Effects of insecticides on the foraging behaviour and survival of Cotesia vestalis,a larval parasitoid of the diamondback moth,Plutella xylostella

The effects of the insecticides etofenprox, malathion, diazinon, methomyl, alanycarb, clothianidin and emamectin benzoate on the foraging behaviour and survival of Cotesia vestalis (Hymenoptera: Braconidae), a larval parasitoid of the diamondback moth Plutella xylostella (Lepidoptera: Plutellidae) were investigated in the laboratory. The period required for C. vestalis females to reach P. xylostella‐infested Komatsuna (Brassica rapa) plants treated with etofenprox, methomyl or malathion was significantly longer than that to infested plants treated with emamectin benzoate or clothianidin; and the period to reach alanycarb or diazinon‐treated plants was intermediate between them. The period to reach emamectin benzoate‐ or clothianidin‐treated plants was not significantly different from that to distilled water‐sprayed plants, suggesting that etofenprox, methomyl and malathion have strong inhibitory effects on the flight response, whereas the inhibitory effects of alanycarb and diazinon are relatively weak. By contrast, emamectin benzoate and clothianidin showed no inhibitory effect. The time of residency on the clothianidin‐treated plants was significantly longer than that on other insecticide‐treated plants (etofenprox, methomyl, alanycarb, malathion or diazinon), with the time of residency on emamectin benzoate‐treated plants being intermediate between them. These results suggest that etofenprox, methomyl, alanycarb, malathion, and diazinon have a strong inhibitory effect on host‐searching behaviour, while emamectin benzoate and clothianidin have a relatively weak effect. Furthermore, the mortality of wasps after foraging on the clothianidin‐treated plants was significantly higher than after foraging on other insecticide‐treated plants (etofenprox, methomyl or malathion), with subsequent mortality on alanycarb‐, diazinon‐ and emamectin benzoate‐treated plants being intermediate between them. Our results suggest that subsequent mortality increases with decreased inhibitory effect on the foraging behaviour of C. vestalis.     

Females of Cotesia vestalis,a parasitoid of diamondback moth larvae,learn to recognise cues from aphid‐infested plants to exploit honeydew

1. To maximise their reproductive success, the females of most parasitoids must not only forage for hosts but must also find suitable food sources. These may be nectar and pollen from plants, heamolymph from hosts and/or honeydew from homopterous insects such as aphids. 2. Under laboratory conditions, females of Cotesia vestalis, a larval parasitoid of the diamondback moth (Plutella xylostella) which does not feed on host blood, survived significantly longer when held with cruciferous plants infested with non‐host green peach aphids (Myzus persicae) than when held with only uninfested plants. 3. Naïve parasitoids exhibited no preference between aphid‐infested and uninfested plants in a dual‐choice test, but those that had been previously fed aphid honeydew significantly preferred aphid‐infested plants to uninfested ones. 4. These results suggest that parasitoids that do not use aphids as hosts have the potential ability to learn cues from aphid‐infested plants when foraging for food. This flexible foraging behaviour could allow them to increase their lifetime reproductive success.     

Effects of an artificial blend of host‐infested plant volatiles on plant attractiveness to parasitic wasps

For the biological control of diamondback moth (DBM) larvae in commercial greenhouses, we have previously identified a blend of volatiles that attracted Cotesia vestalis, a parasitoid of DBM larvae. Here, we tested the effects of an artificial volatile blend on the attractiveness of komatsuna plants (Japanese mustard spinach; Brassica rapa var. perviridis) to C. vestalis under greenhouse conditions. First, we showed that female C. vestalis preferred infested komatsuna plants to uninfested plants in the greenhouse. Under the same conditions, placing the artificial attractants near both infested and uninfested plants did not affect the wasps’ preference. However, when comparing infested komatsuna plants coupled with the artificial attractants with infested plants without them, significantly more female C. vestalis were attracted to the former. The possible use of artificial C. vestalis attractants for the biological control of DBM is discussed.     

Maize plants sprayed with either jasmonic acid or its precursor,methyl linolenate,attract armyworm parasitoids,but the composition of attractants differs

Treatment of both uninfested and armyworm‐infested maize plants with jasmonic acid (JA) is known to attract the parasitic wasp, Cotesia kariyai Watanabe (Hymenoptera: Braconidae). Here, we show that treatment with a methyl ester of a JA precursor, methyl linolenate (MeLin), also causes maize plants to attract this wasp, yet does not cause elevated levels of endogenous JA. The volatile chemicals emitted from either infested or uninfested maize plants treated with MeLin were qualitatively and quantitatively different from those emitted from JA‐treated plants. Among compounds emitted from MeLin‐treated plants, α‐pinene and menthol attracted wasps in pure form in a two‐choice test using a choice chamber. A mixture of methyl salicylate, α‐copaene, and β‐myrcene also attracted wasps. In contrast, (Z)‐3‐hexenyl acetate was among the main attractants for C. kariyai in JA‐treated plants. These data show that in addition to JA, MeLin also has the potential to increase the host‐finding ability of C. kariyai, but that the composition of attractants they induce differs.     

Application of synthetic herbivore‐induced plant volatiles causes increased parasitism of herbivores in the field

We previously reported that Cotesia vestalis (Hymenoptera, Braconidae), a parasitoid of diamondback moth (DBM) (Plutella xylostella; Lepidoptera, Plutellidae) larvae, was attracted to volatiles from crucifer plants infested by moth larvae kept in a desktop acrylic box, and that a blend of four DBM‐induced plant volatiles was responsible for this attraction. In this study, using a specially designed dispenser to release the four compounds, we demonstrated that the wasp was attracted to intact komatsuna plants (Brassica rapa var. perviridis). The experiments were performed in a climate‐controlled room, which was approximately 1000 times larger than the acrylic box used previously. Similarly, using the dispenser in the field, C. vestalis females were attracted to intact komatsuna plants with the dispenser from a distance of three metres. We also examined the effect of the volatile blend on the incidence of parasitism of DBM larvae in the field. Three small containers containing DBM‐infested komatsuna plants with dispensers, and three control containers containing only infested plants (control) were arranged in two lines running perpendicular to a komatsuna field in which both DBM larvae and C. vestalis populations were maintained, at distances of 12, 30 and 70 m. The results showed that the incidence of DBM parasitism was significantly higher in containers containing dispensers than in the control containers, suggesting that the blend could potentially be applied to DBM control in agroecosystems.     

Host‐searching responses to herbivory‐associated chemical information and patch use depend on mating status of female solitary parasitoid wasps

1. In a tritrophic interaction system consisting of plants, herbivores, and their parasitoids, chemicals released from plants after herbivory are known to play important roles for many female parasitoids to find their hosts efficiently. On the plant side, chemical information associated with herbivory can act as an indirect defence by attracting the natural enemies of the host herbivores. 2. However, mated and virgin females of haplodiploid parasitoids might not necessarily respond to such chemical cues in the same way. Since virgin females can produce only sons, they might refrain from searching for hosts to invest eggs until copulation, in order to produce both sexes. 3. Here, we investigated differential host‐searching behaviours shown by mated and virgin females in the solitary parasitoid wasp, Cotesia vestalis, in response to herbivory‐associated chemical information from cruciferous plants infested by their host larvae, Plutella xylostella. 4. Mated females showed a significantly higher flight preference for host‐infested plants over intact plants, while no preference was observed with virgin females. Mated females also showed more intensive antennal searching and ovipositor probing behaviours to leaf squares with wounds caused by hosts than did virgin females. Furthermore, mated females stayed longer in host patches with higher parasitism rates than virgin females. 5. These results indicate that mating status of C. vestalis females clearly influences their host‐searching behaviour in response to herbivory‐associated chemical information and patch exploitation. Female parasitoids seem to forage for hosts depending on their own physiological condition in a tritrophic system.     

Cover Caption

Cotesia vestalis has been used as a good biological control agent for management the pest of global cruciferous plants, Plutella xylostella. The successful parasitization strictly relies on C. vestalis olfactory perception, and odorant binding protein (OBP) play a key role in searching for hosts (see pages 1354-1368). The cover photo shows C. vestalis is parasitizing the host with the help of three OBP genes expressed in C. vestalis antennae for locating P. xylostalla larva. Photo provided by Xi-Qian Ye.     

Adult experience modifies attraction of the leafminer parasitoidOpius dissitus (Hymenoptera: Braconidae) to volatile semiochemicals

Oviposition-experienced females of Opius dissitus Muesebeck, a braconid parasitoid of Liriomyza sativaeBlanchard, preferentially landed on leafminer-infested rather than uninfested lima bean (Phaseolus lunatus L.) plants in a flight tunnel assay. Both naive and oviposition-experiencedparasitoids responded strongly to odors of infested lima bean plants in a four-arm olfactometer in comparison with odors of uninfested plants, suggesting that volatile semiochemicals are used in host location. Parasitoids with an oviposition experience on lima bean (lima-experienced) spent significantly more time in the infested odor than naive individuals, however, eggplant-experienced wasps did not spend significantly more time in the infested odor field than naive wasps. When parasitoids reared on leafminers in lima bean were provided a choice between the odor of infested lima bean and the odor of infested eggplant or cotton, naive and lima-experienced wasps preferred infested lima odor. An oviposition experience on the other plant species resulted in a dramatic shift in preference. It was concluded that the experience effect was due, at least in part, to associative learning, as has been reported for other parasitoids. The parasitoids may perceive unconditioned stimuli during host contact and oviposition on an infested leaf and may associate those stimuli with volatile semiochemicals emanating from the leaf or host. Subsequently, the volatiles associated with the presence of hosts are used in directing the search for hosts.     

Close-Range Host Searching Behavior of the Stemborer Parasitoids <Emphasis Type="Italic">Cotesia sesamiae</Emphasis> and <Emphasis Type="Italic">Dentichasmias busseolae</Emphasis>: Influence of a Non-Host Plant <Emphasis Type="Italic">Melinis minutiflora</Emphasis>

Studies were conducted on the host searching behavior of the larval parasitoid Cotesia sesamiae (Cameron) (Hymenoptera: Braconidae) and the pupal parasitoid Dentichasmias busseolae Heinrich (Hymenoptera: Ichneumonidae), both of which attack lepidopteran (Crambidae, Noctuidae) cereal stemborers. The behavior of D. busseolae was observed in a diversified habitat that consisted of stemborer host plants (maize, Zea mays L. and sorghum, Sorghum bicolor (L). Moench (Poaceae)) and a non-host plant (molasses grass, Melinis minutiflora Beauv. (Poaceae)), while C. sesamiae was observed separately on host plants and molasses grass. In previous olfactometer studies, C. sesamiae was attracted to molasses grass volatiles while hboxD. busseolae was repelled. The aim of the present study was to investigate the influence of molasses grass on close-range foraging behavior of the parasitoids in an arena that included infested and uninfested host plants. Dentichasmias busseolae strongly discriminated between host and non-host plants, with female wasps spending most of the time on infested host plants and least time on molasses grass. Likewise, C. sesamiae spent more time on uninfested and infested host plants than it did on molasses grass in single choice bioassays. While on infested plants, the wasps spent more time foraging on the stem, the site of damage, than on other areas of the plant. Overall, the results indicate that presence of the non-host plant does not hinder close range foraging activities of either parasitoid.     

Effects of honeydew and insecticide residues on the distribution of foraging aphid parasitoids under glasshouse and field conditions

The opposing effects of attraction to host-derived kairomones and repellency from the pyrethroid insecticide deltamethrin were investigated with aphid parasitoids from the genus Aphidius (Hymenoptera: Aphidiinae). The spatial distribution of female parasitoids was recorded in a series of experiments conducted in a small glasshouse containing wheat plants either infested with cereal aphids, Sitobion avenae (F.) (Homoptera: Aphididae), uninfested or treated with the recommended field concentration of deltamethrin. The number of parasitoids per plant were counted at 0.5 h, 1 h and then at one hourly intervals up to 8 h after release. Parasitoids showed a strong aggregation response to aphid-infested plants compared to adjacent uninfested plants. With the introduction of insecticidetreated plants around the aphid-infested plants, parasitoids showed a greater tendency to disperse away, resulting in fewer parasitoids on plants and significantly lower rates of aphid parasitism. The degree of aphid fall-off from plants was a good indicator of parasitoid foraging activity. In field studies, using sticky traps to measure the activity of parasitoids in plots sprayed with water, deltamethrin and/or an artificial honeydew solution, repellent properties were evident for up to 2 days after application. The attraction/arrestment stimuli associated with the honeydew solution were sufficient for parasitoids to continue searching insecticide-treated areas. The implications of these findings for parasitoids searching crops contaminated with aphid-derived kairomones and insecticides are discussed.     

Relative influences of plant type and parasitoid initial density on host–parasitoid relationships in a tritrophic system

To explore the effects of bottom-up and top-down forces on the relationships between a host, Plutella xylostella (L.) (Lepidoptera, Plutellidae), and its parasitoid, Cotesia vestalis (Haliday) (Hymenoptera, Braconidae), a short-term field experiment was established as a factorial experiment using three different host plants (Brassica pekinensis cv. Yuki F1, Brassica oleracea var. capitata cv. Midorimaru F1 and B. oleracea var. botrytis cv. Snow Crown) in the presence of C. vestalis at two different levels (low and high initial release). The tritrophic interactions were monitored by census counts of live adults 20?days after parasitoid release. The mean numbers of P. xylostella and C. vestalis adults were compared using log-linear analysis of deviance. Also, differences in the levels of parasitism were analysed using logistic analysis of deviance. There was a significant effect of host plant type on the abundance of P. xylostella, the abundance of C. vestalis and the percentage parasitism of P. xylostella by C. vestalis. The mean number of P. xylostella adults per cage on common cabbage or cauliflower was significantly greater than that on Chinese cabbage. The mean number of C. vestalis adults and the proportion of hosts attacked by C. vestalis per cage were significantly greater on Chinese cabbage compared with common cabbage or cauliflower. Indeed, initial parasitoid release did not significantly affect the abundance of P. xylostella but there was a significant influence of initial parasitoid release on the abundance of C. vestalis and the levels of parasitism of P. xylostella by C. vestalis. The mean number of C. vestalis adults and the proportion of P. xylostella parasitised by C. vestalis per cage were greater in high level of parasitoid release compared with low level of parasitoid release. However, there were no significant interacting effect of the factors (plant type?×?parasitoid initial abundance) on the abundance of P. xylostella, the population size of C. vestalis and parasitism of P. xylostella by C. vestalis.     

Offering honey containing a selective insecticide as food for pests and parasitoids: another effective use

We investigated the effects of the presence of a selective insecticide, pyridalyl, in aqueous solutions of honey as food for adults of diamondback moth (DBM) Plutella xylostella (L.) and its larval parasitoid Cotesia vestalis (Halliday) on their performances. We used a commercial formulation of pyridalyl which contained 10% pyridalyl. Survival times of DBMs reared with honey solution with pyridalyl at 10 000‐fold dilution were not significantly different from those of DBMs reared with pure honey solution. However, at 1000‐fold and 100‐fold dilutions of pyridalyl in honey solution, survival times were significantly shorter than those with honey solution alone. By contrast, survival times of C. vestalis reared with honey solution with pyridalyl at 1000‐fold and 100‐fold dilution were not significantly different from those of C. vestalis reared with pure honey solution. Offering honey solution with pyridalyl at 100‐fold dilution to C. vestalis did not affect its parasitization ability or offspring sex ratio. The novel aspects of the use of selective pesticides to control DBMs using C. vestalis are discussed.     

The Role of Chemical Cues in Host and Mate Location in the Pear Psylla Cacopsylla bidens (Homoptera: Psyllidae)

Chemical communication was shown to play a role in the pear psylla, Cacopsylla bidens. Electrophysiological (EAG) and behavioral responses were investigated in males and females pear psylla . Males were found to be attracted to females, and especially to those on host plants, but not to males, uninfested host plants, or plants infested with conspecific larvae. On the other hand, females were not attracted to males or females but displayed some attraction to host plants. Furthermore, females showed a preference for uninfested pear versus plants infested with conspecific larvae. The antennae of males gave highest electroantenographic response to volatiles from pears infested with females but not males, while females, responded also toward the volatiles of pear alone. These results indicate that females of C. bidens emit sex pheromones that are attractive to the males and suggest that, host volatiles may play a role in host selection by pear psylla females.     

Role of volatile infochemicals in foraging behavior of the leafminer parasitoidDacnusa sibirica (Diptera: Agromyzidae)

Previous investigations suggested that the leafminer parasitoid Dacnusa sibirica Telenga does not use a volatile hostrelated infochemical in foraging for hosts. Parasitoids landed with equal frequencies on an uninfested tomato plant and on a tomato plant infested with larvae of the leafminer Liriomyza bryoniae (Kalt.) (Hendrikse et al., 1980). In contrast, we found that volatile infochemicals emitted by uninfested and leafminer-infested tomato plants differently affected the parasitoid 's foraging behavior in a windtunnel. This was obvious from the proportion of wasps flying upwind but not from the proportion of wasps landing on the leaves. Latency time on an uninfested tomato leaflet and proportion of latency time devoted to preflight antennal behavior were influenced by the presence of upwind infested or uninfested tomato leaves. However, these parameters were not affected by odors in the absence of visual plant stimuli. Our data provide a new view on foraging behavior of Dacnusa sibirica.     

Attraction of the specialist parasitoid Cotesia rubecula to Arabidopsis thaliana infested by host or non-host herbivore species

In this study we investigated whether in a two‐choice set‐up the parasitoid Cotesia rubecula (Marshall) (Hymenoptera, Braconidae) distinguishes between volatiles emitted by Arabidopsis thaliana (L.) Heynh. (Brassicaceae) infested with its host, Pieris rapae (L.) (Lepidoptera: Pieridae) and Arabidopsis infested with non‐host herbivores. Four non‐host herbivore species were tested: the caterpillars Plutella xylostella (L.) (Lepidoptera: Plutellidae) and Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae), both chewing insects, the spider mite Tetranychus urticae (Koch) (Acari: Tetranychidae), which punctures parenchymal cells, and the aphid Myzus persicae (Sulzer) (Hemiptera: Aphidoidea), which is a phloem‐feeder. Compared with undamaged plants, C. rubecula females were more attracted to Arabidopsis plants infested by P. rapae, P. xylostella, S. exigua, or T. urticae, but not to plants infested by M. persicae. The parasitoids preferred host‐infested plants to spider mite‐ or aphid‐infested plants, but not to plants infested with non‐host caterpillars (P. xylostella or S. exigua). The data show that when Arabidopsis plants are infested with a leaf tissue‐damaging herbivore they emit a volatile blend that attracts C. rubecula females and the wasps only discriminate between a host and non‐host herbivore when the type of damage is different (chewing vs. piercing). When Arabidopsis is infested with a herbivore that hardly damages leaf tissue, C. rubecula females are not attracted. These results may be explained by differences in the amount of damage and in the relative importance of different signal‐transduction pathways induced by different types of herbivores.     

Diamondback moth females oviposit more on plants infested by non‐parasitised than by parasitised conspecifics

Abstract 1. When offered a choice, female diamondback moths (Plutella xylostella) oviposited more eggs on plants with non‐parasitised conspecific larvae than on plants with parasitised larvae. 2. The leaf area consumed by parasitised larvae was significantly lower than that by non‐parasitised larvae. However, this quantitative difference in larval damage did not explain the female’s ability to discriminate between plants with parasitised and non‐parasitised larvae, as females showed an equal oviposition preference for plants infested by higher or lower densities of non‐parasitised larvae. 3. Pupal weight and duration of the larval stage of P. xylostella were independent of whether larvae were reared on plants that were previously infested by either non‐parasitised or parasitised larvae. 4. The larval parasitoid Cotesia vestalis did not distinguish between plants infested by non‐parasitised larvae and plants infested by larvae that had already been parasitised by conspecific wasps. 5. Based on these data, it can be concluded that the moth oviposition preference for plants infested by non‐parasitised conspecifics relative to plants infested by parasitised conspecifics was not explained by plant quality or by the attractiveness of plants towards wasps. It is hypothesised that one of the reasons for this preference is avoidance of plants where a relatively high risk of parasitism is expected due to the emergence of parasitoids from the parasitised host larvae.     

Pea aphids (Acyrthosiphon pisum Harris) reduce secretion of extrafloral nectar in broad bean (Vicia faba)

1. Herbivores sometimes suppress plant defences. This study tested whether the presence of pea aphids (Acyrthosiphon pisum Harris) on broad bean (Vicia faba) led to decreased secretion of extrafloral nectar (EFN) which functions as an indirect plant defence against herbivores. 2. To determine effects of aphid infestation on EFN secretion, a comparison was done between EFN secretion in uninfested plants and that in plants infested by A. pisum and another aphid species (Aphis craccivora Koch). 3. When broad bean plants were infested by A. pisum, they secreted significantly smaller amounts of EFN than did uninfested plants and A. craccivora‐infested plants. There was no significant difference in EFN secretion between uninfested plants and A. craccivora‐infested plants. The number of extrafloral nectaries did not differ among the three treatments. 4. These results suggest that A. pisum reduced EFN production in broad bean plants.     

Pre- and post-landing response of the parasitoid Encarsia formosa to whitefly hosts on Gerbera jamesonii

One of the factors that may complicate biological control of the greenhouse whitefly on Gerbera jamesonii by Encarsia formosa is the rosette shape of this ornamental, which differs from the vertical shape of most vegetable plants (cucumber, egg plant, tomato, etc.). Therefore, host-habitat location and the behaviour prior to landing on uninfested and infested leaves was studied. Attraction of E. formosa from a short distance by infested leaves could not be detected: the parasitoid females landed at random on uninfested and infested leaves. After the first landing, a redistribution of the wasps occurred on the leaves. After 24 h three times as many wasps were found on the infested leaves than on uninfested ones. In a dispersal experiment with four plants, E. formosa appeared to have no preference for landing on leaves of the medium age class, which is the age class on which most of the whiteflies in a suitable stage for parasitism occur. Twenty percent of the parasitoids were found on the plants 20 min after releasing them. These results were independent of the plant cultivar and the host density on the plants. In the course of 8 h, the number of E. formosa females recovered from plants increased linearly, and this increase was greater on plants where hosts were present and also greater on the plant cultivar with the lowest trichome density. After 24 h, the percentage of females was highest (56%) on plants with the highest host density. E. formosa females were arrested on leaves where hosts were present. Contrary to our expectation, the results from the two G. jamesonii cultivars that differed strongly in leaf hairiness were not significantly different in most experiments. Only at the high host density was parasitism found to be lower on the cultivar with the higher hair density. Parasitoids may walk on top of the `hair coverlet' of cultivars with high trichome density and, therefore, be hampered less than expected.