Assessment of interspecific interactions among parasitoids on the outcome of inoculative biological control of leafminers attacking chrysanthemum

Indigenous natural enemies occur within field grown crops at varying densities dependent upon a variety of other biotic and abiotic parameters. This natural control often does not provide adequate suppression, which results in the application of other pest management solutions including augmentative biological control. When releasing mass-reared natural enemies into a backdrop of existing natural enemy populations, competitive interactions are likely to occur. To assess the influence of these interspecific interactions on the outcome of such biological control practices studies were conducted in a simulated, field cage grown, cut chrysanthemum production system. Competitive interactions of two commercially available parasitoids were studied both in terms of parasitoid-host population dynamics and the impact of interspecific interactions on crop quality at harvest. The parasitoids Diglyphus isaea and Dacnusa sibirica attacking the leafminer Liriomyza langei were used as the model insect system. Both parasitoids are cosmopolitan and are known to occur in many ornamental production areas. Treatment comparisons included single species releases with complimentary releases of both species either simultaneously or with 2-week time lags, as well as a no release control to measure the background effects of natural mortality. Conclusions drawn from results of population-level studies replicated within and among years were that levels of interspecific competition among parasitoid species were undetectable at leafminer densities typical of field-grown ornamental crops (low densities), and thus, the efficacy of one species released into a backdrop of potentially competing parasitoids did not negatively or positively affect the outcome of the augmentative biological control, nor was there a positive outcome; however, crop quality at harvest was influenced.     

Biological control of arthropod pests using banker plant systems: Past progress and future directions

The goal of banker plant systems is to sustain a reproducing population of natural enemies within a crop that will provide long-term pest suppression. The most common banker plant system consists of cereal plants infested with Rhopalosiphum padi L. as a host for the parasitoid Aphidius colemani L. Aphidius colemani continually reproduce and emerge from the banker plants to suppress aphid pests such as Aphis gossypii Glover and Myzus persicae Sulzer. Banker plant systems have been investigated to support 19 natural enemy species targeting 11 pest species. Research has been conducted in the greenhouse and field on ornamental and food crops. Despite this there is little consensus of an optimal banker plant system for even the most frequently targeted pests. Optimizing banker plant systems requires future research on how banker plants, crop species, and alternative hosts interact to affect natural enemy preference, dispersal, and abundance. In addition, research on the logistics of creating, maintaining, and implementing banker plant systems is essential. An advantage of banker plant systems over augmentative biological control is preventative control without repeated, expensive releases of natural enemies. Further, banker plants conserve a particular natural enemy or potentially the ‘right diversity’ of natural enemies with specific alternative resources. This may be an advantage compared to conserving natural enemy diversity per se with other conservation biological control tactics. Demonstrated grower interest in banker plant systems provides an opportunity for researchers to improve biological control efficacy, economics, and implementation to reduce pesticide use and its associated risks.     

Interspecific Interactions among Natural Enemies ofBemisiain an Inundative Biological Control Program

Interspecific interactions among insect natural enemies have seldom been investigated experimentally within the context of biological control. Research in this area is needed due to the often contradictory predictions provided by the many theoretical models, the increasing dependence on biological control, and the concern that biological control agents may adversely affect some nontarget organisms. We describe a study whereby the occurrence and dynamics of interspecific interactions among three natural enemies (two parasitoids:Encarsia formosaandEncarsia pergandiella;and one predatorDelphastus pusillus) of the whitefly,Bemisia argentifolii(previously referred to asBemisia tabacistrain “B”), were evaluated in greenhouse cage experiments. Eight populations consisting of all possible combinations of the three natural enemies and one population of whitefly alone were established to test the following hypotheses: (1) Natural enemy introductions are capable of suppressingB. argentifoliipopulations; (2) all interspecific interactions are detrimental to achieving biological control; (3) the likelihood of achieving biological control decreases as the potential number of interspecific interactions increases; and (4) the species composition of biological control agents is of greater consequence than the number of natural enemy species released. In addition, we tested the hypothesis (5) that the frequency of interspecific interactions increases with a decrease in host or prey availability. Our results demonstrate that all combinations of natural enemies provided significant levels of whitefly suppression. While the intensities of interspecific interactions among natural enemy species were frequently positively and significantly correlated with the densities of parasitized whitefly, interspecific interactions among natural enemies were not detrimental to achieving higher levels of biological control. The composition of species released, rather than the number of species released, was of greater importance to accomplishing biological control. Releases ofD. pusillusin combination with one or both of the parasitoids provided the greatest levels of whitefly suppression. These results suggest that the types of interspecific interactions rather than the numbers of interspecific interactions among natural enemies may be important to the outcome of inundative biological control programs.     

Augmentative biological control of arthropods in Latin America

Augmentative forms of biological control, wherenatural enemies are periodically introduced,are applied over large areas in variouscropping systems in Latin America. About 25%of the world area under augmentative control issituated in this region. Well-known examplesare the use of species of the egg parasitoidTrichogramma for management ofLepidoptera in various crops. In Mexico, forexample, about 1.5 million hectares are treatedwith Trichogramma spp. Application ofTrichogramma also occurs on large areasin Colombia and Cuba, but use is limited inother Latin American countries for economicreasons, the generally low level of educationof farmers, and, more importantly, because ofthe intensive use of pesticides that preventsuse of natural enemies. Of the other eggparasitoids, the main species used incommercial releases are Trissolcusbasalis (Wollaston) against the heteropteranNezara viridula (L.) in soybean inBrazil, and Telenomus remus Nixon againstSpodoptera frugiperda (J.E. Smith) incorn in Venezuela. Natural enemies attackinglarval and pupal stages are not used to a largeextent in augmentative biological control infield crops, with the exception of the use ofCotesia parasitoids against sugarcaneborers in Brazil and several other LatinAmerican countries. In addition to the use ofparasitoids and predators, Latin America isapplying microbial control agents on a largescale, such as viruses for control ofcaterpillars in soybean, fungi for control ofpests in coffee, cotton and sugar cane, andnematodes for control of soil pests. A recentdevelopment in biological control in LatinAmerica is the use of natural enemies andantagonists for disease and pest control inprotected cultivation, for example, inColombia, Brazil and Peru. Up to date, reliablefigures on current use of inundative andseasonal inoculative biological controlappeared hard to obtain, but it is clear thatLatin America currently is a main player in thefield of augmentative releases.     

Improving the biological control of leafminers (Diptera: Agromyzidae) using the sterile insect technique

The leafminer Liriomyza trifolii (Burgess) (Diptera: Agromyzidae) is a worldwide pest of ornamental and vegetable crops. The most promising nonchemical approach for controlling Liriomyza leafminers in greenhouses is regular releases of the parasitoid Diglyphus isaea (Walker) (Hymenoptera: Eulophidae). In the current study, we examine the hypothesis that the use of D. isaea for biological control of leafminers in greenhouse crops may be more practical and efficient when supplemented with additional control strategies, such as the sterile insect technique (SIT). In small cages, our SIT experiments suggest that release of sterile L. trifolii males in three sterile-to-fertile male ratios (3:1, 5:1, and 10:1) can significantly reduce the numbers of the pest offspring. In large cage experiments, when both parasitoids and sterile males were released weekly, the combined methods significantly reduced mine production and the adult leafminer population size. Moreover, a synergistic interaction effect between these two methods was found, and a model based on our observed data predicts that because of this effect, only the use of both methods can eradicate the pest population. Our study indicates that an integrated pest management approach that combines the augmentative release of the parasitoid D. isaea together with sterile leafminer males is more efficient than the use of either method alone. In addition, our results validate previous theoretical models and demonstrate synergistic control with releases of parasitoids and sterile insects.     

三种外来入侵斑潜蝇种间竞争研究进展

美洲斑潜蝇、南美斑潜蝇、三叶斑潜蝇是危害蔬菜、花卉的世界性大害虫。不同种间相互更替或取代的现象时有发生。根据国内外相关研究报道,综述了对近年来3种斑潜蝇种间竞争的研究。对斑潜蝇种间更替和取代现象的分析显示,生殖干扰、新生物型的出现、天敌、生态位、寄主植物以及抗药性等因素可能是影响它们种间竞争的关键。以期为斑潜蝇种群演替研究及防治策略制定提供参考。     

The state of commercial augmentative biological control: plenty of natural enemies,but a frustrating lack of uptake

Augmentative biological control concerns the periodical release of natural enemies. In commercial augmentative biological control, natural enemies are mass-reared in biofactories for release in large numbers to obtain an immediate control of pests. The history of commercial mass production of natural enemies spans a period of roughly 120 years. It has been a successful, environmentally and economically sound alternative for chemical pest control in crops like fruit orchards, maize, cotton, sugar cane, soybean, vineyards and greenhouses. Currently, augmentative biological control is in a critical phase, even though during the past decades it has moved from a cottage industry to professional production. Many efficient species of natural enemies have been discovered and 230 are commercially available today. The industry developed quality control guidelines, mass production, shipment and release methods as well as adequate guidance for farmers. However, augmentative biological control is applied on a frustratingly small acreage. Trends in research and application are reviewed, causes explaining the limited uptake are discussed and ways to increase application of augmentative biological control are explored.     

Interspecific extrinsic and intrinsic competitive interactions in egg parasitoids

Interspecific competitive interactions can occur either between adult parasitoids searching/exploiting hosts (extrinsic competition) or between parasitoid larvae developing within the same host (intrinsic competition). Understanding how interspecific competition between parasitoids can affect pest suppression is important for improving biological pest control. The purpose of this work was to review both extrinsic and intrinsic competition between egg parasitoid species. These are organisms that are often candidates for biological control programs due to their ability to kill the pest before the crop feeding stage. We first reviewed the literature about interspecific competitive abilities of adult parasitoids in terms of comparative host location strategies highlighting which ecological and behavioral factors are likely to shape extrinsic competition. Then we focused on the interspecific competitive interactions between immatures developing within the same host taking into account which factors play a key role in the outcome of intrinsic competition. Finally we conclude stressing on the need to elucidate the overall competitive interaction that parasitoid species may experience in the field in order to enhance biological control success.     

Constraints to the implementation of biological control in Sri Lanka

Sri Lanka is a tropical island with a rich diversity of arthropods, with many species of indigenous natural enemies of economic pests. However, no extensive island wide surveys have been carried out for natural enemies of major crop ecosystems and only a few of the indigenous natural enemies are reported useful for augmentation biological pest control by massive field releases of laboratory-produced insects. Most successful biological control programs on the island are importation (i.e. classical) biological control programs, where established exotic natural enemies control certain pest populations in valuable crops. There is growing interest in the use of native natural enemies in pest management, thus creating a need for intensive research on the ecology of indigenous natural enemies and development of infrastructure and technology to produce natural enemies for augmentation. This paper examines constraints and opportunities for implementation of biological control in Sri Lanka.     

Combined use of the larvo‐pupal parasitoids Diachasmimorpha longicaudata and Aganaspis daci for biological control of the medfly

In biological control programmes, it is very common to employ multiple species to manage a single insect pest. However, the beneficial effects of natural enemies are not always additive because of several factors, including interspecific competition between these biocontrol agents. For this reason, in the present study we assessed several biological parameters (percentage parasitism, fertility, induced mortality and population reduction) of the parasitoids Diachasmimorpha longicaudata and Aganaspis daci when used together against the medfly Ceratitis capitata under laboratory and greenhouse conditions. Our results showed that, under laboratory conditions, fertility and percentage parasitism corresponded to a different functional response for each species (D. longicaudata: type II; A. daci: type III), whilst under greenhouse conditions, and unlike what occurs with single releases, both parasitoids showed a type III functional response; this is the only response which may lead to direct density dependence when host densities are low. Our results also revealed that when both species acted together, they produced a very high total percentage parasitism compared to that reported for single releases under both laboratory (64–76%) and greenhouse (21–51%) conditions. The parasitism was also higher for A. daci except when medfly larvae were provided in an artificial diet. Furthermore, host mortality induced by the two parasitoids acting together was very high, especially at low‐host densities; medfly population was almost completely reduced under greenhouse conditions. In summary, the data reported here supports the combined use of these species in biological control programmes against the medfly and highlights the importance of several factors, such as climatic conditions and host density, when planning their field releases.     

Biological control of Myzus persicae (Hemiptera: Aphididae) through banker plant system in protected crops

Banker plants with Aphidius colemani were tested in greenhouse for control of Myzus persicae on arugula and sweet pepper crops and compared to inoculative releases of parasitoids. Banker plants system consisted of pots of oat (non-crop plant) infested with Rhopalosiphum padi (non-pest herbivore). The non-pest herbivore serves as an alternative host for A. colemani (parasitoid of the target crop pest). In the arugula crop significant differences in the pest population between the two strategies of biological control showed the lowest densities of the pest when introducing the banker plant system. In the sweet pepper crop, there was no difference in the pest population between the two strategies of biological control.     

Effects of crop species richness on pest-natural enemy systems based on an experimental model system using a microlandscape

The relationship between crop richness and predator-prey interactions as they relate to pest-natural enemy systems is a very important topic in ecology and greatly affects biological control services. The effects of crop arrangement on predator-prey interactions have received much attention as the basis for pest population management. To explore the internal mechanisms and factors driving the relationship between crop richness and pest population management, we designed an experimental model system of a microlandscape that included 50 plots and five treatments. Each treatment had 10 repetitions in each year from 2007 to 2010. The results showed that the biomass of pests and their natural enemies increased with increasing crop biomass and decreased with decreasing crop biomass; however, the effects of plant biomass on the pest and natural enemy biomass were not significant. The relationship between adjacent trophic levels was significant (such as pests and their natural enemies or crops and pests), whereas non-adjacent trophic levels (crops and natural enemies) did not significantly interact with each other. The ratio of natural enemy/pest biomass was the highest in the areas of four crop species that had the best biological control service. Having either low or high crop species richness did not enhance the pest population management service and lead to loss of biological control. Although the resource concentration hypothesis was not well supported by our results, high crop species richness could suppress the pest population, indicating that crop species richness could enhance biological control services. These results could be applied in habitat management aimed at biological control, provide the theoretical basis for agricultural landscape design, and also suggest new methods for integrated pest management.     

Effect of flower traits and hosts on the abundance of parasitoids in perennial multiple species wildflower strips sown within oilseed rape (<Emphasis Type="Italic">Brassica napus</Emphasis>) crops

Reducing the use of insecticides is an important issue for agriculture today. Sowing wildflower strips along field margins or within crops represents a promising tool to support natural enemy populations in agricultural landscapes and, thus, enhance conservation biological control. However, it is important to sow appropriate flower species that attract natural enemies efficiently. The presence of prey and hosts may also guide natural enemies to wildflower strips, potentially preventing them from migrating into adjacent crops. Here, we assessed how seven flower traits, along with the abundance of pollen beetles (Meligethes spp., Coleoptera: Nitidulidae) and true weevils (Ceutorhynchus spp., Coleoptera: Curculionidae), affect the density of parasitoids of these two coleopterans in wildflower strips sown in an oilseed rape field in Gembloux (Belgium). Only flower traits, not host (i.e. pollen beetles and true weevils) abundance, significantly affected the density of parasitoids. Flower colour, ultraviolet reflectance and nectar availability were the main drivers affecting parasitoids. These results demonstrate how parasitoids of oilseed rape pests react to flower cues under field conditions. Similar analyses on the pests and natural enemies of other crops are expected to help to develop perennial flower mixtures able to enhance biological control throughout a rotation system.     

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.     

Meligethes aeneus oviposition preferences,larval parasitism rate and species composition of parasitoids on Brassica nigra,Raphanus sativus and Eruca sativa compared with on Brassica napus

The trap crop strategy is based on host plant discrimination by pests and their parasitoids, which may respond differently to various host plant cues, thus affecting their respective population distributions. We conducted a three-year study to compare the responses of the most damaging pest of oilseed rape (Brassica napus L.), the pollen beetle (Meligethes aeneus Fab.), and its hymenopteran parasitoids to various potential trap crops: Brassica nigra L., Raphanus sativus var. olifera Pers. and Eruca sativa Mill. with that to B. napus. We recorded their abundance, oviposition preferences and the species composition of the parasitoids.Our results show that oviposition rates of the pollen beetle and its parasitoids as well the species composition of the parasitoids varies with plant species. We discuss the potential of these plant species, especially B. nigra, to enhance the natural control of the beetle by fostering several parasitoid species. The species composition of the parasitoids on different host plants compared with on B. napus is presented for the first time. In addition to trapping pests, the trap crops could also act as parasitoid banks, enhancing natural control of the pest through providing suitable hosts for natural enemies, without increasing the population growth of the next generation of pests.     

Edges in Agricultural Landscapes: Species Interactions and Movement of Natural Enemies

Agricultural landscapes can be characterized as a mosaic of habitat patches interspersed with hostile matrix, or as a gradient of patches ranging from suitable to unsuitable for different species. Arthropods moving through these landscapes encounter a range of edges, with different permeability. Patches of native vegetation in these landscapes may support natural enemies of crop pests by providing alternate hosts for parasitic wasps and/or acting as a source for predatory insects. We test this by quantifying species interactions and measuring movement across different edge-types. A high diversity of parasitoid species used hosts in the native vegetation patches, however we recorded few instances of the same parasitoid species using hosts in both the native vegetation and the crop (canola). However, we did find overall greater densities of parasitoids moving from native vegetation into the crop. Of the parasitoid groups examined, parasitoids of aphids (Braconidae: Aphidiinae) frequently moved from native vegetation into canola. In contrast, parasitoids of caterpillars (Braconidae: Microgastrinae) moved commonly from cereal fields into canola. Late season samples showed both aphids and parasitoids moving frequently out of native vegetation, in contrast predators moved less commonly from native vegetation (across the whole season). The season-long net advantage or disadvantage of native vegetation for pest control services is therefore difficult to evaluate. It appears that the different edge-types alter movement patterns of natural enemies more so than herbivorous pest species, and this may impact pest control services.     

Strategies for the Control of Aphis gossypii Glover (Hom.: Aphididae) with Aphidius colemani Viereck (Hym.: Braconidae) in Protected Cucumbers

Aphis gossypii Glover (Hom.: Aphididae) is a damaging pest of protected cucumbers in the UK, and control measures are required which are compatible with other components in the overall cucumber integrated pest management programme. Two methods of establishing the parasitoids, Aphidius colemani Viereck (Hym.: Braconidae), in cucumber crops prior to invasion of the aphids were developed. The first involved weekly releases of small numbers of parasitoids beginning before A. gossypii became established on the plants. The second method used open-rearing units based on maize, wheat and rygrass plants infested with Rhopalosiphum padi L (Hom.: Aphididae), which is a common host to many natural enemies of A. gossypii but not a threat to the cucumber crop. Both methods were found to be more efficient in summer than in late spring. Parasitoid release rates were established for the two control methods at both of these times of the year. Like all biological control measures, these methods will require careful management in practice and some fine-tuning to suit individual crop production systems.     

Conservation biological control and enemy diversity on a landscape scale

Conservation biological control in agroecosystems requires a landscape management perspective, because most arthropod species experience their habitat at spatial scales beyond the plot level, and there is spillover of natural enemies across the crop–noncrop interface. The species pool in the surrounding landscape and the distance of crop from natural habitat are important for the conservation of enemy diversity and, in particular, the conservation of poorly-dispersing and specialized enemies. Hence, structurally complex landscapes with high habitat connectivity may enhance the probability of pest regulation. In contrast, generalist and highly vagile enemies may even profit from the high primary productivity of crops at a landscape scale and their abundance may partly compensate for losses in enemy diversity. Conservation biological control also needs a multitrophic perspective. For example, entomopathogenic fungi, plant pathogens and endophytes as well as below- and above-ground microorganisms are known to influence pest-enemy interactions in ways that vary across spatiotemporal scales. Enemy distribution in agricultural landscapes is determined by beta diversity among patches. The diversity needed for conservation biological control may occur where patch heterogeneity at larger spatial scales is high. However, enemy communities in managed systems are more similar across space and time than those in natural systems, emphasizing the importance of natural habitat for a spillover of diverse enemies. According to the insurance hypothesis, species richness can buffer against spatiotemporal disturbances, thereby insuring functioning in changing environments. Seemingly redundant enemy species may become important under global change. Complex landscapes characterized by highly connected crop–noncrop mosaics may be best for long-term conservation biological control and sustainable crop production, but experimental evidence for detailed recommendations to design the composition and configuration of agricultural landscapes that maintain a diversity of generalist and specialist natural enemies is still needed.     

Effect of <Emphasis Type="Italic">Diachasmimorpha longicaudata</Emphasis> releases on the native parasitoid guild attacking <Emphasis Type="Italic">Anastrepha</Emphasis> spp. larvae in disturbed zones of Chiapas,Mexico

We evaluated the effect of augmentative releases of Diachasmimorpha longicaudata (Ashmead), on the native parasitoid guild of Anastrepha spp. over a two year period in zones adjacent to mango commercial orchards in Chiapas, Mexico. We chose two 15 ha working zones, 15 km apart, harbouring fruit fly hosts of varying densities without chemical control. In 2013, parasitoids were released in zone “A” while zone “B” served as control. In 2014 zones were exchanged. As expected, releases of D. longicaudata significantly increased total parasitism, from around 0.5–5% to over 22%, but annual parasitism by native parasitoids was only significantly affected in zone “A”. The numbers of native parasitoids were higher in zone “A” in both years, and diversity (H′) was not affected by D. longicaudata releases in both zones. Our results suggest that releases of D. longicaudata affect the relative abundance but not the species richness of native parasitoids.     

我国烟粉虱主要捕食和寄生性天敌控制能力研究进展

烟粉虱Bemisia tabaci Gennadius是一种广泛分布于世界各地的多食性害虫,对我国多个省市区的农作物和观赏植物造成了严重的危害。化学杀虫剂的大量使用在杀伤天敌的同时使烟粉虱产生了不同程度的抗性,防治越来越困难;相较于化学防治,在不同地区筛选有效的天敌对烟粉虱进行生物防治是对烟粉虱进行有效控制的重要方法。我国报道的捕食性天敌共计26科109种,寄生性天敌共计2科59种。烟粉虱防治过程中由于单一的防治效果不理想,联合多个天敌资源的利用是增加对烟粉虱的生物防治效果的重要手段。本文通过对我国烟粉虱捕食性和寄生性天敌种类系统全面的整理,同时对烟粉虱优势种天敌中的单种或者多种组合利用后对烟粉虱的的控害潜能进行综述,以期为烟粉虱天敌昆虫种类的筛选和实现高效的生物防治提供科学依据。