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.     

An implicit approach to model plant infestation by insect pests

Various spatial approaches were developed to study the effect of spatial heterogeneities on population dynamics. We present in this paper a flux-based model to describe an aphid-parasitoid system in a closed and spatially structured environment, i.e. a greenhouse. Derived from previous work and adapted to host-parasitoid interactions, our model represents the level of plant infestation as a continuous variable corresponding to the number of plants bearing a given density of pests at a given time. The variation of this variable is described by a partial differential equation. It is coupled to an ordinary differential equation and a delay-differential equation that describe the parasitized host population and the parasitoid population, respectively. We have applied our approach to the pest Aphis gossypii and to one of its parasitoids, Lysiphlebus testaceipes, in a melon greenhouse. Numerical simulations showed that, regardless of the number and distribution of hosts in the greenhouse, the aphid population is slightly larger if parasitoids display a type III rather than a type II functional response. However, the population dynamics depend on the initial distribution of hosts and the initial density of parasitoids released, which is interesting for biological control strategies. Sensitivity analysis showed that the delay in the parasitoid equation and the growth rate of the pest population are crucial parameters for predicting the dynamics. We demonstrate here that such a flux-based approach generates relevant predictions with a more synthetic formalism than a common plant-by-plant model. We also explain how this approach can be better adapted to test different management strategies and to manage crops of several greenhouses.     

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.     

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.     

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.     

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.     

Optimized timing of parasitoid release: a mathematical model for biological control of <Emphasis Type="Italic">Drosophila suzukii</Emphasis>

We present a model for the population dynamics of the invasive fruit fly Drosophila suzukii and its pupal parasitoid Trichopria drosophilae. Seasonality of the environment is captured through a system of delay differential equations with variable delays. The model is used to explore optimal timing for releasing parasitoids in biological control programs. According to the results, releasing parasitoids is most effective between late spring and early summer when the host population begins to increase. A single parasitoid release event can be more efficient than multiple releases over a prolonged period, but multiple releases are more robust to suboptimal timing choices. The findings can be useful for optimizing parasitoid release and should be transferable for similar systems. More generally, the model is an example for stage-structured resource-consumer dynamics in a varying environment.     

Effects of Predator and Prey Dispersal on Success or Failure of Biological Control

Biological control, defined as the reduction of pest populations by natural enemies, is often a component of integrated pest management strategies. Augmentation of natural enemy numbers by planned releases is a common biological control method, the successes and failures of which have been extensively reviewed. The effectiveness of biological control is influenced by how populations of predators and prey (or hosts and parasitoids) disperse in patchy environments. Here, we address the question of whether such dispersal leads to beneficial or detrimental pest control outcomes by developing a simple predator-prey model with constant releases of natural enemies in a two-patch environment. Theoretical and numerical results for all possible cases indicate that population dispersal has significant effects on the persistence of pests. For some ranges of dispersal rates or parameter space, dispersal is beneficial for pest control measures but this is not so for other ranges when it is detrimental. Therefore, knowledge of pest and natural enemy dispersal is crucial for understanding the effectiveness of biological control in a patchy environment. Finally, the model is generalised for multi-patch systems.     

Models for pest control: Complementary effects of periodic releases of sterile pests and parasitoids

Four host-parasitoid models that incorporate the simultaneous or sequential release during each generation of sterile hosts and parasitoids for control or eradication of host species are presented. The models are based on two modifications of the Nicholson-Bailey model which incorporate density regulation either in the host larvae or via parasitoid oviposition. Parasitization of host larvae and adults forms another comparison. The models indicate that the release of sterile hosts alone is more efficient than release of parasitoids alone in controlling the hosts if population regulation is in the parasitoids; otherwise, the release of parasitoids alone is more efficient. The release of both steriles and parasitoids is much more efficient than the release of either alone for either suppressing or eradicating the hosts. This greater efficiency in combination rather than separately appears to be a special case of a more general principle, which is that two pest control methods will mutually complement each other if their optimal actions in reducing host numbers are at very different host densities. This is the case for sterile releases (optimal at low host densities) and parasitoid inundation (optimal at high host densities).     

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.     

Testing a candidate parasitoid in the glasshouse: control efficacy of <Emphasis Type="Italic">Aphaereta debilitata</Emphasis> (Hymenoptera: Braconidae) against shore fly populations

Biological control efforts against the shore fly Scatella tenuicosta Collin, a pest of commercial glasshouses, have had limited success. The ability of one of its parasitoids, Aphaereta debilitata Morley, to control shore fly populations was investigated on lettuce crops within six experimental glasshouse units, over 26 weeks. The six shore fly populations, either with or without a single release of 150 mixed-sexed parasitoids, were estimated by rearing from harvested pots each week. The presence of the parasitoid significantly reduced shore fly numbers from a mean of 30.3–13.2 adult flies emerging per pot. The level of damage to each lettuce was assessed using a scoring system (0–5: no damage to heavy damage, respectively). The introduction of parasitoids reduced the median damage score of the lettuces from 2 to 1 over the study, representing a considerable change in the marketability of the crop. This study shows that single inoculative releases of A. debilitata can quickly establish within a glasshouse and significantly reduce crop damage. This suggests that the parasitoid may represent a valuable addition to an IPM strategy for shore flies.     

Prey stage preference and functional response of the predatory mite Galendromus flumenis to Oligonychus pratensis

The Banks grass mite, Oligonychus pratensis (Banks) (Acari: Tetranychidae), is a serious pest in dates (Phoenix dactylifera L.) in the New World. Currently O. pratensis is managed using the miticide, Savey, and alternative strategies are necessary to remove pressure from a single control method due to the risk of resistance evolution. For this purpose, studies are underway to develop biological control strategies using the predatory mite, Galendromus flumenis (Chant) (Acari: Phytoseiidae). The current study determined the consumption rate of G. flumenis at constant densities of O. pratensis eggs, larvae, protonymphs and deutonymphs, and defined the functional response of predator females. The predator consumed significantly more eggs than other prey stages, and displayed a type II functional response on all prey stages. The highest attack rate and shortest handling time were obtained for predators feeding on prey larvae and eggs, respectively. The proportions of prey consumed by G. flumenis were higher at lower densities for all stages of Banks grass mite, implying that G. flumenis should be more effective at suppressing Banks grass mite populations at lower densities. Therefore, in an augmentative release program, G. flumenis would need to be released early in the infestation.     

Biocontrol of Pests of Apples and Pears in Northern and Central Europe: 2. Parasitoids

The parasitoids of arthropod pests of apple and pear in northern and central Europe and their use as biological control agents are reviewed. The review demonstrates that apple and pear pests are host to a large and varied parasitoid fauna. All important pests are known to be host of parasitoids, but many parasitoids play only a minor part in regulating populations of their host. However, many parasitoid species are important natural enemies and some effectively regulate pest populations in unsprayed and/or commercial (insecticide sprayed) apple or pear orchards either individually or as part of parasitoid guilds. Exploitation/fostering of existing populations of parasitoids has been demonstrated to be an effective or partially effective approach for natural control of several important pest species. Important examples include natural regulation of the apple sawfly by Lathrolestes ensator and Aptesis nigrocincta, of the summer fruit tortrix moth by Colpoclypeus florus and Teleutaea striata, of leaf midges by Platygaster demades, of woolly aphid by Aphelinus mali and of leaf mining moths by guilds of parasitoid species. Introduction of parasitoids is an alternative approach to the exploitation of parasitoids already present in the orchard. This approach has been little explored and its success rate has been low, mainly confined to the control of non-indigenous pests by introducing parasitoids from their native region. Mass production methods for parasitoids are difficult and costly and are likely to be economic only where long-term populations can be established. Even where low cost mass culture techniques are developed, the degree of control may not be high enough to prevent economic pest damage as demonstrated by negative results with mass release of Trichogramma egg parasites for control of tortricids in orchards. Suitability of the orchard habitat is recognized as crucial to the success of individual parasitoids. Key requirements are adequate populations of the pest(s) and/or alternative hosts, suitable shelter, overwintering sites or food sources and avoidance of harmful effects of pesticides. Many species are highly sensitive to broad-spectrum insecticides, especially in the adult life-stage. Avoiding the harmful affects of insecticides is crucial to successful exploitation. The use of insecticides needs to be avoided, either altogether or at crucial times in the parasitoids' life cycle, or less harmful alternatives need to be used. Numerous parasitoids could potentially be exploited as biological control agents but hitherto have received little attention because little is known about them and/or because they are sensitive to broad-spectrum pesticides and are thus virtually absent from commercial orchards. The aim of future studies should be to develop effective strategies for establishing equilibria between important pests and their parasitoids, with pest damage rarely exceeding the economic threshold.     

The Functional Response of Parasitoids and its Implications for Biological Control

The parasitoid functional response is regarded as central to host-parasitoid dynamics. If so, then the shape of this response may be related to parasitoid success in biological control programmes. We test this by reviewing the literature on the functional response together with the BIOCAT database. Only 32 out of 94 papers have dealt experimentally with the functional response of parasitoids used in biocontrol. The study suggests that most parasitoid species have a type II response. Also, there is no clear relationship between curve shape and success in control. We conclude that other aspects of the parasitoid behaviour deserve more attention in order to understand and predict these insects' success as control agents.     

Evaluating the efficacy of entomopathogenic nematodes for the biological control of crop pests: a nonequilibrium approach

The efficacy of entomopathogenic nematodes for biological control is assessed using deterministic models. Typically, the examination of such models involves stability analyses to determine the long-term persistence of control. However, in agricultural systems, control is often needed within a single season. Hence, the transient dynamics of the systems were assessed under specific, short-term control scenarios using stage-structured models. Analyses suggest that preemptive application may be the optimum strategy if nematode mortality rates are low; applying before pest invasion can result in greater control than applying afterward. In addition, repeated applications will suppress a pest, providing the application rate exceeds a threshold. However, the period between applications affects control success, so the economic injury level of the crop and the life history of the pest should be evaluated before deciding the strategy. In all scenarios, the most important parameter influencing control is the transmission rate. These findings are applicable to more traditional biological control agents (e.g., microparasites and parasitoids), and we recommend the approach adopted here when considering their practical use. It is concluded that it is essential to consider the specific crop and pest characteristics and the definition of control success before selecting the appropriate control strategy.     

Pest control by the release of insects carrying a female-killing allele on multiple loci

With recent advances in genetics, many new strategies for pest control have become feasible. This is the second article in which we model new techniques for pest control based on the mass release of genetically modified insects. In this article we model the release of insects carrying a dominant and redundant female killing or sterilizing (FK) allele on multiple genetic loci. If such insects are released into a target population, the FK allele can become widely spread in the population through the males while reducing the population each generation by killing females. We allow the number of loci used to vary from 1 to 20. We also allow the FK allele to carry a fitness cost in males due to the gene insertions. Using a model, we explore the effectiveness and optimal strategies for such releases. In the most ideal circumstances (no density-dependence and released insects equal in fitness to wild ones), FK releases are several orders of magnitude more effective than equal sized sterile male releases. For example, a single release of 19 FK-bearing males for every two wild males, with the released males carrying the FK allele on 10 loci, reduces the target population to 0.002% of no-release size. An equal sized sterile release reduces the target population to 5% of no-release size. We also show how the effectiveness of the technique decreases as the fitness cost of the FK alleles in males increases. For example, the above mentioned release reduces the target population to 0.7% of no-release size if each FK allele carries a fitness cost in males of 5%. Adding a simple model for density-dependence and assuming that each of the released males carries the FK allele on six loci, we show that the release size necessary to reduce the target population to 1/100 of no-release size in 10 generations of releases varies from 0.44:1 to 4:1 (depending on parameter values). We also calculate the optimal number of loci on which to put the FK allele under various circumstances.     

Suppression of Ceratitis capitata (Wied.) (Diptera: Tephritidae) populations in coffee in the Mexico–Guatemala border region through the augmentative releases of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae)

In Guatemalan coffee plantations, Ceratitis capitata populations were suppressed by the application of augmentative releases of parasitoids. These releases significantly increased parasitism of this fruit fly over paired no-release control areas. Integrated management plus biological control presented a significant reduction in the pest population. These results support the application of biological control in C. capitata management.     

Potential for controlling codling moth Cydia pomonella (Linnaeus) (Lepidoptera: Tortricidae) in Argentina using the sterile insect technique and egg parasitoids

Codling moth is the main pest affecting apples and pears worldwide. Most pest control strategies used against this insect have relied on the use of broad‐spectrum insecticides which have led to non‐desirable effects like pesticide resistance, residues in the environment, human health concerns and the reduction of access to international markets. Therefore, alternative pest control strategies that would result in sustainable fruit production systems while taking care of the environment are strongly promoted. The use of the sterile insect technique has proven to be a valuable pest control tactic within area‐wide integrated pest management strategies, and its synergistic effect for Lepidoptera pests when combined with other biological control tactics such as parasitoids has been documented. The purposes of this research were to evaluate the response of an Argentinean codling moth strain to a sub‐sterilizing radiation dose of 100 Gy and to assess the acceptability and suitability of sterile codling moth eggs by the egg parasitoids, Trichogramma cacoeciae (Marchal) and Trichogramma nerudai (Pintureau and Gerding). Irradiated female moths survived better than irradiated male moths and non‐irradiated male and female moths. Also, the fecundity of irradiated female moths was reduced by more than 30% as compared to non‐irradiated ones whereas their fertility was close to zero. The F₁ generation was male biased with a lower fertility (inherited sterility) than the parental generation. Trichogramma cacoeciae and T. nerudai parasitized both fertile and sterile eggs. However, there was a significant reduction in acceptability for sterile eggs. Trichogramma nerudai parasitized more eggs than T. cacoeciae, but egg acceptability for this species was proportionally lower than for T. cacoeciae especially on eggs oviposited by irradiated females. Development to adult of both parasitoids species was not substantially affected by the origin of the eggs and the wasps had acceptable levels of adult emergence, survival and fecundity. These results provided useful information on the potential for controlling the codling moth using egg parasitoids and the sterile insect technique in Argentina.     

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.