problems currently facing litchi pest management and the importance of conservation biological control in the development and implementation of integrated pest management (IPM).

Genetic control of invasive fish: technological options and its role in integrated pest management

Genetic options for the control of invasive fishes were recently reviewed and synthesized at a 2010 international symposium, held in Minneapolis/St. Paul, MN, USA. The only option currently available “off-the-shelf” is triploidy, which can be used to produce sterile males for a release program analogous to those widely and successfully used for biological control of insect pests. However, the Trojan Y and several recombinant options that heritably distort pest population sex ratios are technologically feasible, are at or are close to proof-of-concept stage and are potentially much more effective than sterile male release programs. All genetic options at this stage require prolonged stocking programs to be effective, though gene drive systems are a potential for recombinant approaches. They are also likely to differ in their current degree of social acceptability, with chromosomal approaches (triploidy and Trojan Y) likely to be the most readily acceptable to the public and least likely to require changes in legislative or policy settings to be implemented. Modelling also suggests that the efficacy of any of these genetic techniques is enhanced by, and in turn non-additively enhance, conventional methods of pest fish control.

Cloning and characterization of a novel cry8Ab1 gene from Bacillus thuringiensis strain B-JJX with specific toxicity to scarabaeid (Coleoptera: Scarabaeidae) larvae

Isolation of Bacillus thuringiensis (Bt) strain or its cry gene encoding insecticidal crystal protein (ICP) with specific toxicity is of great importance to biological control of insect pests. In this study, by screening 66 strains of Bt isolated from soil samples collected in Shandong Province, China, a new cry8-type gene from Bt strain B-JJX was identified via PCR-RFLP method. This novel gene, cry8Ab1, was cloned from the Bt strain B-JJX and expressed in an acrystalliferous mutant strain HD-73−. The open reading frame of the cry8Ab1 gene consists of 3543bp with a G+C content of 37.99% and encodes a protein of 1180 amino acids with a putative MW of 133.3kDa which was confirmed by SDS-PAGE analysis. The Cry8Ab1 protein was expressed and released as spherical parasporal crystals from Bt acrystalliferous mutant strain HD-73− along with the presence of spores. In bioassays, this protein was toxic to 3-day-old larvae of the scarabaeid pests, Holotrichia oblita and H. parallela, with an LC50 of 5.72 and 2.00μgtoxing−1soil, respectively. The results are in accordance with the insecticidal activities of the original Bt strain B-JJX, which had an LC50 of 1.72 and 0.96μgtoxing−1soil against H. oblita and H. parallela, respectively.

Optimal barrier zones for stopping the invasion of Aedes aegypti mosquitoes via transgenic or sterile insect techniques

Biological invasions have dramatically altered the natural world by threatening native species and their communities. Moreover, when the invading species is a vector for human disease, there are further substantive public health and economic impacts. The development of transgenic technologies is being explored in relation to new approaches for the biological control of insect pests. We investigate the use of two control strategies, classical sterile insect techniques and transgenic late-acting bisex lethality (Release of Insects carrying a Dominant Lethal), for controlling invasion of the mosquito Aedes aegypti using a spatial stage-structured mathematical model. In particular, we explore the use of a barrier zone of sterile/transgenic insects to prevent or impede the invasion of mosquitoes. We show that the level of control required is not only highly sensitive to the rate at which the sterile/transgenic males are released in the barrier zone but also to the spatial range of release. Our models characterise how the distribution of sterile/transgenic mosquitoes in the barrier zone can be controlled so as to minimise the number of mass-produced insects required for the arrest of species invasion. We predict that, given unknown rates of mosquito dispersal, management strategies should concentrate on larger release areas rather than more intense release rates for optimal control.

Winter bird numerical responses to a key defoliator in mountain pine forests

The challenging question of predator–prey interactions contributing or not to limit insect outbreaks in forest ecosystems is still ongoing. Winter numerical responses of generalist insectivorous birds to overwintering larvae of a key pine defoliator, the pine processionary moth, has received little attention to date. Here, we tested the effects of forest structure and composition at stand and landscape scales on overwintering moth density and winter bird communities, including generalist moth predators. We assessed moth nest density and bird communities during two consecutive winters on 25 linear transects along an elevation gradient in mountain pine forests of the southern French Prealps. We found that winter severity significantly decreased both moth density and total bird abundance and richness. Pine processionary moth density increased with south-facing aspects and forest fragmentation, especially edge density, at the landscape scale. Winter bird communities were influenced more by forest fragmentation at the landscape scale than stand-scale variables, except moth density. Total bird abundance increased significantly with moth density only in the colder winter. Great tit Parus major abundance also increased significantly with moth density, but irrespective of winter severity. Winter bird numerical responses were mediated primarily by landscape composition, and secondarily by forest stand structure and composition. We suggest that landscape-scale conservation of bird functional diversity in both breeding and wintering seasons would increase opportunities for biological control of pest insects in mountain forests.

The effect of obligate hyperparasitoids on biological control: Differential vulnerability of primary parasitoids to hyperparasitism can mitigate trophic cascades

Obligate hyperparasitoids are widely considered an important ecological disturbance to biological control of insect pests, as they develop at the expense of primary parasitoids. However, supporting evidence is largely derived from direct trophic interactions in simple food webs. Yet, a multitude of insect pest populations simultaneously support development of several primary parasitoid species in horticultural and natural systems. Since primary parasitoid species in a community can differ in vulnerability to obligate hyperparasitoids, it is desirable to establish if the invulnerable primary parasitoids can take advantage of reduced competition from affected species by increasing their contribution to total primary parasitism levels thereby mitigating effects of hyperparasitism on biological control. To investigate this question, populations of the diamondback moth, Plutella xylostella (Linnaeus) (Plutellidae), its primary parasitoids and hyperparasitoids were monitored on unsprayed cabbage plots at weekly intervals over six consecutive years. Cotesia vestalis (Haliday) (Braconidae), a dominant primary parasitoid in this system, was a secondary host to three obligate hyperparasitoids: Mesochorus sp. (Ichneumonidae), Eurytoma sp. (Eurytomidae) and Pteromalus sp. (Pteromalidae). The higher efficiency of C. vestalis in utilizing younger host larvae at lower hyperparasitism levels limited host availability to other major primary parasitoids. But, as hyperparasitism levels increased and its populations declined, populations of Oomyzus sokolowskii (Kurdjumov) (Eulophidae) and Diadromus collaris (Gravenhorst) (Ichneumonidae) increased significantly as they parasitized a greater proportion of available hosts. As a consequence, the impact of hyperparasitoids did not result in trophic cascades, as their impact on total primary parasitism levels and infestation levels was insignificant. This study shows that primary parasitoid species that are invulnerable to hyperparasitism can take over the function of vulnerable ones in communities where interspecific interactions among species are strong. Thus, an approach that considers both direct and indirect effects of hyperparasitoids in primary parasitoid communities improves our understanding of the net impact of hyperparasitism on biological control of insect pests.