Targeting diamondback moths in greenhouses by attracting specific native parasitoids with herbivory-induced plant volatiles

植物の香りで特定の天敵を誘引し、標的とした害虫の発生抑制に成功 --植物の香りを用いた新しい害虫防除法--. 京都大学プレスリリース. 2020-12-02.We investigated the recruitment of specific parasitoids using a specific blend of synthetic herbivory-induced plant volatiles (HIPVs) as a novel method of pest control in greenhouses. In the Miyama rural area in Kyoto, Japan, diamondback moth (DBM) (Plutella xylostella, Lepidoptera: Plutellidae) larvae are an important pest of cruciferous crops in greenhouses, and Cotesia vestalis (Hymenoptera: Braconidae), a larval parasitoid of DBM, is found in the surrounding areas. Dispensers of HIPVs that attracted C. vestalis and honey feeders were set inside greenhouses (treated greenhouses). The monthly incidence of DBMs in the treated greenhouses was significantly lower than that in the untreated greenhouses over a 2-year period. The monthly incidences of C. vestalis and DBMs were not significantly different in the untreated greenhouses, whereas monthly C. vestalis incidence was significantly higher than monthly DBM incidence in the treated greenhouses. Poisson regression analyses showed that, in both years, a significantly higher number of C. vestalis was recorded in the treated greenhouses than in the untreated greenhouses when the number of DBM adults increased. We concluded that DBMs were suppressed more effectively by C. vestalis in the treated greenhouses than in the untreated greenhouses

Oviposition Experience of Parasitoid Wasps with Nonhost Larvae Affects their Olfactory and Contact-Behavioral Responses toward Host- and Nonhost-Infested Plants

In nature, parasitoid wasps encounter and sometimes show oviposition behavior to nonhost species. However, little is known about the effect of such negative incidences on their subsequent host-searching behavior. We tested this effect in a tritrophic system of maize plants (Zea mays), common armyworms (hosts), tobacco cutworms (nonhosts), and parasitoid wasps, Cotesia kariyai. We used oviposition inexperienced C. kariyai and negative-experienced individuals that had expressed oviposition behavior toward nonhosts on nonhost-infested maize leaves. We first observed the olfactory behavior of C. kariyai to volatiles from host-infested plants or nonhost-infested plants in a wind tunnel. Negative-experienced wasps showed significantly lower rates of taking-off behavior (Step-1), significantly longer duration until landing (Step-2), and lower rates of landing behavior (Step-3) toward nonhost-infested plants than inexperienced wasps. However, the negative-experience did not affect these three steps toward host-infested plants. A negative experience appears to have negatively affected the olfactory responses to nonhost-infested plants. The chemical analyses suggested that the wasps associated (Z)-3-hexenyl acetate, a compound that was emitted more in nonhost-infested plants, with the negative experience, and reduced their response to nonhost-infested plants. Furthermore, we observed that the searching duration of wasps on either nonhost- or host-infested plants (Step-4) was reduced on both plant types after the negative experiences. Therefore, the negative experience in Step-4 would be nonadaptive for wasps on host-infested plants. Our study indicated that the density (i.e., possible encounters) of nonhost species as well as that of host species in the field should be considered when assessing the host-searching behavior of parasitoid wasps

Herbivore-Specific, Density-Dependent Induction of Plant Volatiles: Honest or “Cry Wolf” Signals?

Plants release volatile chemicals upon attack by herbivorous arthropods. They do so commonly in a dose-dependent manner: the more herbivores, the more volatiles released. The volatiles attract predatory arthropods and the amount determines the probability of predator response. We show that seedlings of a cabbage variety (Brassica oleracea var. capitata, cv Shikidori) also show such a response to the density of cabbage white (Pieris rapae) larvae and attract more (naive) parasitoids (Cotesia glomerata) when there are more herbivores on the plant. However, when attacked by diamondback moth (Plutella xylostella) larvae, seedlings of the same variety (cv Shikidori) release volatiles, the total amount of which is high and constant and thus independent of caterpillar density, and naive parasitoids (Cotesia vestalis) of diamondback moth larvae fail to discriminate herbivore-rich from herbivore-poor plants. In contrast, seedlings of another cabbage variety of B. oleracea (var. acephala: kale) respond in a dose-dependent manner to the density of diamondback moth larvae and attract more parasitoids when there are more herbivores. Assuming these responses of the cabbage cultivars reflect behaviour of at least some genotypes of wild plants, we provide arguments why the behaviour of kale (B. oleracea var acephala) is best interpreted as an honest signaling strategy and that of cabbage cv Shikidori (B. oleracea var capitata) as a “cry wolf” signaling strategy, implying a conflict of interest between the plant and the enemies of its herbivores: the plant profits from being visited by the herbivore's enemies, but the latter would be better off by visiting other plants with more herbivores. If so, evolutionary theory on alarm signaling predicts consequences of major interest to students of plant protection, tritrophic systems and communication alike

An apparent trade-off between direct and signal-based induced indirect defence against herbivores in willow trees.

Signal-based induced indirect defence refers to herbivore-induced production of plant volatiles that attract carnivorous natural enemies of herbivores. Relationships between direct and indirect defence strategies were studied using tritrophic systems consisting of six sympatric willow species, willow leaf beetles (Plagiodera versicolora), and their natural predators, ladybeetles (Aiolocaria hexaspilota). Relative preferences of ladybeetles for prey-infested willow plant volatiles, indicating levels of signal-based induced indirect defence, were positively correlated with the vulnerability of willow species to leaf beetles, assigned as relative levels of direct defence. This correlation suggested a possible trade-off among the species, in terms of resource limitation between direct defence and signal-based induced indirect defence. However, analyses of volatiles from infested and uninfested plants showed that the specificity of infested volatile blends (an important factor determining the costs of signal-based induced indirect defence) did not affect the attractiveness of infested plant volatiles. Thus, the suggested trade-off in resource limitation was unlikely. Rather, principal coordinates analysis showed that this 'apparent trade-off' between direct and signal-based induced indirect defence was partially explained by differential preferences of ladybeetles to infested plant volatiles of the six willow species. We also showed that relative preferences of ladybeetles for prey-infested willow plant volatiles were positively correlated with oviposition preferences of leaf beetles and with the distributions of leaf beetles in the field. These correlations suggest that ladybeetles use the specificity of infested willow plant volatiles to find suitable prey patches

Data from: Fecundity of diamondback moth females when offered honey with pyridalyl, a selective insecticide

<p class="MsoNormal"><span>We previously reported that the presence of pyridalyl, a selective insecticide, in aqueous honey  (50 % v/v) negatively affects the survival of diamondback moth (<em>Plutella xylostella</em>: DBM) adults. However, it remains unclear whether toxicity of pyridalyl in aqueous honey affects the fecundity of adult female DBMs. We analyzed the survival and fecundity of adult DBM under the water, honey, or honey + pyridalyl conditions in glass tubes</span><span> containing Japanese mustard spinach (</span><em><span>Brassica rapa</span></em><span>: Komatsuna) leaves</span><span> for 10 days. The survival of adults under the honey (50 % v/v) and honey + pyridalyl (100-fold dilution) conditions was significantly higher and lower, respectively, than under the water condition during the experimental period. The number of eggs laid by DBM females each day (fecundity) under the water condition was significantly lower than that under the honey condition throughout the experimental period, except on day 1. In contrast, the numbers under the water, and honey + pyridalyl conditions were not significantly different, except on day 2 (the honey + pyridalyl condition was significantly lower). To study the effects of plants grown in pots on the survival and fecundity of DBM females, we conducted experiments using acrylic cages containing potted komatsuna plants. The survival trends under the honey, and honey + pyridalyl conditions in the cages were similar to those in the glass tubes. Fecundity was evaluated based on the total number of subsequent generations (DBM larvae and pupae) on day 10. The numbers were significantly higher in the honey condition than in the water condition. </span><span>In contrast, the number in the honey + pyridalyl condition was not significantly different from that in the water condition. Based on these findings, the possible use of pyridalyl in honey for the biological control of DBM is discussed.</span></p><p>Funding provided by: Japan Society for the Promotion of Science<br>Crossref Funder Registry ID: https://ror.org/00hhkn466<br>Award Number: 22H00425</p><p class="MsoNormal"><strong><span>Food sources </span></strong></p> <p class="MsoNormal"><span>A commercial formulation of pyridalyl (Pleo<sup>®</sup> flowable: pyridalyl 10 % in water; Sumitomo Chemical Company Limited, Osaka, Japan) was used as the selective insecticide. A 100-fold dilution of pyridalyl in aqueous honey solution was selected as the test food source (see Introduction). An aqueous honey solution (50 % v/v) was provided to DBM adults as a positive control food source. As a negative control, we offered a non-sugary food source (water only) to DBM adults.</span></p> <p class="MsoNormal"><strong><span>Experiments</span></strong></p> <p class="MsoNormal"><span>Experiments were conducted in glass tubes and acrylic cages. </span><span>Glass tube experiments were designed to isolate and examine the effects of pyridalyl on honey. Acrylic cage experiments were structured to evaluate how the combination of plants and pyridalyl in honey affected the performance of DBM adults. </span><span> </span></p> <p class="MsoNormal"><em><span>Glass tube experiment.</span></em><strong><em> </em></strong><span>The effects of different food sources on the survival and number of eggs laid by DBM females were observed in a glass tube (1.8 cm diameter; length: 12 cm) containing a piece of komatsuna leaf (1 cm × 3 cm) as an oviposition substrate (Uefune et al. 2016). A piece of cotton wool (1 cm × 1 cm) impregnated with 500</span><span> m</span><span>L of either honey or honey plus </span><span>pyridalyl </span><span>was placed in a tube. For the non-sugary food condition, a piece of moist cotton wool (1 cm × 1 cm) was placed near the tube opening. One female and one male were introduced into each tube. When females did not deposit eggs on the day following the commencement of the experiment (i.e., mating did not occur in the tube on the first day), the experiment was terminated.  The number of eggs laid on the leaf pieces and the surface of the glass tube were counted daily. The glass tubes were renewed daily using cotton wool and leaf pieces. We repeated the experiments 18 times for honey, and non-sugary food conditions and 17 times for the honey + </span><span>pyridalyl </span><span>condition by using different males and females in the </span><span>climate-controlled room (25 ± 3 °C, 50 ± 10 % relative humidity) for 10 days.</span><strong><span> </span></strong></p> <p class="MsoNormal"><em><span>Acrylic cage experiment.</span></em><span> The effects of the food source on the survival and number of the next generation (larvae and pupae) were also determined in an acrylic cage </span><span>(60 cm × 60 cm × 60 cm) equipped with two windows (25 cm × 25 cm) covered with nylon gauze on opposite sides and a 30 cm × 30 cm sliding door at the front, set in the climate-controlled room. Nine potted komatsuna plants were placed in cages (3 × 3 formations) </span><span>to study the effects of plants grown in soil on the survival and fecundity of DBM females.</span><span> To water the plants, a komatsuna pot was placed in a plastic cup (</span><span>upper diameter: 12 cm, lower diameter: 9.5 cm, depth: 6 cm</span><span>) filled with water. Three experimental conditions were examined: water only, honey, and honey + pyridalyl. Two </span><span>food-feeding </span><span>devices (either dish or bottle devices; see section below) were placed in the cage separately near the meshed windows in a symmetrical position. Three females and six males were released. The food-feeding devices were replaced with new ones three and six days after release. Observations were conducted 3, 6, and 10 d after the start of the experiment. On day-3 and day-6, the number of live DBM adults in the cage was visually counted. On day-10, the number of DBM larvae and pupae was counted.<span class="msoIns"> </span>The plants were removed, and the number of adults introduced on day 0 (dead or alive) and the larvae and pupae of the next generation were counted. The experiments for each type of </span><span>food-feeding </span><span>device were repeated three times on three experimental days in the </span><span>climate-controlled room.</span></p> <p class="MsoNormal"><strong><span>Food-feeding </span></strong><strong><span>devices</span></strong></p> <p class="MsoNormal"><span>In the acrylic cage, we used two different types of </span><span>food-feeding </span><span>devices to feed the adults. The first type had a wide accessible space for DBM adults: a plastic rectangular dish (14.0 cm </span><span>×</span><span> 10.0 cm </span><span>×</span><span> 1.5 cm) with a sheet of cotton wool in which the food source (100 mL) was impregnated (dish device). The second type was originally designed to feed <em>C. vestalis</em> which has a narrow accessible space for DBM adults: a glass vial (3.0 cm diameter; 5.8 cm height: 30 mL) with a yellow lid through which a fiber rod (1.2 cm diameter; 7.0 cm height) was vertically pierced was used to supply food (vial device) (revision of Shimoda et al., 2014). The vials were filled with 25 mL of sugary food.  </span></p&gt

The Use of Synthetic Herbivory-Induced Plant Volatiles That Attract Specialist Parasitoid Wasps, Cotesia vestalis, for Controlling the Incidence of Diamondback Moth Larvae in Open Agricultural Fields

<jats:p>We evaluated the effectiveness of using a blend of volatiles that attract <jats:italic>Cotesia vestalis</jats:italic>, a specialist parasitoid wasp of diamondback moth (DBM) larvae, to control DBM larvae on cabbage plants under open field conditions. We set three dispensers of the synthetic <jats:italic>C. vestalis</jats:italic> attractant together with one sugary-food feeder in a cabbage plot (10 m × 1 m; the treated plot) on one side of a pesticide-free open agricultural field (approximately 20 m × 20 m) from June to September in 2010 and July to August in 2011. On the other side of the field, we created a control cabbage plot of the same size in which neither dispensers nor a feeder was set. The incidences of DBM larvae and <jats:italic>C. vestalis</jats:italic> cocoons in the control and treated plots were compared. In 2010, the incidence of DBM larvae in the treated plot was significantly lower than that in the control plot. Poisson regression analyses in 2010 showed that the rate of increase in the number of <jats:italic>C. vestalis</jats:italic> cocoons along with an increase in the number of DBM larvae in the treated plot was significantly higher than that in the control plot. In 2011, the incidence in both the treated and control plots remained low (five larvae per plant or less) with no significant difference between the plots. Poisson regression analyses in 2011 showed that the number of <jats:italic>C. vestalis</jats:italic> cocoons in the treated plot was significantly higher than that in the control plot, irrespective of the number of DBM larvae. This 2-year field study suggested that the dispensers recruited native <jats:italic>C. vestalis</jats:italic> from the surrounding environment to the treated plot, and the dispensers controlled the number of DBM larvae in 2010 when the density of DBM larvae exceeded the economic injury levels for the cabbage crop. We also compared the incidences of other arthropods in the control and treated plots. The incidences of <jats:italic>Pieris rapae</jats:italic> larvae and Plusiinae spp. were not affected by the treatments. The number of aphids in the treated and control plots was inconsistent between the 2 years. Based on these 2-year results, the possible use of <jats:italic>C. vestalis</jats:italic> attractants in open agricultural fields is discussed.</jats:p&gt

Degree of specificity of infested plant volatiles and preferences of ladybeetles to willow plant volatiles.

<p>The degree of specificity of infested-plant volatiles compared with uninfested-plant volatiles was indicated by the dissimilarity distances between volatiles from uninfested and infested plants within a plant species. The relative residence time of predatory ladybeetles <i>Aiolocaria hexaspilota</i>, attracted by willow plant volatiles was defined as an index of the preferences of the ladybeetles. Erio: <i>Salix eriocarpa</i>; Chae: <i>S. chaenomeloides</i>; Inte: <i>S. integra</i>; Miya: <i>S. miyabeana</i>; Jess: <i>S. jessoensis</i>; Grac: <i>S. gracilistyla</i> and Tria: <i>S. triandra</i>.</p

Relationship between vulnerability of willow plants and preferences of ladybeetles to willow plant volatiles.

<p>Leaf areas damaged by five larvae of leaf beetle <i>Plagiodera versicolora</i> until pupation was defined as an index of vulnerability of willow plants (mean ± S.E., N = 10). The relative residence time of predatory ladybeetles <i>Aiolocaria hexaspilota</i>, attracted by willow plant volatiles was defined as an index of the preferences of the ladybeetles (mean ± S.E., N = 30). Odour source: (A) infested plants and (B) uninfested plants. Erio: <i>Salix eriocarpa</i>; Chae: <i>S. chaenomeloides</i>; Inte: <i>S. integra</i>; Miya: <i>S. miyabeana</i>; Jess: <i>S. jessoensis</i>; Grac: <i>S. gracilistyla</i> and Tria: <i>S. triandra</i>.</p

Total quantities of infested plant volatiles and indirect defence level.

<p>The relative residence time of predatory ladybeetles <i>Aiolocaria hexaspilota</i>, attracted by infested willow plant volatiles was defined as an index of induced indirect defence level of willow plant species (mean ± S.E., N = 30). Erio: <i>Salix eriocarpa</i>; Chae: <i>S. chaenomeloides</i>; Inte: <i>S. integra</i>; Miya: <i>S. miyabeana</i>; Jess: <i>S. jessoensis</i>; Grac: <i>S. gracilistyla</i> and Tria: <i>S. triandra</i>. The value of total quantities of infested plant volatiles represents mean (± S.E.) for four samples.</p

Relationship between oviposition preferences of leaf beetles and preferences of ladybeetles to willow plant volatiles.

<p>The number of eggs laid by leaf beetles <i>Plagiodera versicolora</i> was defined as an index of oviposition preferences of leaf beetles (mean ± S.E., N = 9). The relative residence time of predatory ladybeetles <i>Aiolocaria hexaspilota</i>, attracted by willow plant volatiles was defined as an index of the preferences of the ladybeetles (mean ± S.E., N = 30). Odour source: (A) infested plants and (B) uninfested plants. Erio: <i>S. eriocarpa</i>; Chae: <i>S. chaenomeloides</i>; Inte: <i>S. integra</i>; Miya: <i>S. miyabeana</i>; Jess: <i>S. jessoensis</i>; Grac: <i>S. gracilistyla</i> and Tria: <i>S. triandra</i>.</p