Non-target host risk assessment of the idiobiont parasitoid Bracon celer (Hymenoptera: Braconidae) for biological control of olive fruit fly in California

Non-target risk posed by an African parasitoid, Bracon celer Szépligeti (Hymenoptera: Braconidae), was assessed for a classical biological control program against olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae: Dacinae), in California, USA. Behavioral and reproductive responses to non-target tephritid species were tested with beneficial (Chaetorellia succinea [Costa] and Parafreutreta regalis Munro) (Tephritidae: Tephritinae) and native (Rhagoletis fausta [Osten Sacken]) (Tephritidae: Trypetinae) fruit fly species in successive no-choice and choice experiments under close confinement in quarantine. Non-target host-plant substrates exposed to B. celer were yellow-starthistle flower heads containing C. succinea, Cape ivy stem galls containing P. regalis, and bitter-cherry fruit containing R. fausta. The parasitoid probed all three infested non-target plant substrates, but significantly less than olives infested with B. oleae. It produced offspring from P. regalis in Cape ivy stem galls, but appeared unable to penetrate yellow-starthistle flower heads with its ovipositor. Bracon celer killed some B. oleae and R. fausta larvae without parasitism. Reproduction on P. regalis indicates that B. celer has a broad physiological host range, which, combined with the parasitoid's acceptance of all three host-plant substrates, indicates a strong potential to negatively impact non-target species. Although physical and temporal barriers to host attack may reduce risk to most non-target tephritids by B. celer in California, the parasitoid should not be released due to its risk of harming the beneficial P. regalis. Release of P. regalis is still under consideration, however, and final risk assessment should depend on whether the fly proves useful for weed control.     

Dynamics of a host–parasitoid model with Allee effect for the host and parasitoid aggregation

In this paper, a discrete-time host–parasitoid model is investigated. Two biological phenomena, the Allee effect of the host population and the aggregation of the parasitism, are considered in our mathematical model. Through extensive numerical simulations, we gain some interesting findings related to Allee effect from this research. Firstly, the ranges of parameter, in which the population dynamics is chaos, are compressed when Allee effect is added. Secondly, the sensitivity to initial conditions of the host–parasitoid system decreased after adding Allee effect. Thirdly, without Allee effect, we observed two complicated dynamics, intermittent chaos and supertransients. However, when Allee effect is included, these two phenomena are replaced by another kind of phenomenon-period alternation, where chaos is eliminated. From above three novel findings, it can be concluded that dynamic complexities are alleviated by Allee effect. This conclusion is crucial in resolving the discrepancy between real population dynamics and theoretical predictions. Furthermore, the importance of this research is to help us understand the mechanisms inducing the irregular fluctuations of the natural populations.     

Non-target organism risk assessment of MIR604 maize expressing mCry3A for control of corn rootworm

Abstract:  Event MIR604 maize expresses a modified Cry3A protein (mCry3A), for control of corn rootworm. As part of the environmental safety assessment of MIR604 maize, risks to non-target organisms of mCry3A were assessed. The potential exposure of non-target organisms to mCry3A following cultivation of MIR604 maize was determined, and the hypothesis that such exposure is not harmful was tested. The hypothesis was tested rigorously by making worst-case or highly conservative assumptions about exposure, along with laboratory testing for hazards using species taxonomically related to the target pest and species expected to have high exposure to mCry3A, or both. Further rigour was introduced by study designs incorporating long exposures and measurements of sensitive endpoints. No adverse effects were observed in any study, and in most cases exposure to mCry3A in the study was higher than the worst-case expected exposure. In all cases, exposure in the study was higher than realistic, but still conservative, estimates of exposure. These results indicate minimal risk of MIR604 maize to non-target organisms.     

A comparison of methodologies for the assessment of host preference of the gregarious egg parasitoid Trichogramma platneri

The innate preference of Trichogramma platneri for the eggs of six host species (Chrysoperla carnea (Stephens), Cydia pomonella (L.), Ephestia kuehniella (Zeller), Helicoverpa zea (Boddie), Manduca sexta (L.), and Sitotroga cerealella (Olivier)) was evaluated as the first host accepted by an individual female parasitoid when eggs were presented simultaneously. Selective exploitation of the same hosts by T. platneri was evaluated in no-choice, paired-choice, and multiple-choice tests, using number of parasitoids emerged, proportion of female offspring, and proportion of time spent on host eggs as different measures of preference. T. platneri showed a strong innate preference for C. pomonella and M. sexta. H. zea and M. sexta were the most preferred hosts and S. cerealella the least preferred, in the no-choice and choice tests. The number of progeny emerged and proportion of female offspring were equally suitable measures of host preference for T. platneri. Although no-choice and choice tests provided very similar preference ranking for T. platneri, a polyphagous species, the no-choice tests appeared poorer at separating hosts that were close in rank and multiple-choice tests were considered likely to be more realistic for more specialized control agents.     

Success of classical biocontrol agent Torymus sinensis within its expanding range in Europe

Torymus sinensis Kamijo (Hymenoptera, Torymidae), a classical biocontrol agent of chestnut gall wasp Dryocosmus kuriphilus (Hymenoptera, Cynipidae), was released in Croatia, Slovenia and Hungary in 2015. Following the introduction, the research of parasitism rates and population genetic indices on 40 different sites was performed to monitor and evaluate the success of establishment. The observed parasitism rates were unexpectedly high and negatively correlated with the distance from westernmost locality, while population genetic indices showed that populations of T. sinensis did not suffer from bottleneck‐induced founder effect phenomenon. Moreover, lack of genetic differentiation demonstrates that all populations share similar genetic structure, which could be shaped only by high levels of gene flow. We conclude that T. sinensis established viable and genetically diverse populations and successfully spread naturally from Italy across Slovenia to Croatia and Hungary.     

No loss of genetic divergence in Torymus sinensis following its release for Dryocosmus kuriphilus control in Europe

1. Arrival, establishment, and further dispersal of non-native natural enemies are considered essential for a successful biological control programme, while among the factors that may determine the success of such a programme, genetic diversity of the introduced population plays an important role in the establishment of a non-native species.
2. The Chinese parasitoid wasp Torymus sinensis Kamijo (Hymenoptera: Torymidae) was initially released in Europe in Italy to control biologically the Asian chestnut gall wasp Dryocosmus kuriphilus Yasumatsu (Hymenoptera: Cynipidae), and reduce the damage induced on sweet chestnut (Castanea sativa Miller). In the following years, T. sinensis was then released in numerous other European countries as a biological control agent of D. kuriphilus. Its presence has also been reported beyond the countries of release due to rapid natural dispersal.
3. To assess the post-release genetic diversity of D. kuriphilus, we screened T. sinensis populations from six European countries and tested the possibility of these populations suffering from frequently observed genetic effects that could threaten its successful establishment in Europe.
4. Our results exhibit that T. sinensis populations have suffered neither from the Allee effect nor from genetic bottleneck after their release and establishment in Europe, something that increases the possibility to effectively control D. kuriphilus in Europe.

     

To mark the host or the patch: Decisions of a parasitoid searching for concealed host larvae

We found evidence for patch marking in the parasitic wasp Halticoptera laevigata (Hymenoptera: Pteromalidae) foraging for concealed hosts. Wasps attack larvae of the fruit fly Myoleja lucida (Diptera: Tephritidae) in fruits of honeysuckle. A special feature of this host-parasitoid system is the limited food supply of a patch (i.e. a fruit of honeysuckle), which allows the successful development of only a single host fly larva. Females of the parasitoid H. laevigata were found to mark the host patch with a pheromone and to abandon the patch following oviposition into a single host larva. Field data revealed that eggs of the parasitoid were spread out evenly among infested patches, with several larvae of the host fly left unparasitized in those patches that contained more than one host. Since many parasitic insects mark the parasitized host after oviposition, we assumed host marking to be the ancestral character state and studied the patch-marking behaviour of H. laevigata as a derived character state as an alternative foraging strategy. We used stochastic dynamic modelling to investigate under what conditions mutant (patch) markers would be able to invade a population of normal (larval) markers. The models suggested that, under a variety of conditions, wasps marking the patch obtained higher fitness than wasps only marking the larva. Consequently, the results from our model predict the evolution of the patch-marking behaviour found in the empirical investigation. Finally, we discuss alternative pathways to the evolution of patch marking and point out under what circumstances the evolution of a patch-marking behaviour can generally be expected.     

Influence of the parasitoid Chelonus inanitus and its polydnavirus on host nutritional physiology and implications for parasitoid development

Chelonus inanitus is a solitary egg-larval endoparasitoid, which feeds on host haemolymph during its internal phase. Parasitization induces in the host Spodoptera littoralis a precocious onset of metamorphosis and a developmental arrest in the prepupal stage. At this stage the parasitoid larva emerges from the host and consumes it. We show here that parasitization and the co-injected polydnaviruses affect the nutritional physiology of the host mainly in the last larval instar. Polydnaviruses cause a reduced uptake of food and an increase in the concentration of free sugars in the haemolymph and of glycogen in whole body. The parasitoid larva, along with polydnaviruses, causes a reduction of proteins in the host's plasma and an accumulation of lipids in whole body. Dilution of host haemolymph led to a reduced concentration of lipid in parasitoid larvae and a reduced survival rate. Thus, a sufficient concentration of nutrients in the host's haemolymph appears to be crucial for successful parasitoid development. Altogether, the data show that the parasitoid and the polydnavirus differentially influence host nutritional physiology and that the accumulated lipids and glycogen are taken up by the parasitoid in its haematophagous stage as well as through the subsequent external host feeding.     

Efficiency of host utilisation by coleopteran parasitoid

In insect larvae, optimising food utilisation with respect to available meals and time is essential for achieving maximum adult body size, which is a relevant proxy of fitness. We studied the efficiency of food conversion, body size, mortality, and development time in a solitary idiobiont ectoparasitoid, Brachinus explodens (Coleoptera: Carabidae), reared in the laboratory on the pupae of another carabid genus, Amara. The efficiency of conversion index (ECI - ratio of ingested to assimilated food) was, on average, 54.1±1.1% (n=76), with a minimum of 26.9% and a maximum of 81.6%. The rate of increase in biomass gained (W(gained)) with biomass of the host was constant in females, but it decreased in males over the range of host body mass. Females, therefore, grew heavier from hosts of the same mass compared to males. Body length increased with the host mass and was correlated with W(gained) identically for both sexes. Mortality was unaffected by the host mass, but it significantly increased below 20°C. In contrast, the development time of the feeding phase of the larva increased with the host mass at 20.3 and 23.7°C, but it remained unaffected at 26.9°C and in all three temperatures considering pupal development. W(gained) increased with development time up to ca. 8 days of larval feeding at 23.7°C. To our knowledge, our data are the first on food utilisation in solitary idiobiont coleopteran ectoparasitoids, and they present the highest values of ECI in insects.     

Non-target organism effects tests on Vip3A and their application to the ecological risk assessment for cultivation of MIR162 maize

Transgenic crops producing insecticidal proteins from Bacillus thuringiensis (Bt) provide economic, environmental and health benefits by maintaining or increasing crop yields with fewer applications of insecticide. To sustain these benefits, it is important to delay the evolution of insect resistance to the proteins, and to ensure that the proteins do not harm non-target organisms, particularly those that may control secondary pests that would otherwise flourish because of reduced insecticide applications. Vip3A is a Bt vegetative insecticidal protein that is active against lepidopterous pests. It has a different mode of action from other proteins for control of Lepidoptera in current Bt crops, and when combined with these proteins, it should help to delay the evolution of pest resistance to Bt crops. This paper presents data on the effects of Vip3A on non-target organisms, and an ecological risk assessment of MIR162 maize, which expresses Vip3Aa20. Laboratory studies indicate few adverse effects of Vip3A to non-target organisms: 11 of 12 species tested showed no adverse effects when exposed to high concentrations of Vip3A relative to estimated exposures resulting from cultivation of MIR162 maize. Daphnia magna exposed to Vip3Aa20 were unaffected in terms of survival or fecundity, but grew slightly more slowly than unexposed controls. The data indicate that cultivation of MIR162 maize poses negligible risk to non-target organisms, and that crops producing Vip3A are unlikely to adversely affect biological control organisms such that benefits from reduced insecticide applications are lost.     

Regulation of host diapause by an insect parasitoid

Abstract. 1. The interaction between larval development and parasitism by the braconid wasp Cotesia koebelei (Riley), was investigated in a population of the butterfly Euphydryas editha (Boisduval) (Nymphalidae). In this population, the butterfly host has an obligatory overwintering larval diapause.
2. It was found that E. editha larvae harbouring parasitoids were more likely to pass through an extra feeding instar before entering diapause than were non-parasitized conspecifics.
3. In addition, some individuals that were experimentally exposed to multiple parasitoid attacks bypassed diapause completely; these larvae passed through five or six feeding instars, reaching sizes typical of final instar post-diapause larvae.
4. The observed effect of superparasitism occurred regardless of whether the host larvae subsequently produced mature parasitoids, suggesting that parasitoid attack is sufficient to invoke the response.
5. It is proposed that the parasitoid C.koebelei regulates the number of pre-diapause feeding instars of its insect host E. editha, and that some component of the female venom, injected at oviposition, is responsible for this regulation.     

Maternally induced host regulation by the egg parasitoid Telenomus heliothidis

ABSTRACT. The egg parasitoid Telenomus heliothidis Ashmead (Hymenoptera: Scelionidae) arrested development and prevented emergence of its host, the egg of Heliothis virescens F. (Lepidoptera: Noctuidae). Arrestment was due to a factor injected by the ovipositing parasitoid just prior to egg release. T. heliothidis prevented hatching of H. virescens eggs up to 62 h old. Implantation of the distal region of the parasitoid common oviduct also prevented host emergence. Examination of the distal common oviduct revealed large numbers of protein-containing vesicles in the cytoplasm of the oviduct epithelial cells. These vesicles may be the source of the arrestment factor. The arrestment factor did not prevent emergence of Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae), an interspecific competitor of T. heliothidis.     

Plant and host effects on the leafroller parasitoid Dolichogenidia tasmanica

Parasitism by the braconid wasp Dolichogenidia tasmanica of first instar larvae of the lightbrown apple moth Epiphyas postvittana, established on four different species of potted host plants, was assessed after 2 weeks of field exposure in an apple orchard. Parasitism varied significantly between larval host plants (apple 58%, broom 59%, clover 30%, poplar 19% ). Parasitism on potted apple seedlings of the co-evolutionary host, E. postvittana, was compared in a field trial with that of two native New Zealand leafroller species (to which D. tasmanica has had exposure for 5 decades only). Parasitism varied significantly with larval host (E. postvittana, 83%; Ctenopseustis herana, 58%;Planotortrix octo, 26% ). Larval collections were made from mature apple trees and identification of larvae was achieved by DNA analysis for the leafroller species using PCR-RFLP of ITS1 + ITS2, and for the parasitoid by specific PCR of partial 18S. Parasitism under natural field conditions on mature apple trees was not different between larval hosts (mean 32.5% ). In laboratory studies, more P. octo larvae departed in response to parasitoid probing behaviour than E. postvittana, which is likely to contribute to the difference in parasitism rates. This study conclusively shows that D. tasmanica parasitises native New Zealand leafrollers, despite their different evolutionary origins.     

Vibration-mediated interactions in a host–parasitoid system

The aim of this paper was to obtain behavioral evidence of vibration mediated interactions between the apple tentiform leafminer Phyllonorycter malella (Ger.) (Lepidoptera, Gracillariidae) and its parasitoid Sympiesis sericeicornis Nees (Hymenoptera, Eulophidae). The experimental set-up allowed the simultaneous recording on video film of both the parasitoids and the hosts behavior, thus enabling us to contrast their respective responses to the leaf vibrations produced by the other party. We analysed the one step transition probabilties from one behavioral state to the following. Active larval movements had a marked influence on the parasitoid''s behavior, while feeding and still had no detectable effect. We found no evidence for vibrotaxis on the part of the parasitoid. While parasitoid searching behavior on the leaf surface did not seem to alter the leafminers behavior, ovipositor insertions triggered a characteristic avoidance response. The described interactions are discussed in the context of the ''princess and monster'' model developed in search and game theory.     

Relationships between parasitoid host range and host defence: a comparative study of egg encapsulation in two related parasitoid species

Abstract. Parasitoid host range may proceed from traits affecting host suitability, traits affecting parasitoid foraging behaviour, or both. We tested the hypothesis that encapsulation can be used as a reliable indicator of parasitoid host range in two closely related larval endoparasitoids of Lepidoptera. Cotesia glomerata (L.) (Hymenoptera: Braconidae) is gregarious and a generalist on several species of Pieridae, whereas C. rubecula (Marshall) is solitary and specific to Pieris rapae (L.). We determined the effects of host species ( Pieris brassicae (L.), P. napi (L.) and P. rapae ) (Lepidoptera: Pieridae) and host developmental stage (early first, second and third instar) on encapsulation of parasitoid eggs. Host species and parasitoid species, as well as the resulting interaction between these two factors had significant effects on encapsulation of Cotesia eggs. Encapsulation in Pieris hosts was much lower for C. glomerata (<34%, except for second and third instar of P. rapae ) than for C. rubecula (>32%), even when the latter was parasitizing P. rapae. Encapsulation increased with the age of the larvae, although the only significant difference was for C. glomerata. Overall, P. rapae showed a stronger encapsulation reaction than P. brassicae and P. napi. Encapsulation levels of C. glomerata corresponded well to patterns of female host species and host age preference for oviposition and parasitoid larval performance. In contrast, percentages of encapsulation of C. rubecula were not consistent with host preference and host suitability. We argue that encapsulation alone is unlikely to provide a sufficient explanation for C. glomerata and C. rubecula host range.     

Matching host reactions to parasitoid wasp vibrations.

The sensory ecology of predator detection by prey has been little studied for any arthropod prey predator system, in contrast to the sensory ecology of prey finding by predators. The aim of this study was to quantify the foraging signals produced by the parasitoid Sympiesis sericeicornis (Hymenoptera: Eulophidae) and the sensory ecology of enemy detection and the avoidance behaviour of the leaf-mining host, Phyllonorycter spp. (Lepidoptera: Gracillariidae). We used synthetic vibrations approximating the signals generated by ovipositor insertions to stimulate the host in its mine. Tothe authors' knowledge, this is the first manipulative study to describe a match in the frequency range between a parasitoid foraging stimulus and a host behavioural response. We discuss our findings in relation to other predator-prey systems for which a coevolution between prey sensitivity and predator signal has been described.     

Visual recognition of the host in the parasitoid fly Exorista japonica

We presented the tachinid fly Exorista japonica with moving host models: a freeze-dried larva of the common armyworm Mythimna separata, a black rubber tube, and a black rubber sheet, to examine the effects of size, curvature, and velocity on visual recognition of the host. The host models were moved around the fly on a metal arm driven by motor. The size of the larva, the velocity of movement, and the length and diameter of the rubber tube were varied. During the presentation of the host model, fixation, approach, and examination behaviours of the flies were recorded. The fly fixated on, approached, and examined the black rubber tube as well as the freeze-dried larva. Furthermore, the fly detected the black rubber tube at a greater distance than the larva. The rubber tube elicited higher rates of approach and examination responses than the rubber sheet, suggesting that curvature affects the responses of the flies. The length, diameter, and velocity of host models had little effect on response rates of the flies. During host pursuit, the fly appeared to walk towards the ends of the tube. These results suggest that the flies respond to the leading or trailing edges of a moving object and ignore the length and diameter of the object.