Optimal release strategies for the biological control of aphids in melon greenhouses

In this paper, we report the use of a new spatially implicit host-parasitoid model to compare different biological control strategies. We demonstrate how this approach could be used as a decision tool for crop protection by testing various strategies for the inoculative release of parasitoids to target a pest in a greenhouse. The results show that a single curative release of parasitoids is more effective than a single preventative release: that is, the best strategy is to release as many parasitoids as possible once the pest has invaded the crop if the parasitoid exhibits a type II functional response, or to do so a few days later for a type III functional response. We also confirm that multiple releases are more effective than single releases, and that the initial distribution of the pests and the functional response of the parasitoids are decisive factors for the effectiveness of the biological control (parasitoids with a type II functional response being more effective than those with a type III response).     

Effects of pupal treatment with Proteus® and Metarhizium anisopliae sensu lato on functional response of Habrobracon hebetor parasitising Helicoverpa armigera in an enclosed experiment system

The ectoparasitoid wasp, Habrobracon hebetor Say (Hymenoptera: Braconidae) is a valuable biocontrol agent attacking larval stages of many lepidopteran pests including Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). The possibility of combined application of this parasitoid wasp with other biological control agents and chemical insecticides is necessary for the success of an Integrated Pest Management (IPM) programme. One of the most important behaviours of a parasitoid refers to the number of hosts attacked by per parasitoid as a function of host density. In this research, the single and joint effects of the insecticide, Proteus® and the entomopathogenic fungus, Metarhizium anisopliae sensu lato (Metsch.) Sorokin (Hypocreales: Clavicipitaceae) (isolate M14) were studied on the functional response of H. hebetor. Newly mated females (<24?h) from treated pupae of H. hebetor were used to study the functional response of this parasitoid wasp to different densities of H. armigera larvae. A type II functional response was observed in all treatments. The results revealed that control and Proteus® treatments developed the lowest (0.5599?±?0.0373?h) and the highest (0.5709?±?0.0443?h) handling time, respectively. The most and the least values of attack rate were observed in control (0.0996?±?0.0164?h^?1) and Proteus® (0.0776?±?0.0119?h^?1) treatments, respectively. The maximum theoretical parasitism rate (T/T_h) was estimated to be 42.86 for female control wasps. After conducting field experiments on functional response along with life table parameters, M. anisopliae sensu lato (isolate M14) may be used as a compatible biocontrol agent with H. hebetor in IPM programmes of H. armigera.     

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.     

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.     

Effects of Palpita unionalis and Galleria mellonella larval densities on functional response,egg dispersion and progeny sex ratio of Habrobracon hebetor

To assess the potential of the hymenopteran ectoparasitoid, Habrobracon hebetor Say as a biological control agent, we evaluated its response to different larval densities of two pyralid hosts, Palpita unionalis Hbn. and Galleria mellonella L. The former host is a serious pest of olive trees, whereas the latter is used as a factitious host in parasitoid mass rearing. In order to study the functional response of the parasitoid, five host densities (1, 2, 3, 5, 7) of either late instar larva per Petri dish were used. The shape of the functional response curve was determined using logistic regression and could be described as a type II response for both hosts, characterised by a monotonic decelerating increase in the number of hosts attacked with increasing host density. Female parasitoids allocated more eggs to the first larva attacked than all the remaining larvae. Aggregated dispersion patterns for parasitoid egg distribution at different host densities were estimated using the Green index. Multiple visits and ovipositions by females did not significantly affect the total number of progeny produced or their sex ratio. This study has generated novel information on egg laying, egg distribution and sex ratio of H. hebetor when reared on G. mellonella and has the potential to be used in the development of sustainable biological control programmes aimed at P. unionalis in olive orchards.     

Ratio dependence in the functional response of insect parasitoids: evidence from Trichogramma minutum foraging for eggs in small host patches

Abstract.  1. Despite considerable recent debate on the suitability of ratio dependence as a more general form for the functional response in consumer–victim relationships, there have been few detailed studies to experimentally determine the response of insect parasitoids to host and parasitoid density at a local scale.
2. The experimental host, Ephestia kuehniella , was used to test for host dependence and ratio dependence in the functional response of the egg parasitoid, Trichogramma minutum , a species widely used in inundative biological control. The functional response was examined through four series of experiments in which either host density, parasitoid density, or the ratio of previously parasitised to healthy hosts was manipulated.
3. The response to host density was type I for both single and simultaneously foraging parasitoids, indicating a lack of host dependence in the functional response. The upper limit to the response was estimated as 39 hosts attacked in a 24-h period, with an estimated per capita search rate of 1.32 for individual females and 0.37 for three simultaneously searching females.
4. The response to parasitoid density provided an interference constant of unity, indicating an equal sharing of hosts and thus ratio dependence in the functional response. Female parasitoids responded to the presence of conspecifically parasitised eggs with a significant increase in search rate (1.75), but with no change to the form or upper limit of the response.
5. It is suggested that ratio dependence may be more common among insect parasitoids than previously supposed, and that a type I functional response, or the absence of host dependence, may be an emergent property of phylogenetic constraint within the monophyletic grouping of Cales , Eretmocerus , and Trichogramma .     

Accounting for differential success in the biological control of homopteran and lepidopteran pests

One of the strongest patterns in the historical record of biological control is that programmes targeted against lepidopteran pests have been far less successful than those targeted against homopteran pests. Despite fueling considerable interest in the theory of host–parasitoid interactions, biological control has few unifying principles and no theoretical basis for understanding the differential pattern of success against these two pest groups. Potential explanations considered here include competitive limitation of natural enemy establishment, the influence of antagonistic parasitoid interactions, generation time ratio, and gregarious parasitoid development. An analysis of the biological control record showed that on average six natural enemies have been introduced per pest for both pest groups, providing no evidence of a differential intensity of competition. Similarly, use of a discrete time host–parasitoid model showed that antagonistic interactions that are common among parasitoids of Lepidoptera should not limit the success of biological control as such interactions can readily be counteracted by host refuge breaking. A similar model showed that a small generation time ratio (coupled with a broad window of host attack) and gregarious development can facilitate the suppression of pest abundance by parasitoids, and both were found to be positively associated with success in the biological control record. Of the four explanations considered here, generation time ratio coupled with a broad window of host attack appears to provide the best explanation for the differential pattern of success.     

Revisiting the influence of learning in predator functional response,how it can lead to shapes different from type III

Predator/parasitoid functional response is one of the main tools used to study predation behavior, and in assessing the potential of biological control candidates. It is generally accepted that predator learning in prey searching and manipulation can produce the appearance of a type III functional response. Holling proposed that in the presence of alternative prey, at some point the predator would shift the preferred prey, leading to the appearance of a sigmoid function that characterized that functional response. This is supported by the analogy between enzyme kinetics and functional response that Holling used as the basis for developing this theory. However, after several decades, sigmoidal functional responses appear in the absence of alternative prey in most of the biological taxa studied. Here, we propose modeling the effect of learning on the functional response by using the explicit incorporation of learning curves in the parameters of the Holling functional response, the attack rate (a), and the manipulation time (h). We then study how the variation in the parameters of the learning curves causes variations in the shape of the functional response curve. We found that the functional response product of learning can be either type I, II, or III, depending on what parameters act on the organism, and how much it can learn throughout the length of the study. Therefore, the presence of other types of curves should not be automatically associated with the absence of learning. These results are important from an ecological point of view because when type III functional response is associated with learning, it is generally accepted that it can operate as a stabilizing factor in population dynamics. Our results, to the contrary, suggest that depending on how it acts, it may even be destabilizing by generating the appearance of functional responses close to type I.     

Parasitoid diversity reduces the variability in pest control services across time on farms

Recent declines in biodiversity have increased interest in the link between biodiversity and the provision and sustainability of ecosystem services across space and time. We mapped the complex network of interactions between herbivores and parasitoids to examine the relationship between parasitoid species richness, functional group diversity and the provision of natural pest control services. Quantitative food webs were constructed for 10 organic and 10 conventional farms. Parasitoid species richness varied from 26 to 58 species and we found a significant positive relationship between parasitoid species richness and temporal stability in parasitism rates. Higher species richness was associated with lower variation in parasitism rate. A functional group analysis showed significantly greater parasitoid species complementarity on organic farms, with on average more species in each functional group. We simulated parasitoid removal to predict whether organic farms experienced greater robustness of parasitism in the face of local extinctions. This analysis showed no consistent differences between the organic and conventional farm pairs in terms of loss of pest control service. Finally, it was found that the different habitats that make up each farm do not contribute equally to parasitoid species diversity, and that hedgerows produced more parasitoid species, significantly more so on organic farms.     

Functional response and egg distribution among hosts by Pseudapanteles dignus,a larval endoparasitoid of Tuta absoluta

The functional response of a biocontrol agent has been classically pointed out as a quantitative evaluation criterion to understand its killing capacity to an arthropod pest. In this paper, we revisited the functional response of the internal larval parasitoid Pseudapanteles dignus (Muesebeck) (Hymenoptera: Braconidae), a candidate for biocontrol of the South American tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), measured as the daily egg oviposition of single parasitoid females at increasing densities of T. absoluta larvae through dissection of hosts. The functional response curve of the number of parasitized hosts was fitted out taking into account the number of eggs laid and their distribution among hosts at each T. absoluta larval density. The data also allowed us to discuss the self-superparasitism strategy of this parasitoid as an adaptive trait. Pseudapanteles dignus showed a sigmoid shape functional response and a contagious distribution of eggs among hosts, favouring self-superparasitism and laying a similar number of eggs in each superparasitized host at each T. absoluta density. This research is firstly intended to ascertain about the oviposition behaviour of P. dignus and additionally to provide information on its reproduction to be applied in mass rearing procedures and augmentative releases against T. absoluta.     

Temporal autocorrelation in host density increases establishment success of parasitoids in an experimental system

Environmental variation is classically expected to affect negatively population growth and to increase extinction risk, and it has been identified as a major determinant of establishment failures in the field. Yet, recent theoretical investigations have shown that the structure of environmental variation and more precisely the presence of positive temporal autocorrelation might alter this prediction. This is particularly likely to affect the establishment dynamics of biological control agents in the field, as host–parasitoid interactions are expected to induce temporal autocorrelation in host abundance. In the case where parasitoid populations display overcompensatory dynamics, the presence of such positive temporal autocorrelation should increase their establishment success in a variable environment. We tested this prediction in laboratory microcosms by introducing parasitoids to hosts whose abundances were manipulated to simulate uncorrelated or positively autocorrelated variations in carrying capacity. We found that environmental variability decreased population size and increased parasitoid population variance, which is classically expected to extinction risk. However, although exposed to significant environmental variation, we found that parasitoid populations experiencing positive temporal autocorrelation in host abundance were more likely to persist than populations exposed to uncorrelated variation. These results confirm that environmental variation is a key determinant of extinction dynamics that can have counterintuitive effects depending on its autocorrelation structure.     

The functional response of Ibalia leucospoides (Hymenoptera: Ibaliidae), a parasitoid of Sirex noctilio (Hymenoptera: Siricidae)

We experimentally studied the functional response of the parasitoid Ibalia leucospoides on its host, Sirex noctilio. Our results show a type III functional response, which we suggest in due to a changing probability, in host encounter. We discuss its relevance to the biological control of woodwasp populations in the field.     

If and when successful classical biological control fails

Classical biological control of insects has a long history of success, with high benefit–cost ratios. However, most attempts to introduce a biological control agent have been unsuccessful, largely because the agent does not establish in the new environment. This perspectives paper discusses the possibility that even successful biological control may eventually fail, although records show that this is far from a common event. A documented example of eventual biological control failure is discussed and the prospect for future failures analyzed. Part of this analysis is based on an introduced weevil pest in New Zealand and its successful parasitoid biological control agent. The potential fragility of this host–parasitoid relationship is considered, as well as why it may indeed be starting to show signs of instability; this is particularly from the point of view of New Zealand’s often species-poor agricultural ecosystems.     

Host-Parasitoid Dynamics and the Success of Biological Control When Parasitoids Are Prone to Allee Effects

In sexual organisms, low population density can result in mating failures and subsequently yields a low population growth rate and high chance of extinction. For species that are in tight interaction, as in host-parasitoid systems, population dynamics are primarily constrained by demographic interdependences, so that mating failures may have much more intricate consequences. Our main objective is to study the demographic consequences of parasitoid mating failures at low density and its consequences on the success of biological control. For this, we developed a deterministic host-parasitoid model with a mate-finding Allee effect, allowing to tackle interactions between the Allee effect and key determinants of host-parasitoid demography such as the distribution of parasitoid attacks and host competition. Our study shows that parasitoid mating failures at low density result in an extinction threshold and increase the domain of parasitoid deterministic extinction. When proned to mate finding difficulties, parasitoids with cyclic dynamics or low searching efficiency go extinct; parasitoids with high searching efficiency may either persist or go extinct, depending on host intraspecific competition. We show that parasitoids suitable as biocontrol agents for their ability to reduce host populations are particularly likely to suffer from mate-finding Allee effects. This study highlights novel perspectives for understanding of the dynamics observed in natural host-parasitoid systems and improving the success of parasitoid introductions.     

Modelling age‐ and density‐structured reproductive biology and seasonal survival of Apanteles galleriae Wilkinson (Hym., Braconidae)

Abstract: The biology of Apanteles galleriae Wilkinson, an important biological control agent of wax moths, is well described in the literature. We developed models simulating the functional response of fecundity and female progeny proportion of adult females as a function of age, host and/or parasitoid density to integrate current knowledge. Daily pattern of age‐related fecundity and female progeny proportion of different parasitoids was also examined. We investigated the effect of sex, mating status and seasonal time on adult longevity. We derived survival data of females in two different seasonal periods. We found that 50% of adult life span is important for an efficient fecundity. The patterns of host and/or parasitoid density‐dependent fecundity and sex ratio varied considerably. The highest fecundity and female progeny proportion occurred with one parasitoid and one female equivalent host. Longevity of adults was affected by sex and month periods, but mating status did not affect their longevity. Female survival was greater between December and May relative to June and November. Our results indicated that age, host and parasitoid density, and the timing of rearing influenced the life processes of parasitoids.     

Effect of <Emphasis Type="Italic">Fopius arisanus</Emphasis> oviposition experience on parasitization of <Emphasis Type="Italic">Bactrocera dorsalis</Emphasis>

Fopius arisanus (Sonan) (Hymenoptera: Braconidae) is an important fruit fly parasitoid, successfully introduced in programs of classical biological control around the world. One aspect of its reproductive biology that has received increasing attention is the role of learning on parasitization by individual females. In this study, we examined the effect of previous oviposition opportunities on the reproductive success and progeny sex ratio of F. arisanus on eggs of Bactrocera dorsalis Hendel (Diptera: Tephritidae). Our results indicate that the proportion of eggs parasitized and parasitoid yield both increase with increasing experience, as acquired by individual females via previous oviposition opportunities. These effects are shown to be unrelated to parasitoid age out to three weeks, which we found not to have an effect on parasitization, yield, or sex ratio. We discuss the implications of our results on mass rearing and also in terms of the efficiency of this biological control agent in the field.     

Plant Resistance Affects the Olfactory Response and Parasitism Success of Cotesia vestalis

Understanding the factors influencing host-selection behavior of parasitoids is essential in studies on host-parasitoid ecology and evolution, and in combining sustainable strategies of pest management, such as host-plant resistance and biological control. The effects of host-plant resistance on the olfactory response and parasitism success by Cotesia vestalis, a parasitoid of diamondback moth (Plutella xylostella) larvae were examined. Here, it was demonstrated that host-plant resistance can strongly influence foraging behavior and parasitism success of the parasitoid. In olfactometer experiments, C. vestalis did not differentiate between crucifer plant types with similar levels of susceptibility or resistance to P. xylostella but showed a strong preference for susceptible compared with partially-resistant host plants. The influence of previous oviposition activity varied with the host-plant type experienced by the parasitoid. In cage experiments, C. vestalis preferred to parasitize P. xylostella larvae on a susceptible plant compared with larvae on a partially resistant host plant when exposed to hosts for 24 h. However, this preference appeared to be transitory, and was not found after 96 h exposure. The present study suggests that combining partial host-plant resistance with biological control by C. vestalis for the control of P. xylostella may in some circumstances be antagonistic and negatively affect parasitism success.     

Parasitic mites as part-time bodyguards of a host wasp

Some bees and wasps that host mites have peculiar pocket-like structures called acarinaria. These have long been considered as morphological adaptations to securely transfer beneficial mites into nests, and thus are thought to be the product of a mutualistic relationship. However, there has been little compelling evidence to support this hypothesis. We demonstrated that the parasitic mite Ensliniella parasitica, which uses acarinaria, increases the reproductive success of its host wasp Allodynerus delphinalis by protecting it from parasitoid wasps. Every time the parasitoid Melittobia acasta accessed a prepupal or pupal wasp host cell, adult mites attacked it, continuously clinging to it and possibly piercing the intersegmental membrane of the parasitoid with their chelicerae. Subsequent mortality of the parasitoid depended on the number of attacking mites: an average of six mites led to a 70% chance of mortality, and 10 mites led to a 100% chance of mortality. In this way, parent mites protect the food source (juvenile wasps) for themselves and ultimately for their offspring. We propose that wasps evolved acarinaria to maintain this protective guarding behaviour.     

The effect of variability on host feeding and reproductive success in parasitoids

We model the behaviour of a solitary parasitoid that can either eat a host or lay an egg on it. When the parasitoid does not die as a result of starvation, it should always lay an egg on a host. We compute the parasitoid's lifetime reproductive success in this case, and illustrate the effects of the mean time to find hosts and the variance in this time. We then develop a state-dependent model in which the decision to eat the host or lay an egg on it depend on the parasitoid's state. This model is used to explore the effects of variability in the time to find hosts on the parasitoid's lifetime reproductive success. It is shown that there can be a non-monotonic relationship between reproductive success and variability.     

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.