Behavior Matters-Future Need for Insect Studies on Odor-Mediated Host Plant Recognition with the Aim of Making Use of Allelochemicals for Plant Protection.

Allelochemicals, chemical cues that, among other things, mediate insect-plant interactions, such as host plant recognition, have attracted notable interest as tools for ecological control of pest insects. Advances have recently been made in methods for sampling and analyzing volatile compounds and technology for tracking insects in their natural habitat. However, progress in odor-mediated behavioral bioassays of insects has been relatively slow. This perspective highlights this odor-mediated insect behavior, particularly in a natural setting and considering the whole behavioral sequence involved in the host location, which is the key to understanding the mechanisms underlying host plant recognition. There is thus a need to focus on elaborate behavioral bioassays in future studies, particularly if the goal is to use allelochemicals in pest control. Future directions for research are discussed.

Root-associated entomopathogenic fungi manipulate host plants to attract herbivorous insects.

Root-associated entomopathogenic fungi (R-AEF) indirectly influence herbivorous insect performance. However, host plant-R-AEF interactions and R-AEF as biological control agents have been studied independently and without much attention to the potential synergy between these functional traits. In this study, we evaluated behavioral responses of cabbage root flies [Delia radicum L. (Diptera: Anthomyiidae)] to a host plant (white cabbage cabbage Brassica oleracea var. capitata f. alba cv. Castello L.) with and without the R-AEF Metarhizium brunneum (Petch). We performed experiments on leaf reflectance, phytohormonal composition and host plant location behavior (behavioral processes that contribute to locating and selecting an adequate host plant in the environment). Compared to control host plants, R-AEF inoculation caused, on one hand, a decrease in reflectance of host plant leaves in the near-infrared portion of the radiometric spectrum and, on the other, an increase in the production of jasmonic, (+)-7-iso-jasmonoyl-L-isoleucine and salicylic acid in certain parts of the host plant. Under both greenhouse and field settings, landing and oviposition by cabbage root fly females were positively affected by R-AEF inoculation of host plants. The fungal-induced change in leaf reflectance may have altered visual cues used by the cabbage root flies in their host plant selection. This is the first study providing evidence for the hypothesis that R-AEF manipulate the suitability of their host plant to attract herbivorous insects.

The Potential for Decision Support Tools to Improve the Management of Root-Feeding Fly Pests of Vegetables in Western Europe.

Several important vegetable crops grown outdoors in temperate climates in Europe can be damaged by the root-feeding larvae of Diptera (Delia radicum, Delia floralis, Chamaepsila rosae, Delia platura, Delia florilega, Delia antiqua). Knowledge of pest insect phenology is a key component of any Integrated Pest Management (IPM) strategy, and this review considers the methods used to monitor and forecast the occurrence of root-feeding flies as a basis for decision-making by growers and the ways that such information can be applied. It has highlighted some current management approaches where such information is very useful for decision support, for example, the management of C. rosae with insecticidal sprays and the management of all of these pests using crop covers. There are other approaches, particularly those that need to be applied at sowing or transplanting, where knowledge of pest phenology and abundance is less necessary. Going forward, it is likely that the number of insecticidal control options available to European vegetable growers will diminish and they will need to move from a strategy which often involves using a single 'silver bullet' to a combination of approaches/tools with partial effects (applied within an IPM framework). For the less-effective, combined methods, accurate information about pest phenology and abundance and reliable decision support are likely to be extremely important.

Attraction of Chrysotropia ciliata (Neuroptera, Chrysopidae) Males to P-Anisaldehyde, a Compound with Presumed Pheromone Function.

In a field-trapping experiment with plant volatiles, we observed notably high attraction of green lacewing (Chrysotropia ciliata) males to the compound p-anisaldehyde. Based on this finding, we initiated the present study to elucidate this phenomenon and to investigate the chemical ecology of C. ciliata. Scanning electron microscopy revealed elliptical glands abundantly distributed on the 2nd to 6th abdominal sternites of C. ciliata males, whereas females of the species completely lacked such glands. No p-anisaldehyde was found in extractions of body parts of C. ciliata. Methyl p-anisate and p-methoxybenzoic acid were identified exclusively in the extract from abdominal segments 2-8 of males. Field-trapping experiments revealed no attraction of C. ciliata to either methyl p-anisate or p-methoxybenzoic acid. In contrast, males showed marked attraction to p-anisaldehyde in the field and antennae showed strong responses to this compound. Headspace collections in the field from living insects in their natural environment and during their main daily activity period indicated that p-anisaldehyde was emitted exclusively by C. ciliata males. Our overall results suggest that p-anisaldehyde might serve as a male-produced pheromone that attracts conspecific C. ciliata males. Here, we discuss hypotheses regarding possible mechanisms involved in regulation of p-anisaldehyde production, including involvement of the compounds methyl p-anisate and p-methoxybenzoic acid, and the potential ecological function of p-anisaldehyde in C. ciliata.

Kairomone-assisted trap cropping for protecting spring oilseed rape (Brassica napus) from pollen beetles (Coleoptera: Nitidulidae).

BACKGROUND: Pollen beetles are key pests in oilseed rape (OSR) production. These beetles use visual and olfactory cues to locate their host plants at specific phenological stages, hence trap cropping may represent an alternative pest control strategy. In this study, a trap crop strategy for spring OSR was developed. To elaborate such a trap cropping system, a pest control measure that eradicates the attracted beetles in the trap crop before they migrate further into the main crop was included in the final trap cropping strategy. RESULTS: Testing yellow-flowering turnip rape and one yellow- and two cream-coloured flowering OSR cultivars as potential crops in different trap cropping strategies, we found that pollen beetles clearly preferred turnip rape over the cream-coloured and yellow OSR cultivars, and preferred the yellow OSR cultivar over the two cream-coloured cultivars. This behaviour was related to the plant growth stage and associated volatile and colour signals of the tested cultivars. Using turnip rape as a trap crop and testing kairomone- or insecticide-assisted trap cropping as the pest control strategy was as effective as compared with whole fields treated with a standard pesticide. CONCLUSION: Combining a turnip rape cultivar as trap crop with kairomone traps placed in the trap crop as a killing agent may enable renunciation of pesticides in spring OSR production. © 2020 Society of Chemical Industry.

Recruiting on the Spot: A Biodegradable Formulation for Lacewings to Trigger Biological Control of Aphids.

Upon herbivory, plants release herbivore-induced plant volatiles (HIPVs), which induce chemical defenses in the plant as well as recruit natural enemies. However, whether synthetic HIPVs can be employed to enhance biological control in a cultivated crop in the field is yet to be explored. Here we show that a biodegradable formulation loaded with induced and food-signaling volatiles can selectively recruit the common green lacewing, Chrysoperla carnea, and reduce pest population under field conditions. In apple orchards, the new formulation attracted lacewing adults over a 4-week period, which correlated well with independent assessments of the longevity of the slow-release matrix measured through chemical analyses. In barley, lacewing eggs and larvae were significantly more abundant in treated plots, whereas a significant reduction of two aphid species was measured (98.9% and 93.6% of population reduction, for Sitobion avenae and Rhopalosiphum padi, respectively). Results show the potential for semiochemical-based targeted recruitment of lacewings to enhance biological control of aphids in a field setting. Further research should enhance selective recruitment by rewarding attracted natural enemies and by optimizing the application technique.

A Wind Tunnel for Odor Mediated Insect Behavioural Assays.

Olfaction is the most important sensory mechanism by which many insects interact with their environment and a wind tunnel is an excellent tool to study insect chemical ecology. Insects can locate point sources in a three-dimensional environment through the sensory interaction and sophisticated behavior. The quantification of this behavior is a key element in the development of new tools for pest control and decision support. A wind tunnel with a suitable flight section with laminar air flow, visual cues for in-flight feedback and a variety of options for the application of odors can be used to measure complex behaviour which subsequently may allow the identification of attractive or repellent odors, insect flight characteristics, visual-odor interactions and interactions between attractants and odors lingering as background odors in the environment. A wind tunnel holds the advantage of studying the odor mediated behavioural repertoire of an insect in a laboratory setting. Behavioural measures in a controlled setting provide the link between the insect physiology and field application. A wind tunnel must be a flexible tool and should easily support the changes to setup and hardware to fit different research questions. The major disadvantage to the wind tunnel setup described here, is the clean odor background which necessitates special attention when developing a synthetic volatile blend for field application.

Adjusting the scent ratio: using genetically modified Vitis vinifera plants to manipulate European grapevine moth behaviour.

Herbivorous insects use olfactory cues to locate their host plant within a complex olfactory landscape. One such example is the European grapevine moth Lobesia botrana, a key pest of the grape in the Palearctic region, which recently expanded both its geographical and host plant range. Previous studies have showed that a synthetic blend of the three terpenoids, (E)-ß-caryophyllene, (E)-ß-farnesene and (E)-4,8-dimethyl-1,3,7-nonatriene (DMNT), was as attractive for the moth as the complete grape odour profile in laboratory conditions. The same studies also showed that the specific ratio of these compounds in the grape bouquet was crucial because a percentage variation in any of the three volatiles resulted in almost complete inhibition of the blend's attractiveness. Here, we report on the creation of stable grapevine transgenic lines, with modified (E)-ß-caryophyllene and (E)-ß-farnesene emission and thus with an altered ratio compared to the original plants. When headspace collections from these plants were tested in wind tunnel behavioural assays, they were less attractive than control extracts. This result was confirmed by testing synthetic blends imitating the ratio found on natural and transformed plants, as well as by testing the plants themselves. With this evidence, we suggest that a strategy based on volatile ratio modification may also interfere with the host-finding behaviour of L. botrana in the field, creating avenues for new pest control methods.

Olfactory cues from different plant species in host selection by female pea moths.

In herbivorous insects specialized on few plant species, attraction to host odor may be mediated by volatiles common to all host species, by specific compounds, or combinations of both. The pea moth Cydia nigricana is an important pest of the pea. Volatile signatures of four host plant species were studied to identify compounds involved in pea moth host selection and to improve previously reported attractive volatile blends. P. sativum and alternative Fabaceae host species were compared regarding female attraction, oviposition, and larval performance. Pea moth females were strongly attracted to the sweet pea Lathyrus odoratus, but larval performance on that species was moderate. Chemical analyses of sweet pea odor and electrophysiological responses of moth antennae led to identification of seven sweet-pea-specific compounds and ten compounds common to all tested host species. Blends of these specific and common cues were highly attractive to mated pea moth females in wind tunnel and field experiments.

Attraction of pea moth Cydia nigricana to pea flower volatiles.

The pea moth Cydia nigricana causes major crop losses in pea (Pisum sativum) production. We investigated attraction of C. nigricana females to synthetic pea flower volatiles in a wind tunnel and in the field. We performed electroantennogram analysis on 27 previously identified pea plant volatiles, which confirmed antennal responses to nine of the compounds identified in pea flowers. A dose-dependent response was found to eight of the compounds. Various blends of the nine pea flower volatiles eliciting antennal responses were subsequently studied in a wind tunnel. A four-compound blend comprising hexan-1-ol, (E)-2-hexen-1-ol, (Z)-ß-ocimene and (E)-ß-ocimene was equally attractive to mated C. nigricana females as the full pea flower mimic blend. We conducted wind-tunnel tests on different blends of these four pea flower compounds mixed with a headspace sample of non-flowering pea plants. By considering the effects of such green leaf background odour, we were able to identify (Z)- and (E)-ß-ocimene as fundamental for host location by the pea moths, and hexan-1-ol and (E)-2-hexen-1-ol as being of secondary importance in that context. In the field, the two isomers of ß-ocimene resulted in trap catches similar to those obtained with the full pea flower mimic and the four-compound blend, which clearly demonstrated the prime significance of the ß-ocimenes as attractants of C. nigricana. The high level of the trap catches of female C. nigricana noted in this first field experiment gives a first indication of the potential use of such artificial kairomones in pea moth control.

Comparison of plant preference hierarchies of male and female moths and the impact of larval rearing hosts.

Selection of a suitable host plant is essential for the fitness of herbivorous insects. For polyphagous insects the underlying proximate mechanisms for host plant selection, including phenotypic plasticity, remain only partially understood. We established an experimental protocol evaluating preferences to five plant species in males and females of the polyphagous moth Spodoptera littoralis. Female preference hierarchies were assessed by oviposition decisions; those of males were assessed by the attraction to female sex pheromones in background odors of different plant species. The experiments revealed clear preference hierarchies in both males and females, which were partly overlapping in spite of the different behavioral contexts of the respective assays. Furthermore, we demonstrated strong effects of the larval rearing host on adult plant preference, where the larval host plant species was generally elevated to the most preferred plant in both sexes, without otherwise affecting the overall preference hierarchy. Our results suggest that both sexes are involved in host plant choice and that experience-based convergent intersexual plant preferences may confer selective advantages. The host plant choice is guided by a stable plant preference hierarchy, which can be modified by the larval rearing host, permitting fast adaptation to variation in local conditions and to novel environments. It may also provide a mechanism for reducing costs associated with polyphagy by functional plasticity in plant choice.