Effects of specialist parasitoids on oviposition preference of phytophagous insects: encounter–dilution effects in a tritrophic interaction

Abstract.  1. Host plant preferences of the female diamondback moth Plutella xylostella were studied.
2. Female moths preferred conspecific-damaged cabbage plants over undamaged cabbage plants. The performance of P. xylostella larvae on conspecific-infested plants did not differ significantly from that of larvae on undamaged plants.
3.  Cotesia plutellae , the specialist parasitoid wasp of P. xylostella larvae, displayed equal preference for plants with differing levels of host-larvae damage, and the wasp attacked only one or two hosts on average before leaving an infested plant, irrespective of the number of hosts on the plant. It is hypothesised that the oviposition preferences of P. xylostella females for host plants already damaged by conspecific larvae demonstrate an encounter–dilution effect against C. plutellae .     

Infochemically mediated tritrophic interaction webs on cabbage plants

In response to damage by herbivores, plants are known to emit infochemicals that enhance the effectiveness of insect parasitoids. Studies on plant–parasitoid interactions mediated by such infochemicals have focused on the tritrophic systems in which plants are infested by a single herbivore species. In natural ecosystems, however, plants are often simultaneously infested by several herbivorous species. The present study focuses on two herbivorous species that simultaneously attack crucifer plants and their respective parasitic wasps. We first show the specific responses of the two specialist parasitic wasps [Cotesia plutellae and C. glomerata (Hymenoptera: Braconidae)] to infochemicals originating from cabbage plants (Brassica oleracea cv. Sikidori) infested by each of their respective host larvae [Plutella xylostella (Lepidoptera: Yponomeutidae) and Pieris rapae (Lepidoptera: Pieridae)]. We then coupled the two tritrophic systems on the same cabbage plants. These experiments demonstrated the presence of indirect interactions between the two species of herbivores. Overall, the results indicate the presence of infochemically mediated tritrophic interaction webs on a single plant. Received: September 1, 2000 / Accepted: February 8, 2001     

Differential parasitism of Plutella xylostella (Lepidoptera: Plutellidae) larvae by the parasitoid Cotesia plutellae (Hymenoptera: Braconidae) on two host plant species

Laboratory experiments were conducted to examine host selection by Cotesia plutellae Kurdjumov when larvae of its host, Plutella xylostella (Linnaeus), fed on Chinese cabbage, Brassica campestris L. ssp. pekinensis and those fed on common cabbage, Brassica oleracea L. var. capitata were provided simultaneously, and to investigate the roles of plant and host volatiles in mediating host selection. When C. plutellae were provided with equal numbers of host larvae on plants of the two species in one arena, the parasitoid parasitized 4- to 15-fold more host larvae on Chinese cabbage than on common cabbage. This preference changed little with host density. However, an experience of searching coupled with an oviposition in a host larva on a leaf of the less-preferred plant, common cabbage, significantly increased the preference for parasitizing host larvae on this plant and resulted in twice as many host larvae parasitized on this plant than on Chinese cabbage. Dual choice tests with a Y-tube olfactometer showed that plant volatiles from Chinese cabbage were more attractive to female C. plutellae than those from common cabbage when plants of both species were either intact or infested. In parallel to the increased parasitism on common cabbage following experience, oviposition in a host larva on this less-preferred plant significantly increased the response to volatiles emanating from that plant. These results indicate that host plants may strongly influence the foraging behaviour of C. plutellae, but their differential attractiveness to the parasitoid may be altered by experience of the parasitoid.     

Bottom-up cascading effects in a tritrophic system: interactions between plant quality and host-parasitoid immune responses

Abstract.  1. Little is known about underlying mechanisms by which plants indirectly affect parasitism success in hymenopteran endoparasitoids. The hypothesis that host-plant effects can challenge the innate immune system of an insect host was experimentally tested in this study using a model tritrophic, crucifer – lepidopteran [ Plutella xylostella (L.)] – parasitoid [ Cotesia plutellae (Kurdjumov)], system.
2. The effects of host-plant suitability on herbivore performance and parasitism were examined. The bottom-up effect of plant suitability on host-parasitoid immune responses was then evaluated using measures of cellular and humoral effectors.
3. Host-plant quality showed a significant effect on the encapsulation response of P. xylostella to first instar but not to second instar parasitoid larvae. Encapsulation was never sufficient to prevent parasitoid emergence.
4. Poor host-plant suitability suppressed phenoloxidase activity in the absence of the parasitoid. The suppressive effect of C. plutellae on phenoloxidase activity was much greater and no plant effects were detectable after insects had been parasitized.
5. Despite strong plant effects on parasitism, those on immune effectors of the host were transitory or overwhelmed by the effect of the parasitoid.
6. These results demonstrated that plant-mediated variation in parasitism success by C. plutellae were not as a result of plant nutritional status or other attributes affecting the immune function of P. xylostella , nor to host-plant effects on superparasitism.
7. In these experiments, P. xylostella was a fully permissive host to C. plutellae and host-plant-mediated effects on the innate immune response appeared to play no part in parasitoid survival within hosts.     

粉蝶盘绒茧蜂中国和荷兰种群学习行为及EAG反应的比较

昆虫的取食危害可导致植物释放的挥发物发生质和量的变化,天敌利用植物在受到植食性昆虫的危害后释放的挥发性物质来寻找寄主,这种植物挥发物在寄生蜂寻找寄主过程中扮演者重要的角色。粉蝶盘绒茧蜂(Cotesia glomerata)是菜粉蝶(pieris rapae)主要的内寄生蜂,是优良的蜂种,在生物防治上具有广阔的应用前景。分别以中国种群和荷兰种群的粉蝶盘绒茧蜂为研究对象,利用Y型嗅觉仪和触角电位(Electroantennogram,EAG)技术,比较了不同地理种群粉蝶盘绒茧蜂雌蜂的学习行为和触角电生理反应差异。旨在明确虫害植株释放的挥发物在两个地理种群中的作用。Y型嗅觉仪试验结果表明,雌蜂不同的学习经历会影响其对寄主植株的趋性行为。没有学习经历的中国种群雌蜂对虫害甘蓝挥发物较虫害紫甘蓝和虫害羽衣甘蓝挥发物表现出更强地趋性行为,无学习经历荷兰种群对虫害甘蓝挥发物同样表现出更强地趋性行为,中国种群3次间隔产卵和3次间隔气味学习使其对经历过的寄主植物挥发物趋性明显提高。荷兰种群3次间隔气味学习也会提高该蜂对经历寄主挥发物的趋性。EAG试验结果显示,两个地理种群雌蜂对所测定三类挥发物(体积比10-1)的反应强弱依次为:C6化合物>脂肪族化合物>萜类化合物;且在所测定的6种化合物剂量范围内,两个地理种群雌蜂均与trans-2--己醛和乙酸己酯(体积比10-4—10-1),壬醛、月桂烯和里那醇(体积比10-4—10-2)化合物的活性成正相关。结果表明,中国和荷兰种群雌蜂均表现出较为一致的学习能力和电生理反应。研究显示粉蝶盘绒茧蜂雌蜂可能利用甘蓝挥发物作为利它素而寻觅适宜的寄主,学习经历会明显提高该蜂对经历的寄主挥发物的趋性的行为。实验结果为菜粉蝶的生物防治提供理论基础。     

小菜蛾化学生态学研究现状与展望

本文综述了几种植物吸引或阻抑小菜蛾成虫产卵或幼虫取食的效应。完整的、机械损伤的和菜粉蝶为害的甘蓝类蔬菜释放出数十种醇、醛、酯、酮、硫化物、羧酸类、异硫氰酸酯类和萜烯类挥发性化合物。机械损伤的甘蓝和小菜蛾、菜粉蝶及蜗牛为害的甘蓝释放的挥发物引诱菜粉蝶绒茧蜂。小菜蛾为害甘蓝释放的挥发物引诱菜蛾绒茧蜂。小菜蛾性信息素基本成分是顺 -1 1 -十六碳烯醛和顺 -1 1 -十六碳烯乙酸酯。当顺 -1 1 -十六碳烯醛、顺 -1 1 -十六碳烯乙酸酯和顺 -1 1 -十六碳烯醇以 5∶5∶0 1或顺 -1 1 -十六碳烯醛、顺 -1 1 -十六碳烯乙酸酯、顺 -1 1 -十六碳烯醇和顺 -9-十四碳烯乙酸酯按70∶3 0∶1∶0 0 1比例制成的诱芯诱蛾效果较好。宜深入探究寄主植物—小菜蛾—菜蛾绒茧蜂间的通讯机制 ,开发高效诱芯。     

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.     

外源茉莉酸诱导植物反应对菜蛾绒茧蜂寄生选择行为的影响

茉莉酸是植物体内重要的伤信号分子,向植物施用外源茉莉酸后, 可诱导植物产生各种防卫反应, 如挥发物组成发生改变等, 进而影响植食性昆虫及其天敌。该文报道用不同浓度外源茉莉酸处理白菜和甘蓝后,诱导植物反应所产生的挥发物对菜蛾绒茧蜂搜索及寄生选择行为的影响。外源茉莉酸处理白菜和甘蓝后,处理植株的挥发物对菜蛾绒茧蜂的引诱力增强;与在对照植株上相比,该蜂对经茉莉酸处理后白菜植株上的小菜蛾幼虫的寄生数显著要高。表明茉莉酸处理白菜及甘蓝后,植物诱导反应导致其挥发物的作用发生变化,进而可提高该蜂的搜索和寄生效率。     

Innate responses of the parasitoidsCotesia glomerata andC. rubecula (Hymenoptera: Braconidae) to volatiles from different plant-herbivore complexes

To determine and compare innate preferences of the parasitoid speciesCotesia glomerata andC. rubecula for different plant-herbivore complexes, long-range (1-m) foraging behavior was studied in dual-choice experiments in a wind tunnel. In this study we tested the hypothesis that naive females of the specialistC. rubecula should show more pronounced preferences for different plant-herbivore complexes than females of the generalistC. glomerata. The herbivore species used were the pieridsPieris brassicae, P. rapae, P. Napi, andAporia crataegi and the nonhostsPlutella xylostella andMamestra brassicae. All herbivore species feed mainly on cabbage and wild crucifers, exceptAporia crataegi, which feeds on species of Rosaceae. Both parasitoid species preferred herbivore-damaged plants over nondamaged plants. NeitherC. rubecula norC. glomerata discriminated between plants infested by different caterpillar species, not even between plants infested by host-and nonhost species. Both parasitoid species showed preferences for certain cabbage cultivars and plant species. No differences were found in innate host-searching behavior betweenC. glomerata andC. rubecula. The tritrophic system cabbage-caterpillars-Cotesia sp. seems to lack specificity on the herbivore level, whereas on the plant level differences in attractiveness to parasitoids were found.     

Differential effects of jasmonic acid treatment of Brassica nigra on the attraction of pollinators, parasitoids, and butterflies

Herbivore-induced plant defences influence the behaviour of herbivores as well as that of their natural enemies. Jasmonic acid is one of the key hormones involved in both these direct and indirect induced defences. Jasmonic acid treatment of plants changes the composition of defence chemicals in the plants, induces volatile emission, and increases the production of extrafloral nectar. However, few studies have addressed the potential influence of induced defences on flower nectar chemistry and pollinator behaviour. These have shown that herbivore damage can affect pollination rates and plant fitness. Here, we have investigated the effect of jasmonic acid treatment on floral nectar production and the attraction of pollinators, as well as the effect on the behaviour of an herbivore and its natural enemy. The study system consisted of black mustard plants, Brassica nigra L. (Brassicaceae), pollinators of Brassica nigra (i.e., honeybees and syrphid flies), a specialist herbivore, Pieris rapae L. (Lepidoptera: Pieridae), and a parasitoid wasp that uses Pieris larvae as hosts, Cotesia glomerata L. (Hymenoptera: Braconidae). We show that different trophic levels are differentially affected by jasmonic acid-induced changes. While the herbivore prefers control leaves over jasmonic acid-treated leaves for oviposition, the parasitoid C. glomerata is more attracted to jasmonic acid-treated plants than to control plants. We did not observe differences in pollinator preference, the rates of flower visitation by honeybees and syrphid flies were similar for control and jasmonic acid-treated plants. Plants treated with jasmonic acid secreted less nectar than control plants and the concentrations of glucose and fructose tended to be lower than in nectar from control plants. Jasmonic acid treatment resulted in a lower nectar production than actual feeding damage by P. rapae caterpillars.     

The role of volatiles from cruciferous plants and pre-flight experience in the foraging behaviour of the specialist parasitoid Cotesia plutellae

The braconid Cotesia plutellae is an important larval parasitoid of the diamondback moth (Plutella xylostella), a major pest of crucifers in the tropics and sub-tropics. The in-flight searching behaviour of C. plutellae was investigated in a wind tunnel and the close-range attack behaviour observed in cages. The relative importance of volatile stimuli emanating from the plant-host-complex, oilseed rape (Brassica napus) – P. xylostella, in the long-range attraction of C. plutellae was investigated. Plants that were mechanically damaged, or damaged by P. xylostella larvae, were attractive to the parasitoid. Host-damaged leaves remained attractive to the parasitoid after removal of the host larvae. These results indicate that C. plutellae predominantly uses plant derived stimuli in its in-flight searching behaviour. An oviposition experience or contact with a host-damaged leaf prior to the bioassay significantly increased the response to these volatile cues. The foraging behaviour of C. plutellae is compared with other braconid larval parasitoids attacking lepidopteran hosts on crucifers.     

Effects of Bt plants on the development and survival of the parasitoid Cotesia plutellae (Hymenoptera: Braconidae) in susceptible and Bt-resistant larvae of the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae)

A range of crops have been transformed with delta-endotoxin genes from Bacillus thuringiensis (Bt) to produce transgenic plants with high levels of resistance to lepidopteran pests. Parasitoids are important natural enemies of lepidopteran larvae and the effects of Bt plants on these non-target insects have to be investigated to avoid unnecessary disruption of biological control. This study investigated the effects of Cry1Ac-expressing transgenic oilseed rape (Brassica napus) on the solitary braconid endoparasitoid Cotesia plutellae in small-scale laboratory experiments. C. plutellae is an important natural enemy of the diamondback moth (Plutella xylostella), the most important pest of brassica crops world-wide. Bt oilseed rape caused 100% mortality of a Bt-susceptible P. xylostella strain but no mortality of the Bt-resistant P. xylostella strain NO-QA. C. plutellae eggs laid in Bt-susceptible hosts feeding on Bt leaves hatched but premature host mortality did not allow C. plutellae larvae to complete their development. In contrast, C. plutellae developed to maturity in Bt-resistant hosts fed on Bt oilseed rape leaves and there was no effect of Bt plants on percentage parasitism, time to emergence from hosts, time to adult emergence and percentage adult emergence from cocoons. Weights of female progeny after development in Bt-resistant hosts did not differ between plant types but male progeny was significantly heavier on wildtype plants in one of two experiments. The proportion of female progeny was significantly higher on Bt plants in the first experiment with Bt-resistant hosts but this effect was not observed again when the experiment was repeated.     

Effects of Bacillus thuringiensis on Adults of Cotesia plutellae (Hymenoptera: Braconidae), a Parasitoid of the Diamondback Moth, Plutella xylostella (Lepidoptera: Plutellidae)

To complement existing information on the mortality of larvae of the wasp Cotesia plutellae attacking moth caterpillars infected with Bacillus thuringiensis (Bt) we tested the direct and indirect effects of the bacterium on adult wasp longevity and oviposition behaviour. In one experiment with female parasitoids, mean longevity (SEM) was not significantly different between females exposed to Bt (1.98 +/- 0.08 days) and those not exposed (2.18 +/- 0.13 days). In a second experiment with both males and females, Bt treatment did not significantly effect either male or female parasitoids exposed to Bt. To observe the possible effects of Bt on oviposition behaviour of C. plutellae each of 10 females were given five larvae that had been treated with Bt and five untreated larvae at the same time. All parasitoids were observed to make oviposition attempts in both untreated and treated larvae. Upon dissection of the host larvae, one or more C. plutellae eggs were found in each of the larvae in which a parasitoid attempted oviposition. There was no effect of Bt treatment on parasitoid oviposition. The mean number of ovipositions in treated larvae (4.3 +/- 0.3) was not significantly different from untreated larvae (4.7 +/- 0.2).     

Inhibition of lipoxygenase affects induction of both direct and indirect plant defences against herbivorous insects

Herbivore-induced plant defences influence the behaviour of insects associated with the plant. For biting–chewing herbivores the octadecanoid signal-transduction pathway has been suggested to play a key role in induced plant defence. To test this hypothesis in our plant—herbivore—parasitoid tritrophic system, we used phenidone, an inhibitor of the enzyme lipoxygenase (LOX), that catalyses the initial step in the octadecanoid pathway. Phenidone treatment of Brussels sprouts plants reduced the accumulation of internal signalling compounds in the octadecanoid pathway downstream of the step catalysed by LOX, i.e. 12-oxo-phytodienoic acid (OPDA) and jasmonic acid. The attraction of Cotesia glomerata parasitoids to host-infested plants was significantly reduced by phenidone treatment. The three herbivores investigated, i.e. the specialists Plutella xylostella, Pieris brassicae and Pieris rapae, showed different oviposition preferences for intact and infested plants, and for two species their preference for either intact or infested plants was shown to be LOX dependent. Our results show that phenidone inhibits the LOX-dependent defence response of the plant and that this inhibition can influence the behaviour of members of the associated insect community.     

Non-host plant extracts reduce oviposition of Plutella xylostella (Lepidoptera: Plutellidae) and enhance parasitism by its parasitoid Cotesia plutellae (Hymenoptera: Braconidae)

Botanical preparations, usually from non-host plants, can be used to manipulate the behaviour of insect pests and their natural enemies. In this study, the effects of extracts of Chrysanthemum morifolium, a non-host plant of the diamondback moth, Plutella xylostella (Linnaeus), on the olfactory and oviposition responses of this phytophagous insect and on levels of parasitism by its specialist parasitoid Cotesia plutellae (Kurdjumov) were examined, using Chinese cabbage Brassica campestris L. ssp. pekinensis as the test host plant. Olfactometer tests showed that volatiles of chrysanthemum extract-treated host plants were less attractive to P. xylostella females than those from untreated host plants; and in contrast, volatiles of the chrysanthemum extract-treated host plants were more attractive to females of its parasitoid C. plutellae than those from untreated host plants. Oviposition preference tests showed that P. xylostella females laid only a small proportion of their eggs on chrysanthemum extract-treated host plants, while ovipositing parasitoid females parasitized a much higher proportion of host larvae feeding on the treated host plants than on untreated host plants. These results suggest that certain non-host plant compounds, when applied onto a host plant, may render the plant less attractive to a phytophagous insect but more attractive to its parasitoids. Application of such non-host plant compounds can be explored to develop push-pull systems to reduce oviposition by a pest insect and at the same time enhance parasitism by its parasitoids in crops.     

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.     

小菜蛾主要寄生性天敌——菜蛾绒茧蜂与菜蛾啮小蜂间的相互作用

在28℃下,以小菜蛾3龄幼虫作寄主,研究了菜蛾绒茧蜂与菜蛾啮小蜂间的相互关系．当寄主供2种蜂同时产卵寄生时,与只供1种蜂时相比。绒茧蜂的寄生率无显著变化,而啮小蜂的寄生率则显著下降;2种蜂的合计寄生率与任一种蜂单独存在时相比无显著差异．当寄主先供绒茧蜂寄生,再供啮小蜂寄生时,绒茧蜂的成功寄生率不受影响,而啮小蜂的寄生率仅为8％～13％;啮小蜂能寄生在寄主体内的绒茧蜂高龄幼虫．绒茧蜂能寄生已被啮小蜂寄生的寄主幼虫,其子代部分个体能正常发育至成虫羽化．当已被绒茧蜂寄生和未被寄生的寄主同时存在时,啮小蜂主要寄生未被寄生的寄主．表明绒茧蜂具有竞争优势。但这种优势可因啮小蜂的寄生而被削弱．     

The influence of the host plant of diamond-back moth (Plutella xylostella) on the plant preferences of its parasitoid Cotesia plufellae in Sri Lanka

Abstract. In Y-tube olfactometer tests, female Cotesia plutellae Kurdjmov (Hymenoptera: Braconidae), a major parasitoid of Plutella xylostella (L.) in southeast Asia, preferred the odour of the brassica type (Blue Lake cabbage) on which they had developed.Such plants were even preferred to the odour of caterpillar-infested and damaged leaves of another brassica (Early Phenomenal cauliflower).However, within one brassica type, the odour of caterpillar-infested leaves was preferred to that of uninfested and undamaged leaves.Odours of both Blue Lake and Early Phenomenal were preferred to the control odour (water).However, following the transfer of the parasitoid from Blue Lake to another cabbage (Brunswick) for one generation, females no longer distinguished between Blue Lake and Early Phenomenal.