A comprehensive review published in the journal Crop Health synthesizes decades of research on how parasitoids, a group of more than 100,000 described insect species that kill their hosts during development, use semiochemicals to locate mates and hosts. The review traces the field from its earliest documented records, including a description of tachinid fly parasitism on silkworm caterpillars in China dating to 1096 AD, through the landmark intercontinental introductions of the late nineteenth century, to the sophisticated laboratory and field applications being developed today. The authors argue that semiochemicals serve three critical purposes in biological control: monitoring parasitoid population dynamics, optimizing mating conditions in mass-rearing facilities, and improving host orientation and localization by parasitic wasps in the field.

Parasitoids are deployed through three primary biological control approaches: classical biological control, which involves importing and establishing exotic species; augmentative biological control, which relies on mass rearing and periodic release of established species; and conservation biological control, which focuses on preserving natural enemies through environmental manipulation. Among these, augmentative biological control has attracted significant attention, with commercially developed rearing systems for the egg parasitoid Trichogramma operating worldwide. The successful release of parasitoids depends on synchronizing deployment with the vulnerable life stages of pests, achieved through either inoculative release, which re-establishes declining natural enemy populations, or inundative release, which seeks immediate pest suppression through large-scale deployment.

Once released, parasitoids face a fundamental challenge: finding mates and hosts in complex, unfamiliar environments. They navigate this challenge using a sequence of chemical cues that vary in detectability and reliability. Plant volatiles, emitted from host habitats, are abundant and highly detectable but less reliable indicators of host presence. Sex pheromones, herbivore-induced plant volatiles, and host-derived compounds, by contrast, are highly reliable but harder to detect from a distance. This trade-off, known as the reliability-detectability dilemma, shapes every stage of parasitoid foraging behavior and has driven the evolution of specialized chemosensory systems in these insects.

Sex pheromone communication in parasitoids, while less studied than in Lepidoptera, has yielded remarkable discoveries. Since the identification of bombykol in the silkworm moth, research on insect sex pheromones has been a cornerstone of chemical ecology. In parasitoids, volatile sex pheromones include aldehydes, ketones, esters, and olefins with diverse structures. Recently, tetradecanal and 2-heptadecanone, applied in a 1:4.6 ratio, were identified as sex pheromones released by female Campoletis chlorideae, restoring male attraction and eliciting characteristic courtship wing-fanning behavior when applied to washed female wasps. In addition to female-produced pheromones, some parasitoids use male-released pheromones to attract females, with the jewel wasp Nasonia vitripennis producing two hydroxy-decanolide isomers that mark the first identified male sex pheromones in parasitoids. Cuticular hydrocarbons serve as contact pheromones at close range, with compounds such as 3-methylnonacosane in Dibrachys cavus and 7-methyltetracosane in Urolepis rufipes providing critical mate suitability information.

Host localization by parasitoids involves two primary stages: long-distance host habitat searching and close-range host localization. During habitat searching, parasitoids rely on abundant but less reliable environmental cues, including plant volatiles and, increasingly recognized, microbial emissions. Recent research has shown that odors from nectar fermented by bacteria isolated from buckwheat are attractive to the egg parasitoid Trissolcus basalis, while styrene and benzaldehyde emitted by bacterial strains from the habitat of the generalist aphid parasitoid Aphidius colemani attract this parasitoid. Upon arriving at the host habitat, female parasitoids search within 1 to 2 centimeters of host-associated plants, using antennae and other chemosensory organs to probe plant tissues damaged by hosts. The chemical cues for this close-range localization fall into two categories: distress signals released by plants in response to host damage, and kairomones emitted by the host itself, including sex pheromones, aggregation pheromones, fecal odors, and body scales.

Herbivore-induced plant volatiles, or HIPVs, serve as synomones that guide parasitoids to concealed hosts. Since the 1980s, researchers have recognized that plants damaged by herbivores emit volatile compounds to recruit parasitoids for indirect defense. HIPV profiles have been characterized for crops including cotton, maize, tobacco, kidney bean, and tomato, with common components including green leaf volatiles such as (Z)-3-hexen-1-ol and (Z)-3-hexenyl acetate, monoterpenes such as (E)-beta-ocimene and linalool, sesquiterpenes such as (E)-beta-caryophyllene, and homoterpenes such as DMNT and TMTT. Recent advances in sequencing technologies have enabled what the authors call reverse chemical ecology to identify active HIPV components. In Campoletis chlorideae, transcriptome sequencing revealed that an odorant receptor called CchlOR62 is exclusively expressed in female antennae and responds to (Z)-jasmone, an HIPV component from cotton and tobacco that strongly attracts female parasitoids and significantly enhances their parasitism efficiency in early-instar bollworm larvae.

Beyond feeding-induced volatiles, oviposition by herbivorous insects induces the emission of oviposition-induced plant volatiles, or OIPVs, that function as synomones, particularly for attracting egg parasitoids. Oviposition by the pine sawfly Diprion pini on pine needles triggers volatile emissions that attract the egg parasitoid Chrysonotomyia ruforum, while volatiles emitted by bean plants following oviposition by the southern green stink bug Nezara viridula strongly attract the egg parasitoid Trissolcus basalis. Remarkably, recent research indicates that OIPVs convey precise information about egg age, with the egg parasitoid Trichogramma japonicum strongly preferring the odor of rice plants bearing 2-day-old eggs of the rice leaf folder over plants with younger or older eggs, mediated by detection of the OIPV components D-limonene and alpha-pinene. Plant pathogen infections also induce the release of volatile bouquets that parasitoids exploit, with Cotesia glomerata showing stronger preference for volatiles emitted by aphid-infested plants infected with a compatible pathogen compared with healthy plants.

Host-derived kairomones provide some of the most reliable cues for parasitoid host localization. Insect sex pheromones, owing to their high species specificity, serve as critical kairomones for natural enemies. The egg parasitoids Trichogramma chilonis and Cotesia plutellae showed significant attraction to the sex pheromone blend of the diamondback moth in olfactometer assays, while Telenomus busseolae was attracted to the sex pheromone blend of its host Sesamia nonagrioides during the calling period. Intriguingly, larval parasitoids also respond to host sex pheromones, which can persist in the environment for days and be adsorbed onto plant tissues, providing a temporal window for parasitoids to detect residual cues and locate host larvae. In wind tunnel experiments, the larval parasitoid Leptopilina heterotoma exhibited a strong preference for the sex pheromone of its host Drosophila melanogaster, specifically (Z)-11-vaccenyl acetate. Other host pheromones, including alarm, aggregation, and trail pheromones, also serve as host-finding kairomones, with the aphid alarm pheromone (E)-beta-farnesene acting as a kairomone for several aphid parasitoids and the specialist parasitoid Pseudacteon tricuspis using alarm pheromones released by worker ants to locate its host.

Decades of laboratory research on semiochemicals have opened new avenues for manipulating parasitoid behaviors through synthetic biology. By engineering plant or yeast metabolic pathways, researchers can produce specific semiochemicals, including HIPVs, host alarm pheromones, and host sex pheromones, that function as synomones and kairomones to attract parasitoids. Transgenic Arabidopsis thaliana expressing the peppermint (E)-beta-farnesene synthase gene produces this sesquiterpene, eliciting strong alarm and repellent responses in the green peach aphid while attracting and retaining the parasitoid Diaeretiella rapae. Similarly, Arabidopsis overexpressing the maize terpene synthase gene TPS10 emits a sesquiterpene blend including (E)-beta-farnesene and (E)-alpha-bergamotene, attracting the parasitoid Cotesia marginiventris. Cotton plants engineered to express DMNT-synthesis genes emit 10- to 15-fold higher DMNT levels than wild-type controls, significantly increasing recruitment of the parasitoid Peristenus spretus. Yeast cell factories have also been utilized to produce moth sex pheromones through metabolic engineering of oleaginous yeasts, with notable examples including (Z)-11-hexadecenal, the primary sex pheromone component of the cotton bollworm, and (Z)-9-tetradecenyl acetate, the primary sex pheromone component of the fall armyworm.

Companion planting, or intercropping, represents another widely adopted habitat manipulation strategy that increases the abundance of natural enemies. Intercropping maize with the molasses grass Melinis minutiflora significantly reduces stem-borer infestation and increases larval parasitism by Cotesia sesamiae, an effect attributed to volatiles such as DMNT emitted by the companion plant that repel female stem borers while attracting foraging female parasitoids. Similarly, the cornflower Centaurea cyanus is highly attractive to the parasitoid Microplitis mediator, enhancing its survival and parasitism rates. Companion plants including Desmodium intortum, Desmodium uncinatum, and Brachiaria Mulato deter oviposition by the fall armyworm on maize while attracting its larval endoparasitoids Cotesia icipe and Coccygidium luteum, effects likely driven by behavior-modifying compounds such as (Z)-3-hexenyl acetate, (E)-beta-ocimene, DMNT, (E)-beta-caryophyllene, camphor, methyl salicylate, and TMTT.

Despite these advances, field applications of semiochemicals to increase parasitoid efficacy face significant challenges stemming from the complexity of natural environments. Deploying the attractant borneol in apple orchards elevated the densities of the egg parasitoid Cyzenis albicans, which targets the winter moth, yet parasitism rates remained unaffected, likely due to the absence of oviposition-determining cues. Wheat genetically engineered to constitutively emit the aphid alarm pheromone (E)-beta-farnesene repelled aphids and attracted the parasitoid Aphidius ervi in olfactometer assays, but field trials revealed no decline in aphid populations or increase in parasitism, potentially resulting from olfactory habituation caused by prolonged odorant exposure. Parasitoids are also highly sensitive to abiotic stressors, with parasitism by Trichogramma brassicae decreasing by nearly 40 percent at temperatures exceeding 35 degrees Celsius. Plants subjected to heat, drought, or elevated ozone levels release volatile blends that closely resemble HIPVs, acting as deceptive cues that diminish parasitoid foraging efficiency, while atmospheric pollutants degrade HIPVs, further hindering host location.

The authors identify several research gaps that warrant further investigation to enhance the practical application of semiochemicals in biological control. Plants typically emit complex blends of volatile compounds, yet most studies have focused on single compounds, overlooking potential synergistic and antagonistic interactions. For example, (Z)-jasmone and (Z)-3-hexenyl acetate individually increased the parasitism efficiency of Campoletis chlorideae on bollworm larvae in indoor cage experiments, but their combination had no effect, while combining (Z)-jasmone with sex pheromones attracted both female and male parasitoids, significantly improving host location and mating success. The interactions among plants, pests, and parasitoids are highly intricate, with the maize HIPV indole attracting the parasitoid Microplitis rufiventris but also modifying the volatile profile on the body surface of Spodoptera littoralis larvae, reducing their attractiveness to the parasitoid and lowering parasitism rates. Hyperparasitoids can exploit plant-emitted synomones and host-derived kairomones to locate and parasitize primary parasitoids, undermining their efficacy in pest control. The semiochemical redundancy hypothesis posits that high local chemical diversity and concentrations may disrupt herbivore foraging through chemical disorientation and masking, which may similarly impair the ability of specialized natural enemies to locate their prey.

Current research on the regulatory effects of semiochemicals on parasitoid behavior remains largely confined to laboratory or semi-field studies, and no commercially available parasitoid attractants have been developed to date. Future efforts should prioritize large-scale field experiments to validate laboratory findings under real-world conditions, incorporating real plants and large-scale greenhouse setups to simulate field conditions. The development of effective methods for releasing semiochemicals in the field is critical, with transgenic plants engineered to emit key semiochemicals representing a promising solution, particularly with advancements in gene-editing technologies. In commercially important genera such as Trichogramma and Telenomus, no odorant receptor functions have been reported, likely due to the minute body size of these parasitoids, which poses significant challenges for behavioral monitoring and physiological manipulation. Recent advances in machine learning, such as quantitative structure-activity relationship modeling, have achieved up to 95 percent success in predicting ligands for lepidopteran odorant receptors, and the application of this approach to predict ligands for parasitoid receptors, followed by functional validation, provides a rapid method for identifying novel semiochemicals for pest control. Taken together, the metabolic engineering of plant volatiles has shown significant potential for enhancing indirect plant defense by attracting parasitoids, with transgenic plants producing and emitting (E)-beta-farnesene, (E)-beta-caryophyllene, and (E)-beta-ocimene demonstrating dual functionality, repelling pests while attracting parasitoids, making them promising candidates for novel push-pull pest management systems.

Subject of Research: Harnessing semiochemicals for parasitoid-based biological control: from laboratory identification to field applications

Article Title: Harnessing semiochemicals for parasitoid-based biological control: from laboratory identification to field applications

Article References: Guo, H., & Wang, C.-Z. (2025). Harnessing semiochemicals for parasitoid-based biological control: from laboratory identification to field applications. Crop Health, 3(1), Article 21. https://doi.org/10.1007/s44297-025-00061-4

Image Credits: AI Generated

DOI: 10.1007/s44297-025-00061-4

Keywords: Harnessing, semiochemicals, parasitoid-based, biological, control, laboratory, identification, field, applications, scientific research