The effects of parasitoid fecundity and host taxon on the biological control of insect pests: the relationship between theory and data

1. A simple, intuitive argument and the tenets of the biological control literature both suggest that, in general, parasitoids with a greater fecundity will provide better control of their hosts, and will thus be better biological control agents. 2. A model of host-parasitoid dynamics, based on the standard Thompson–Nicholson–Bailey approach and incorporating the effects of parasitoid fecundity-limitation and host density-dependence, also indicates that as parasitoid fecundity decreases so does local stability and the degree of host suppression. 3. A taxonomically diverse data set obtained from the biological control record failed to support this theoretical prediction, but at the same time indicated a strong effect of host taxon on the outcome of biological control. 4. The hypothesis that the fecundity of parasitoids is correlated positively with their ability to suppress host populations is supported by data exclusively from the host order Lepidoptera. 5. Possible explanations for the divergence between the fecundity-limitation hypothesis and the complete data set include: the ability of parasitoids to provide long-term control of pests without the presence of a stable host–parasitoid equilibrium; differences between the concepts of successful control in theory and practice; evolutionary trade-offs between fecundity and other parasitoid life-history features, such as search efficiency, leading to better pest control by parasitoids with low fecundity; and differing windows of vulnerability to parasitoid attack between host taxa.     

Delayed emergence and the success of parasitoids in biological control

Delayed emergence, a life history feature of many insects living in unpredictable environments, can have major consequences for the dynamics of host–parasitoid interactions, which vary according to their physiological interactions. We studied, through simple modeling, the significance of prolonged diapause on the suppression levels achieved by parasitoids and illustrate our case with a system involving a major forest pest, the woodwasp Sirex noctilio and two of its parasitoid species that have been introduced into different geographical regions through classical biological control programmes. Our findings suggest that the physiological relationship between parasitoid and host delayed emergence patterns may help understand observed variable success in several bio-control programs. We conclude that for given environments, host delayed emergence and the way in which parasitoids deal with it, should be included in the list of selection criteria of natural enemies of many pests, especially those affecting forests.     

Delayed emergence and the success of parasitoids in biological control

Delayed emergence, a life history feature of many insects living in unpredictable environments, can have major consequences for the dynamics of host–parasitoid interactions, which vary according to their physiological interactions. We studied, through simple modeling, the significance of prolonged diapause on the suppression levels achieved by parasitoids and illustrate our case with a system involving a major forest pest, the woodwasp Sirex noctilio and two of its parasitoid species that have been introduced into different geographical regions through classical biological control programmes. Our findings suggest that the physiological relationship between parasitoid and host delayed emergence patterns may help understand observed variable success in several bio-control programs. We conclude that for given environments, host delayed emergence and the way in which parasitoids deal with it, should be included in the list of selection criteria of natural enemies of many pests, especially those affecting forests.     

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.     

Selecting effective parasitoids for biological control introductions: Codling moth as a case study

Codling moth is a notorious fruit-boring pest that has been neglected as a target for biological control introductions. Nonetheless, it is a suitable target as it is an exotic species in the western U.S., on an exotic crop plant, in a relatively undisturbed environment, and has a lower level of abundance in its region of origin in Central Asia. In contrast, it belongs to the Olethreutidae, a family of pests with a very poor history of past successes in the biological control record. From an analysis of a stage-structured model for codling moth, the second instar and cocoon are identified as the most vulnerable life stages in terms of the potential for additional parasitism-based mortality to reduce the intrinsic rate of increase of codling moth populations. Criteria used in the selection of effective parasitoids for introduction to the western U.S. from Central Asia were the absence of antagonistic interactions between parasitoid species, greater than 30% parasitism observed in the region or origin, and parasitoids targeting the second instar and cocoon stages. Three species selected for introduction were the larval parasitoid Bassus rufipes, and two cocoon parasitoids Liotryphon caudatus and Mastrus ridibundus. Of these, M. ridibundus also exhibits three attributes considered to be of value from a theoretical perspective, a positive response to patches of higher host density, a shorter generation time, and production of a greater number of female offspring per host attacked.     

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.     

Traits across trophic levels interact to influence parasitoid establishment in biological control releases

A central goal in ecology is to predict what governs a species’ ability to establish in a new environment. One mechanism driving establishment success is individual species’ traits, but the role of trait combinations among interacting species across different trophic levels is less clear. Deliberate or accidental species additions to existing communities provide opportunities to study larger scale patterns of establishment success. Biological control introductions are especially valuable because they contain data on both the successfully established and unestablished species. Here, we used a recent dataset of importation biological control introductions to explore how life‐history traits of 132 parasitoid species and their herbivorous hosts interact to affect parasitoid establishment. We find that of five parasitoid and herbivore traits investigated, one parasitoid trait—host range—weakly predicts parasitoid establishment; parasitoids with higher levels of phylogenetic specialization have higher establishment success, though the effect is marginal. In addition, parasitoids are more likely to establish when their herbivore host has had a shorter residence time. Interestingly, we do not corroborate earlier findings that gregarious parasitoids and endoparasitoids are more likely to establish. Most importantly, we find that life‐history traits of the parasitoid species and their hosts can interact to influence establishment. Specifically, parasitoids with broader host ranges are more likely to establish when the herbivore they have been released to control is also more of a generalist. These results provide insight into how multiple species’ traits and their interactions, both within and across trophic levels, can influence establishment of species of higher trophic levels.     

Using optimality models to improve the efficacy of parasitoids in biological control programmes

Biological control of insect pests relies on the ability of natural enemies to limit pest populations. The behaviours expressed by natural enemies against their prey or hosts are modulated by a number of factors and a better understanding of these factors is key to obtaining more efficacious pest control. We propose here that optimality models based upon a behavioural ecology approach can provide a framework that should enable optimisation of biological control practices. We limit our discussion to parasitoid natural enemies and review the factors known to influence the behaviour of these insects. The most important areas that have been studied extensively in the behavioural ecology of insect parasitoids are addressed here: (1) residence time in a host patch, (2) clutch size, (3) sex ratio, (4) host and patch marking, and (5) diet choice. We discuss the implications of the incorporation of these optimality models into efficacious biological control practices and suggest areas where a better knowledge of the behavioural ecology of these insects could improve the efficacy of parasitoid‐based pest control.     

Avoiding conflicts between insect and weed biological control: selection of non-target species to assess host specificity of cabbage seedpod weevil parasitoids

Abstract:  Classical biological control of insect pests and weeds may lead to potential conflicts, where insect pests are closely related to weed biological control agents. Such a conflict may occur in the classical biological control of the cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham) in North America, which belongs to the same subfamily, Ceutorhynchinae, as a number of agents introduced or proposed for introduction against non-indigenous invasive weed species. We propose a step-by-step procedure to select non-target species and thereby to develop a non-target species test list for screening candidate entomophagous biological control agents of a herbivore pest insect in a way that would simultaneously evaluate non-target potential on weed biological control agents and other non-target species. Using these recommendations, we developed a non-target test list for host specificity evaluations in the area of origin (Europe) and the area of introduction (North America) for cabbage seedpod weevil parasitoids. Scientifically based predictions on expected host–parasitoid interactions and ecological information about the ecological host range in the area of origin can help avoid conflicts, while still allowing the introduction of safe and effective agents against both insect pests and weeds.     

Effect of adult feeding and timing of host exposure on the fertility and longevity of the parasitoid Anaphes flavipes

The parasitoid Anaphes flavipes (Foerster) (Hymenoptera: Mymaridae) is a gregarious egg parasitoid which is widely used in biological control against important crop pest beetles of the genus Oulema (Coleoptera: Chrysomelidae). Here, we present the first experimental examination of the influence of adult feeding and timing of host exposure on the longevity and fertility of this parasitoid. We confirmed a positive effect of adult feeding on longevity of both sexes. Fed parasitoids lived 3× longer than unfed ones. On the other hand, adult feeding and feeding time had no effect on female fertility. The number of hatched offspring was not increased by adult feeding, which suggests that the parasitoid emerges with already mature ovaries (proovigenic type). However, the fertility of fed females was strongly influenced by the timing of host egg exposure. By providing distinct groups of parasitoids with host eggs at different times, we were able to show lower fertility of fed females that had been offered host eggs more than 24 h after hatching. Our results thus show that the parasitoid's fertility is determined by her age at the time of parasitization rather than by feeding.     

Factors affecting growth in the koinobiont endoparasitoid Venturia canescens in the flour moth Ephestia kuehniella

With resistance of insect pests to synthetic pesticides on the increase, the role of parasitoid wasps as biological control agents is expanding in pest and resistance management strategies. One of the predictors of reproductive success of endoparasitoids is the relative size of the wasp at host emergence. While in idiobiont parasitoids, where the host stops feeding after parasitism, the wasp size is determined by the host size at the time of parasitism; the size of koinobiont wasps, where the host continues to feed after parasitism, is dependent on additional factors. Here we show that the host mass and temperature are important factors that determine survival and development of the koinobiont endoparasitoid Venturia canescens in late instar larvae of the flour moth Ephestia kuehniella.     

Invertebrate predation of 15N-marked prey in semi-field wheat enclosures

One of the most famous examples of successful, classical biological control in Japan is the introduction of the parasitoids Coccobius fulvus and Aphytis yanonensis against the citrus pest arrowhead scale Unaspis yanonensis. Together, they comprise a host‐parasitoid system that has been demonstrated to be stable. To test the conventional theory that successful biological control of pests occurs through the establishment of a low stable equilibrium, brought about by the density‐dependent responses of natural enemies to the pest species, sampling was carried out at five sites in the field during 2000 and 2001 to examine the relationship between the rate of parasitism by C. fulvus and the density of its host. The data were analysed using three statistical techniques at nine spatial scales. Contrary to conventional theoretical predictions, each method of analysis detected very little density‐dependence at any spatial level in this study. Parasitoid aggregations independent of host density were not sufficient to stabilise host–parasitoid interactions. Our results suggest that neither spatial density‐dependent nor density‐independent parasitism is necessary for successful biological control, or for the stability of the host–parasitoid system. We propose an alternative mechanism: a spatial refuge induced by parasitoid introduction may stabilise a system.     

Thermal change alters the outcome of behavioural interactions between antagonistic partners

1. Concerns about climate change often trigger the question whether physiological and behavioural responses of species will enable them to persist. However, species do not exist alone and are largely dependent on interactions with others within communities. 2. In the present study, a mechanistic approach is used to test the hypothesis that inter‐specific differences in metabolic response to unpredictable short‐term thermal changes can change the outcome of host–parasitoid behavioural interactions. 3. The effect of a drop or a rise of 5 °C on resting metabolic rates (RMR) of the main aphid pest of cereal crops in Western Europe, the host Sitobion avenae Fabricius and its main natural enemy, the parasitoid Aphidius rhopalosiphi De Stefani‐Perez was measured. Also, defence and attack behaviours were measured for host and parasitoid separately as well as in interaction, since behavioural strategies of both species largely determine parasitism success. 4. The results showed that, when no change in temperature occurred, parasitoids had the highest oviposition rate. However, only with a rise of temperature behavioural interactions were disrupted: the parasitoid attack rate decreased whereas the aphid defence rate increased. This alteration in behaviour was associated with a stronger thermal response of RMR in hosts than in parasitoids, suggesting that species‐specific thermal responses of RMR could give valuable information on changes in the outcome of species interactions under warm spells but not under cold ones. 5. It was shown that relatively modest thermal changes with non‐lethal effects can have profound consequences for interacting co‐evolved species which may affect ecosystem services, such as biological control of pest populations.     

Pest management through tropical tree conservation

Tropical trees can provide various ecological services to adjacent agricultural environments, including maintaining and amplifying the numbers of beneficial insects. In Mexico, certain tree species harbor a diverse guild of hymenopteran parasitoids that attack pest fruit flies (Diptera: Tephritidae) and are at the same time sources of valuable hardwood timber. Indigenous trees and their associated fauna are slowly disappearing due to forest clearance and the expansion of crop monocultures. Here we explore the relationship among pest and non-pest fruit flies, their fruit-hosts and parasitoids in the context of mango orchards and surrounding patches of uncultivated vegetation and propose a novel mechanism to use these associations in favor of conservation purposes and pest management. Trees of conservation biological control interest are classified as: (1) parasitoid multiplier plants, species that serve as alternate hosts for key fruit fly pests when their commercial hosts are not available, but in which they are unusually vulnerable to parasitism; (2) parasitoid reservoir plants, native or introduced trees in whose fruits non-pest fruit flies serve as hosts to generalist parasitoids that are able to attack pest tephritids in other species of commercially grown fruit; and (3) pest-based parasitoid reservoir plants, native or introduced species that are not economically important locally, but which harbor fruit flies that would be pests in other circumstances and that serve as hosts for parasitoids of the important pests in the vicinity. Protection, multiplication and dissemination of such tree species has the potential to increase the number of naturally produced fruit fly parasitoids and could assist in the management of tephritid pests in areas where destruction of forests has impoverished the historical sources of fruit fly natural enemies. Tropical forest conservation may help resource-poor farmers reduce crop losses, increase biodiversity within fruit-growing regions and conserve native forests for both conservation purposes and commercial use of native hardwoods.     

DNA barcoding of endoparasitoid wasps in the genus Anicetus reveals high levels of host specificity (Hymenoptera: Encyrtidae)

The genus Anicetus includes economically important biocontrol agents that are introduced for control of soft and wax scale insect agricultural pests (Ceroplastes spp.). Understanding of host–parasitoid associations is critical to the successful outcome of their utilization in biological control projects. However, identification of these parasitoids is often difficult because of their small size and generally similar morphological features, and hence, studies on the host–parasitoid associations. Here, nucleotide sequence data were generated from the mitochondrial COI gene and the D2 region of 28S rRNA to assess genetic variation within and between species of Anicetus occurring in China. The results of this study support the use of the COI and the D2 region of 28S rRNA gene as useful markers in separating species of Anicetus, even in cases where morphological differences are subtle. On the other hand, the COI gene is also useful in recognizing species with much variation in morphology. DNA barcoding reveals high levels of host specificity of endoparasitoids wasps in the genus Anicetus. Our results indicate that each Anicetus species is adapted to a limited set of host species, or even are monospecific in their host choice.     

Hyperparasitism and seasonal patterns of parasitism as potential causes of low top-down control in Euproctis chrysorrhoea L. (Lymantriidae)

Pest suppression is an important ecosystem service provided by biodiversity, though antagonistic interactions may jeopardize its impact on pest suppression. Hyperparasitoids may release herbivore populations from natural enemy pressure and lead to outbreaks directly due to parasitism as well as indirect through behavioural interference. In a previous study we reported that in native populations of Euproctis chrysorrhoea L. (Lymantriidae) primary parasitism was very low and outbreaks were more likely in coastal habitats than inland. Here we hypothesise that hyperparasitoids are the underlying cause of such patterns by reporting data on direct hyperparasitism rates as well as seasonal patterns of parasitoid attack. Of the 17 primary parasitoids attacking E. chrysorrhoea, three were found to be hyperparasitized. Hyperparasitoids attack the most important E. chrysorrhoea primary parasitoids which may explain the pattern of moth density in some habitats. Seasonal patterns of parasitoids attack and flight also help to understand antagonistic interactions among E. chrysorrhoea parasitoids. We discuss the implications of our work in the context of pest control in diverse ecosystems.     

The role of transient dynamics in biological pest control: insights from a host-parasitoid community

1. Identifying natural enemies that can maintain pests at low abundances is a priority in biological control. Here, we show that experiments combined with models generate new insights into identifying effective control agents prior to their release in the field. Using a host-parasitoid community (the harlequin bug and its egg parasitoids) as a model system, we report three key findings. 2. The interplay between the host's self-limitation and the parasitoids' saturating functional response causes the long-term (steady-state) outcomes for pest suppression to differ from those of short-term (transient) dynamics. When the bug's self-limitation is moderately strong, the parasitoid with the higher attack rate and conversion efficiency (Ooencyrtus) achieves greater host suppression in the long term, but its longer handling time causes long periods of transient dynamics during which the bug can reach high abundances; when the bug's self-limitation is weak, host fluctuations amplify over time and Ooencyrtus fails at host suppression altogether. In contrast, the parasitoid with the lower attack rate and conversion efficiency but the shorter handling time (Trissolcus) induces only weak transient fluctuations of short duration and can maintain the host at low abundances regardless of the strength of the bug's self-limitation. 3. Release of multiple enemy species can compromise host suppression if an enemy that induces stronger transient fluctuations excludes one that induces weaker fluctuations. For instance, Ooencyrtus excludes Trissolcus despite having a longer handling time because of its higher conversion efficiency. The model correctly predicts the time to exclusion observed in experiments, suggesting that it captures the key biological features of the host-parasitoid interaction. 4. Intraspecific interference reduces long-term pest suppression but improves short-term pest control by reducing the magnitude and duration of transient fluctuations. 5. These results highlight the importance of transient dynamics in pest suppression. Pests are unlikely to be strongly self-limited because they attack crop monocultures. Hence, pest fluctuations are likely to dominate short-term dynamics even when the long-term outcome is a stable equilibrium. The tendency to induce strong transient fluctuations (e.g. through a long handling time) is therefore a crucial consideration when identifying effective pest control agents.     

Effects of the gregarious parasitoids,Apanteles ruficrus and A. Kariyai,on host growth and development

Two gregarious parasitoids, Apanteles ruficrus and A. kariyai attack larvae of the common armyworm, Pseudaletia separata. Their growth pattern and growth rate of the parasitoids were not affected by host age at the time of oviposition, even though host weight increased exponentially with age. Consequently, the maximal weight of a single parasitoid larva was nearly constant regardless of host instar parasitized. Parasitoid females laid more eggs in later-instar hosts than in earlier-instar hosts. When parasitized at the same age, heavily parasitized hosts attained a larger mass than lightly parasitized larvae. Therefore, the ratio of the maximal weight of the host to the parasitoid mass was nearly constant. These results indicate that host growth is regulated by the parasitoids.     

Biological control of the diamondback moth, Plutella xylostella: A review

The diamondback moth (DBM), Plutella xylostella (L.) (Lepidoptera: Plutellidae), is one of the most destructive cosmopolitan insect pests of brassicaceous crops. It was the first crop insect reported to be resistant to DDT and now, in many crucifer producing regions, it has shown significant resistance to almost every synthetic insecticide applied in the field. In certain parts of the world, economical production of crucifers has become almost impossible due to insecticidal control failures. Consequently, increased efforts worldwide have been undertaken to develop integrated pest management (IPM) programs, principally based on manipulation of its natural enemies. Although over 130 parasitoid species are known to attack various life stages of DBM, most control worldwide is achieved by relatively few hymenopteran species belonging to the ichneumonid genera Diadegma and Diadromus, the braconid genera Microplitis and Cotesia, and the eulophid genus Oomyzus. DBM populations native to different regions have genetic and biological differences, and specific parasitoid strains may be associated with the specific DBM strains. Therefore, accurate identification based on genetic studies of both host and parasitoid is of crucial importance to attaining successful control of DBM through inoculative or inundative releases. Although parasitoids of DBM larvae and pupae are currently its principal regulators, bacteria-derived products (e.g., crystal toxins from Bacillus thuringiensis) and myco-insecticides principally based on Zoophthora radicans and Beauveria bassiana are increasingly being applied or investigated for biological control. Viruses, nematodes and microsporidia also have potential as biopesticides for DBM. When an insect pest is exposed to more than one mortality factor, there is the possibility of interactions that can enhance, limit, or limit and enhance the various aspects of effectiveness of a particular control tactic. This paper reviews the effectiveness of various parasitoids and entomopathogens against DBM, interactions among them, and their possible integration into modern IPM programs.