Entomopathogenic fungi stimulate transgenerational wing induction in pea aphids,Acyrthosiphon pisum (Hemiptera: Aphididae)

1. Aphid natural enemies include not only predators and parasitoids but also pathogens, of which fungi are the most studied for biological control. While wing formation in aphids is induced by abiotic conditions, it is also affected by biotic interactions with their arthropod natural enemies. Wing induction via interactions with arthropod natural enemies is mediated by the increase in their physical contact when alarmed (pseudo‐crowding). Pathogenic fungi do not trigger this alarm behaviour in aphids and, therefore, no pseudo‐crowding occurs. 2. We hypothesise that, while pathogenic fungi will stimulate maternally induced wing formation, the mechanism is different and is influenced by pathogen specificity. We tested this hypothesis using two entomopathogenic fungi, Pandora neoaphidis and Beauveria bassiana, an aphid specialist and a generalist respectively, on the pea aphid, Acyrthosiphon pisum Harris. 3. We first demonstrate that pea aphids infected with either pathogen and maintained in groups on broad bean plants produced a higher proportion of winged morphs than uninfected control aphids. We then show that, when maintained in isolation, aphids infected with either pathogen also produced higher proportions of winged offspring than control aphids. There was no difference between P. neoaphidis and B. bassiana in their effects on wing induction in either experiment. 4. Unlike the effect of predators and parasitoids on pea aphid wing induction, the effect of pathogens is independent of physical contact with other aphids, suggesting that physiological cues induce wing formation in infected aphids. It is possible that aphids benefit from wing induction by escaping infected patches whilst pathogens may benefit through dispersion. Possible mechanisms of wing induction are discussed.     

Damage to sagebrush attracts predators but this does not reduce herbivory

Emissions of volatiles increase following herbivory from many plant species and volatiles may serve multiple functions. Herbivore‐induced volatiles attract predators and parasitoids of herbivores and are often assumed to benefit plants by facilitating top‐down control of herbivores; this benefit of induced emissions has been tested only a few times. Volatile compounds released by experimentally clipped sagebrush shoots have been shown to reduce levels of chewing damage experienced by other shoots on the same plant and on neighboring sagebrush plants. In this study, I asked whether experimental clipping attracted predators of herbivorous insects to sagebrush shoots. I also evaluated aphid populations and chewing damage on clipped and unclipped shoots and whether predators were likely to have caused differences in aphids and chewing damage. Shoots that had been clipped recruited more generalist predators, particularly coccinellids and Geocoris spp. in visual surveys conducted during two seasons. Clipping also caused increased numbers of parasitized aphids in one season. Ants were common tending aphids but were not significantly affected by clipping. Despite the increase in generalist predators, clipped plants were more likely to support populations of aphids that increased during both seasons compared to aphids on unclipped control plants. Clipped shoots suffered less damage by chewing herbivores in the 1‐year in which this was measured. Chewing damage was not correlated with numbers of predators. These results suggest that predators and parasitoids were attracted to experimentally clipped sagebrush plants but that these predators were not effective at reducing net damage to the plant. This conclusion is not surprising as much of the herbivory is inflicted by grasshoppers and deer, herbivores that are not vulnerable to the predators attracted to sagebrush volatiles. More generally, it should not be assumed that predators that are attracted by herbivore‐induced volatiles necessarily benefit the plant without testing this hypothesis under field conditions.     

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.     

Field cage evaluation of interspecific interaction of two aphelinid parasitoids and biocontrol effect on Bemisia tabaci (Hemiptera: Aleyrodidae) Middle East‐Asia Minor 1

To explore sustainably effective biological control measures to suppress the super pest Bemisia tabaci (Gennadius) Middle East‐Asia Minor 1 and better understand the biological control effects of single and multiple releases of parasitoids, we evaluated the performance and interaction of two aphelinid parasitoids of B. tabaci, Eretmocerus hayati Zolnerowich & Rose (an exotic primary parasitoid) and Encarsia sophia (Girault & Dodd) (an autoparasitoid, which is controversial in a biological control program). Single species or two species were jointly (1:1 density ratio) released in field cages on cotton in Hebei province, China, in 2010. Results of the field cage experiment showed that all parasitoid release treatments were successful in reducing the densities of the host B. tabaci relative to the control in which no parasitoid was released. The combined release of two parasitoid species showed the highest control effect among the treatments. Different population growth trajectories indicated asymmetric competitive effects of En. sophia on Er. hayati. The densities of Er. hayati were significantly higher in the Er. hayati alone treatment than in the combined release treatment, while densities of En. sophia were lower in the En. sophia alone treatment than in the combined release treatment. Our results demonstrated interspecific competition between autoparasitoid En. sophia and exotic primary parasitoid Er. hayati. However, no evidence indicated that autoparasitoid En. sophia disrupted the host suppression achieved by primary parasitoid Er. hayati. The release of the autoparasitoid together with the primary parasitoid may not influence host suppression in biological control.     

Current status and future perspectives on natural enemies for pest control in Taiwan

ABSTRACT

In Taiwan, the agricultural policy, ‘Reduce the consumption of pesticide to half in the next 10 years’, was launched in 2017. Pesticide application, which results in contamination of food by chemical residues, pest resistance, and other adverse ecological effects, is a growing public and environmental concern. Pest control by natural predators is, thus, the best alternative. Biological control methods implemented based on insights obtained from studies on pest behaviour, rearing, and various crop management modes, increase the possibility of controlling pests in modern organic agricultural systems. More than a decade has passed since the first introduction of a predatory insect in Taiwan for pest control (in the 1990s). Predatory and parasitic natural enemies, including lacewing, predatory stink bugs, Orius, and parasitic wasps, were initially used for controlling thrips, aphids, spider mites, whiteflies, and lepidopteran pests. At present, there exists a wide range of integrated pest management (IPM) methods incorporating other non-chemical, biological, and agricultural methods. However, recently, there has been an increase in research and development on the utilisation of natural enemies of insects and the associated food safety issues. Mass production and release, storage, and handling techniques of insect predators and parasitoids have been successful in recent years. The final goal of present day research is to develop natural enemy products and provide an IPM-based model to farmers for using natural enemies in agricultural production systems, thereby reducing pesticide application and ensuring food security.     

Prey availability in time and space is a driving force in life history evolution of predatory insects

Environmental constraints can be determinant key factors conditioning predator life history evolution. Prey seems to have conditioned life history evolution in their ladybird predator, with the predators of aphids apparently presenting faster development, greater fecundity and shorter longevity than species preying on coccids. However a rigorous comparison has never been done. We hypothesize that aphids and coccids differ by their developmental rate, abundance, and distribution in the field, which act as ecological constraints promoting life history evolution in ladybird predators. Field data reveal that aphids are ephemeral resources available in the form of large colonies randomly distributed in the habitat whereas coccids form smaller colonies that tend to be aggregated in space and available for longer periods. A comparison in laboratory conditions of two predatory species belonging to the tribe Scymnini (Coleoptera: Coccinellidae) show that the aphidophagous species lives at a faster pace than the coccidophagous: it develops faster, matures earlier, is more fecund, has a shorter reproductive life-span and allocate proportionally more fat in its gonads relative to soma. This indicates that the life histories of aphidophagous and coccidophagous ladybird predators appear to have evolved in response to particular patterns of prey availability in time and space. Under the light of these results, the existence of a slow-fast continuum in ladybirds is briefly addressed.     

Natural enemies of Tuta absoluta in the Mediterranean basin,Europe and South America

The tomato leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) represents a global threat to commercial tomato (Solanum lycopersicum L.) production, both in open field and greenhouse. Native to South America, it spread over the Mediterranean Basin, Europe, Africa and part of Asia in only 12 years, and currently it is reported in over 80 countries. Biological control is one of the options for its control and a large number of natural enemies has been reported in association with the pest, both in the areas of origin and of introduction. The egg parasitoid Trichogramma pretiosum, in South America, and the mirid predators Macrolophus pygmaeus and Nesidiocoris tenuis, in Europe and the Mediterranean basin, are used as commercial biocontrol agents. Even if several natural enemies might be promising candidates for biocontrol, their potential role in quantitative pest reduction has been seldom established under practical tomato production conditions.

Since climatic suitability indices predict a high probability for continued invasion by T. absoluta, mainly in China and the USA, there is an urgent need for new control options. In order to minimise the use of broad spectrum insecticides, biocontrol techniques should be considered. As tomato is produced seasonally, augmentative biocontrol seems to be the most effective control option, but pest reduction might be optimised by adding conservation biocontrol, and by combining biocontrol within IPM programmes.

Here, an overview of predators and parasitoids of T. absoluta in South American and Euro-Mediterranean regions, and their biological control efficacy under laboratory, semi-field and field conditions is provided.     

Biological control and sustainable food production

The use of biological control for the management of pest insects pre-dates the modern pesticide era. The first major successes in biological control occurred with exotic pests controlled by natural enemy species collected from the country or area of origin of the pest (classical control). Augmentative control has been successfully applied against a range of open-field and greenhouse pests, and conservation biological control schemes have been developed with indigenous predators and parasitoids. The cost-benefit ratio for classical biological control is highly favourable (1:250) and for augmentative control is similar to that of insecticides (1:2-1:5), with much lower development costs. Over the past 120 years, more than 5000 introductions of approximately 2000 non-native control agents have been made against arthropod pests in 196 countries or islands with remarkably few environmental problems. Biological control is a key component of a 'systems approach' to integrated pest management, to counteract insecticide-resistant pests, withdrawal of chemicals and minimize the usage of pesticides. Current studies indicate that genetically modified insect-resistant Bt crops may have no adverse effects on the activity or function of predators or parasitoids used in biological control. The introduction of rational approaches for the environmental risk assessment of non-native control agents is an essential step in the wider application of biological control, but future success is strongly dependent on a greater level of investment in research and development by governments and related organizations that are committed to a reduced reliance on chemical control.     

Effects of mummy consumption on fitness and oviposition site selection on Harmonia axyridis

Intraguild predation (IGP) has been commonly reported between predators and parasitoids used as biological control agents as predators consuming parasitoids within their hosts. However, the effect of parasitoid–mummy consumption on the fitness of the predator and subsequent oviposition site selection have not been well studied. In our study, we conducted two laboratory experiments to examine the influence of Aphidius gifuensis Ashmead (Hymenoptera: Braconidae) mummies as prey on fitness and subsequently oviposition site selection of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Results indicate that when H. axyridis was reared on A. gifuensis mummies only, its larval development was prolonged, and body weight of the 4th instar larvae and newly emerged adults, and fecundity decreased. Moreover, H. axyridis did not exhibit oviposition preference on plants infested with unparasitized aphids or aphids parasitized for shorter than 9 days. However, compared with plants with mummies (parasitized ≥9 days), H. axyridis laid more eggs on plants with unparasitized aphids. In contrast, H. axyridis previously fed with A. gifuensis mummies did not show a significant oviposition preference between plants with unparasitized aphids and those with mummies (parasitized ≥9 days). Overall, our results suggest that mummy consumption reduced the fitness of H. axyridis. Although H. axyridis avoided laying eggs on plants with A. gifuensis mummies, prior feeding experience on A. gifuensis mummies could alter the oviposition site preference. Thus, in biological control practice, prior feeding experience of H. axyridis should be carefully considered for reduction of IGP and increase of fitness of H. axyridis on A. gifuensis.     

A ‘Goldilocks’ hypothesis for dispersal of biological control agents

The rate at which biological control agents disperse from release sites has important implications for their establishment and spread. Low rates of dispersal can yield spread that is too slow and may necessitate redistribution efforts for importation biological control and a high density of release sites for augmentation. Low dispersal rates may also lead to inbreeding at the site of release. On the other hand, high rates of dispersal can lead to Allee effects at the leading edge of the invasion front, potentially reducing the likelihood of establishment. Given these disadvantages associated with both low and high dispersal rates, we argue that intermediate rates of dispersal are likely to maximize the probability of establishment and appropriate spread for biological control agents released in the context of either importation or augmentative biological control. We consider this putative relationship a ‘Goldilocks hypothesis’ since it posits an optimum at intermediate values. In this review paper we begin by discussing the rationale for the Goldilocks hypothesis and then provide a case study from our work on importation biological control of the soybean aphid, Aphis glycines. Work on the soybean aphid parasitoid Binodoxys communis has shown that long-distance dispersal of immature parasitoids within winged migrating aphids is unlikely. This is likely good news for importation biological control because parasitoids dispersed in this manner would likely encounter crippling Allee effects. On the other hand, results from a field release study also suggest that female B. communis females (but not males) disperse actively from release sites. This female-biased dispersal may lead to strong mate-finding Allee effects and therefore may make establishment less likely.     

Biological control of aphids in the presence of thrips and their enemies

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

Ecological considerations for biological control of aphids in protected culture

Several braconid and aphelinid parasitoids, midges, lacewings, and ladybird beetles are used to control aphids in greenhouses. Here, I review three topics as ecological bases for the biological control of aphids in a protected culture: the preliminary evaluation of biological control agents, natural enemy release strategies, and the effects of intraguild predation (IGP) on biological control. A comparison of several parasitoid species was conducted to select agents for the biological control of aphids; the intrinsic rate of natural increase was a useful criterion in the preliminary evaluation. To compare predators as biological control agents, the aphid-killing rate must be considered as a critical criterion, rather than reproductive criteria. The banker plant system (open rearing system) is used as a release method for Aphidius colemani and other natural enemies of aphids. Continuous release of parasitoid adults, which is the important characteristic of this method, has a stabilizing effect on population fluctuation in the aphid–parasitoid system. Two species of natural enemies can be used to control aphids in greenhouses. When one parasitoid and one predator are used simultaneously in a greenhouse, IGP of the parasitoid by the predator can occur, but the effect of IGP is less important in greenhouses than in the field.     

Host plants and natural enemies of Bemisia tabaci (Hemiptera: Aleyrodidae) in China

Abstract The sweetpotato whitefly, Bemisia tabaci, has been a destructive pest in China for over the past two decades. It is an extremely polyphagous insect, being recorded feeding on hundreds of host plants around the world. Potential host plants and natural enemies of B. tabaci in the south, southeast, middle, north and northwest of China were investigated during the last decade. In total 361 plant species from 89 families were recorded in our surveys. Plants in the families Compositae, Cruciferae, Cucurbitaceae, Solanaceae and Leguminosae were the preferred host species for B. tabaci, which therefore suffered much damage from this devastating pest due to their high populations. In total, 56 species of parasitoids, 54 species of arthropod predators and seven species of entomopathogenic fungi were recorded in our surveys. Aphelinid parasitoids from Encarsia and Eretmocerus genera, lady beetles and lacewings in Coleoptera and Neuroptera were found to be the dominant arthropod predators of B. tabaci in China. The varieties of host plant, their distribution and the dominant species of natural enemies of B. tabaci in different regions of China are discussed.     

Effects of augmentative releases of the coccinellid, Adalia bipunctata, and of insecticide treatments in autumn on the spring population of aphids of the genus Dysaphis in apple orchards

The impact of augmentative releases of indigenous predators and insecticide applications to control the autumn aphid forms of the genus Dysaphis (Homoptera: Aphididae), major pest insects on apple trees, was assessed in one-year field experiments in Switzerland. Eggs and larvae of the two-spot ladybird beetle Adalia bipunctata (L.) (Coleoptera: Coccinellidae) were released on 4-year old apple trees in various numbers at five different dates in autumn 1998 when sexuales of the aphids were present. Additionally, Pyrethrum HP was sprayed at the same five dates to compare the effectiveness of these augmentative releases to a commonly applied insecticide. Augmentative releases of larvae before mid-October significantly prevented the deposition of overwintering eggs by aphids of the genus Dysaphis and consequently reduced the number of hatched fundatrices in spring, 1999. There was a significant negative functional response among the number of released coccinellid larvae in autumn 1998 and the number of observed fundatrices on apple trees in spring 1999. Applications of Pyrethrum HP before mid-October were more effective than augmentative releases of larvae of A. bipunctata. The release of coccinellid eggs had no impact on the number of fundatrices of the genus Dysaphis in the next spring because they did not hatch due to bad weather conditions. The weather conditions in autumn seemed to have an impact on the autumn migration of the winged aphids back to their primary host. The prevention of egg deposition of aphids in autumn is a promising control strategy and deserves further exploration for practical use.     

Parasitism-mediated prey selectivity in laboratory conditions and implications for biological control

In agroecosystems, parasitoids and predators may exert top-down regulation and predators for different reasons may avoid or give preference to parasitised prey, i.e., become an intraguild predator. The success of pest suppression with multiple natural enemies depends essentially on predator–prey dynamics and how this is affected by the interplay between predation and parasitism. We conducted a simple laboratory experiment to test whether predators distinguished parasitised prey from non-parasitised prey and to study how parasitism influenced predation. We used a host-parasitoid system, Spodoptera frugiperda and one of its generalist parasitoids, Campoletis flavicincta, and included two predators, the stinkbug Podisus nigrispinus and the earwig Euborellia annulipes. In the experiment, predators were offered a choice between non-parasitised and parasitised larvae. We observed how long it took for the predator to attack a larva, which prey was attacked first, and whether predators opted to consume the other prey after their initial attack. Our results suggest that, in general, female predators are less selective than males and predators are more likely to consume non-parasitised prey with this likelihood being directly proportional to the time taken until the first prey attack. We used statistical models to show that males opted to consume the other prey with a significantly higher probability if they attacked a parasitised larva first, while females did so with the same probability irrespective of which one they attacked first. These results highlight the importance of studies on predator–parasitoid interactions, as well as on coexistence mechanisms in agroecosystems. When parasitism mediates predator choice so that intraguild predation is avoided, natural enemy populations may be larger, thus increasing the probability of more successful biological control.     

History and Future of Introduction of Exotic Arthropod Biological Control Agents in Spain: A Dilemma?

The first documented introduction of an exotic invertebrate biological control agent (IBCA) in Spain occurred in 1908. Sixty-four additional species have been introduced since then. Information, both previously recorded and original data, on the species introduced for pest control is summarized. Most of the introduced IBCAs focused on citrus pests and homopterans clearly predominate among target phytophagous species. Success has been more frequent for IBCAs used in seasonal inoculative strategies (50.0% of cases) than in classical biological control programs (17.1% of cases). Concerns about potential non-target effects of such species are increasing, but post-release evaluation has often been insufficient to draw any conclusions about them. Most of the beneficial species introduced in Spain were parasitoids (n = 53), and the remaining species were predators (n = 12). Only four parasitoids are considered specialized monophagous natural enemies. The mean number of host species parasitized by parasitoids is 15.2, whereas the mean number of prey species attacked by predators is 21.2. Therefore, polyphagy appears to be quite common among the IBCAs that have been introduced in Spain. The rationale guiding many of these introductions in the past would not be acceptable nowadays. Since classical biological control is such a valuable strategy for pest control, straightforward protocols to evaluate exotic candidate species are urgently needed.     

Influence of cornicle droplet secretions of the cabbage aphid,Brevicoryne brassicae,on parasitism behavior of na＇fve and experienced Diaeretiella rapae

Insects have evolved amazing methods of defense to ward off enemies. Many aphids release cornicle secretions when attacked by predators and parasitoids. These se cretions contain an alarm pheromone that alerts other colony members of danger, thereby providing indirect fitness benefits to the releaser. In addition, contact with cornicle se cretions could also threaten an attacker and could provide direct fitness to the releaser. However, cornicle secretions may also be recruited as a kairomonal cue by aphid natural enemies. In this study, we investigated the effect of the cornicle droplet volatiles of the cabbage aphid, Brevicoryne brassicae （L.）, on the hostsearching behavior of naive and experienced female Diaeretiella rapae （M＇Intosh） parasitoids in olfactometer studies. In addition, we evaluated the role ofB. brassicae cornicle droplets on the oviposition prefer ence of the parasitoid in a twochoice bioassay. Naive females did not exhibit any preference between volatiles from aphids secreting cornicle droplets over nonsecreting aphids, while experienced parasitoids exploited the secretions in their host location. Experienced females were also able to choose volatiles from both secreting and nonsecreting aphids over clean air, while this ability was not observed in naive females. Although secretion of cornicle droplets did not influence the percentage of first attack in either naive or experienced females, the success of attack （i.e. resulting in a larva） was significantly different between secreting and nonsecreting aphids in the case of experienced parasitoids.     

Effect of parasitism on flight behavior of the soybean aphid, Aphis glycines

Many aphid species possess wingless (apterous) and winged (alate) stages, both of which can harbor parasitoids at various developmental stages. Alates can either be parasitized directly or can bear parasitoids eggs or larvae resulting from prior parasitism of alatoid nymphs. Winged aphids bearing parasitoid eggs or young larvae eventually still engage in long-distance flights, thereby facilitating parasitoid dispersal. This may have a number of important implications for biological control of aphids by parasitoids. In this study, we determined the effect of parasitism by Aphelinus varipes (Hymenoptera: Aphelinidae) on wing development and flight of the soybean aphid, Aphis glycines (Hemiptera: Aphididae). We also quantified the influence of aphid flight distance on subsequent A. varipes development. Parasitism by A. varipes was allowed at different A. glycines developmental stages (i.e., alatoid 3rd and 4th-instar nymphs, alates) and subsequent aphid flight was measured using a computer-monitored flight mill. Only 35% of aphids parasitized as L3 alatoid nymphs produced normal winged adults compared to 100% of L4 alatoids. Flight performance of aphids parasitized as 4th-instar alatoid nymphs 24 or 48 h prior to testing was similar to that of un-parasitized alates of identical age, but declined sharply for alates that had been parasitized as 4th-instar alatoid nymphs 72 and 96 h prior to testing. Flight performance of aphids parasitized as alate adults for 24 h was not significantly different from un-parasitized alates of comparable ages. Flight distance did not affect parasitoid larval or pupal development times, or the percent mummification of parasitized aphids. Our results have implications for natural biological control of A. glycines in Asia and classical biological control of the soybean aphid in North America.     

Generalist predators disrupt parasitoid aphid control by direct and coincidental intraguild predation

Generalist predators and parasitoids are considered to be important regulators of aphids. The former not only feed on these pests, but might also consume parasitoids at all stages of development. This direct or coincidental interference affects the natural control of aphids, the scale of which is largely unknown, and it has rarely been examined under natural conditions. Here, molecular diagnostics were used to track trophic interactions in an aphid-parasitoid-generalist predator community during the build-up of a cereal aphid population. We found that generalist predators, principally carabid and staphylinid beetles as well as linyphiid spiders, had strong trophic links to both parasitoids and aphids. Remarkably, more than 50% of the parasitoid DNA detected in predators stems from direct predation on adult parasitoids. The data also suggest that coincidental intraguild predation is common too. Generalist predators, hence, disrupt parasitoid aphid control, although the levels at which the predators feed on pests and parasitoids seem to vary significantly between predator taxa. Our results suggest that taxon-specific trophic interactions between natural enemies need to be considered to obtain a more complete understanding of the route to effective conservation biological control.     

Combining lacewings and parasitoids for biological control of foxglove aphids in sweet pepper

The role of natural enemy diversity in biological pest control has been debated in many studies, and understanding how interactions amongst predators and parasitoids affect herbivore populations is crucial for pest management. In this study, we assessed the individual and combined use of two species of natural enemies, the parasitoid Aphidius ervi Haliday, and the predatory brown lacewing Micromus variegatus (Fabricius), on their shared prey, the foxglove aphid, Aulacorthum solani (Kaltenbach), on sweet pepper. We hypothesized that the presence of intraguild predation (IGP) and predator facilitation (through induced aphid dropping behaviour) might have both negative and positive effects on aphid control, respectively. Our greenhouse trial showed that overall, the greatest suppression of aphids occurred in the treatment with both the parasitoid and the lacewing. While the combination of lacewings and parasitoids significantly increased aphid control compared to the use of parasitoids alone, the effect was not significantly different to the treatment with only predators, although there was a clear trend of enhanced suppression. Thus, the combined effects of both species of natural enemies were between additive and non‐additive, suggesting that the combination is neither positive nor negative for aphid control. High levels of IGP, as proven in the laboratory, were probably compensated for by the strong aphid suppression provided by the lacewings, whether or not supplemented with some level of predator facilitation. For aphid management over a longer time scale, it might still be useful to combine lacewings and parasitoids to ensure stable and resilient aphid control.