Insect Sensilla Research Articles

Three-dimensional reconstruction of insect chemosensory sensillum

The olfactory system is involved in food and mate recognition in insects. However, 3D structures of chemosensory sensilla in insects are unexplored yet. Here, the internal structures of an olfactory sensillum on the antenna of the brown planthopper, Nilaparvata lugens (Hemiptera: Delphacidae), one of the most important rice pests, are examined and imaged using focused ion beam scanning electron microscopy. Based on these images, a 3D structure is reconstructed in this study. We find that the trichoid olfactory sensillum possesses a multiporous wall encircling a lumen with one sensory cell. Besides, there are three accessory cells (ACs) and a glia cell with different cell contents surrounding the sensory cell. The abundant tubular membrane structures in the tormogen cell suggest its role in secreting proteins like odorant binding proteins into the receptor lymph, while three auxiliary cells with simpler cellular content closely enfold the sensory cell, probably to prevent leaking of the receptor lymph into the surrounding epidermis. In the sensory cell, the microtubules and two tandem basal bodies at the base of the microtubules are also reconstructed. They are considered as a propulsive engine to ensure dendrite vibration or spinning in the receptor lymph, so that the proteins and odorant molecules move faster in the receptor lymph, which improves recognition of environmental odors and enables the insect to immediately respond to this information.

Specialized structure and function of the apical extracellular matrix at sense organs

Apical extracellular matrix (aECM) covers every surface of the body and exhibits tissue-specific structures that carry out specialized functions. This is particularly striking at sense organs, where aECM forms the interface between sensory neurons and the environment, and thus plays critical roles in how sensory stimuli are received. Here, we review the extraordinary adaptations of aECM across sense organs and discuss how differences in protein composition and matrix structure assist in sensing mechanical forces (tactile hairs, campaniform sensilla, and the tectorial membrane of the cochlea); tastes and smells (uniporous gustatory sensilla and multiporous olfactory sensilla in insects, and salivary and olfactory mucus in vertebrates); and light (cuticle-derived lenses in arthropods and mollusks). We summarize the power of using C. elegans, in which defined sense organs associate with distinct aECM, as a model for understanding the tissue-specific structural and functional specializations of aECM. Finally, we synthesize results from recent studies in C. elegans and Drosophila into a conceptual framework for aECM patterning, including mechanisms that involve transient cellular or matrix scaffolds, mechanical pulling or pushing forces, and localized secretion or endocytosis.

Morphology and location of sensilla in the antennae and ovipositor of Sirex noctilio (Hymenoptera: Siricidae)

The woodwasp Sirex noctilio Fabricius is a major quarantine pest that was reported in China in 2013 and mostly damages Pinus sylvestris var. mongolica. Reverse chemical ecology, which uses chemical lures to catch or block insects from mating is the classic way to control forestry pests. This indicates that insect sensilla play a crucial role in detecting external chemical and physical stimuli. Nonetheless, the categorization and distribution of sensilla on the antennae and ovipositor of S. noctilio are insufficiently specific. In this paper, scanning electron microscopy (SEM) was used to observe the ultrastructure of the sensilla of S. noctilio on the antenna and ovipositor. It was found that the types and distribution of sensilla on the antennae of S. noctilio male and female are consistent, and six types of sensilla are found: sensilla trichodea (ST), sensilla chaetica (SC), Böhm bristles (BB), sensilla basiconica (SB), sensilla ampullacea (SA), and contact chemoreceptors (CC). Besides, there are five types of sensilla on the female ovipositor. In addition to ST, SC and BB, two more types of sensilla are also found: sensilla cavity (SCa) and sensilla coeloconica (SCo). Through identification of the morphology and distribution of the sensilla, the functions of different sensilla in the mating and host selection mechanisms of S. noctilio are proposed, thereby establishing a foundation for S. noctilio chemical communication research.

Functional analysis of a bitter gustatory receptor highly expressed in the larval maxillary galea of Helicoverpa armigera.

Many plant secondary substances are feeding deterrents for insects and play a key role in the selection of host plants. The taste sensilla of phytophagous insects contain gustatory sensory neurons sensitive to deterrents but the molecular basis of deterrent chemoreception remains unknown. We investigated the function of Gr180, the most highly expressed bitter gustatory receptor in the maxillary galea of Helicoverpa armigera larvae. Functional analyses using the Xenopus oocyte expression system and two-electrode voltage clamp revealed that the oocytes expressing Gr180 responded to coumarin. Tip recording results showed that the medial sensilla styloconica of the maxilla of fifth instar larvae exhibited electrophysiological responses to coumarin. Two-choice feeding bioassays confirmed that coumarin inhibited larval feeding. A homozygous mutant strain of H. armigera with truncated Gr180 proteins (Gr180−/−) was established using the CRISPR-Cas9 system. The responses of the medial sensilla styloconica in Gr180−/− to coumarin were almost abolished, and the responses to sinigrin and strychnine were also significantly decreased. Knockout of Gr180 alleviated the feeding deterrent effects of coumarin, sinigrin, and strychnine. Thus, we conclude that Gr180 is a receptor responding to coumarin,and also participates in sensing sinigrin and strychnine. These results enhance our understanding of the gustatory sensing mechanisms of phytophagous insects to deterrents.

Ultrastructure of sensilla on the antennae and maxillary palpi of the human-biting black flies, Simulium nigrogilvum and Simulium umphangense, (Diptera: Simuliidae) in Thailand

Antennae and maxillary palpi are the most important sensory organs involved in the behaviors of black flies. The ultrastructure of sensilla on these sensory appendages of two human-biting black fly species, Similium nigrogilvum and Simulium umphangense, was studied for the first time. Wild adult females of both species were collected in Umphang District, Tak Province, western Thailand. The morphology and distribution of sensilla were examined using scanning electron microscopy. Overall, the morphology of the antennae and maxillary palpi and distribution of sensilla are similar in the two species. Four major types of sensilla were found on the antennae of both species: sensilla basiconica (three subtypes), coeloconica, chaetica (four subtypes), and trichodea. However, sensilla basiconica subtype IV are only present on the antennal surface of S. nigrogilvum. Sensilla trichodea are the most abundant among the four types of sensilla that occur on the antennae of both species. Significant differences in the length of the antennae (scape and flagellomere IX), length of the maxillary palpi (whole and palpal segments I, III, IV and V), and the length and basal width of four sensilla types (trichodea, chaetica, basiconica, and coeloconica) were found. In addition, two types of sensilla were observed on the maxillary palpi: sensilla chaetica (three subtypes) and bulb-shaped sensilla. Differences were observed in the numbers of bulb-shaped sensilla in the sensory vesicles of S. nigrogilvum and S. umphangense. The findings are compared with the sensilla of other insects, and the probable functions of each sensillum type are discussed. The anatomical data on sensory organs derived from this study will help to better understand black fly behavior.

Sensilla of the Western Flower Thrips, Frankliniella occidentalis (Pergande) (Thysanoptera, Thripidae)

The sensilla of insects play important roles in odor, taste, the feeling environment, and some sensory functions, which are closely associated with insect host locating, feeding, habitat searching, courtship, mating, and oviposition. In this study, we used a scanning electron microscope to observe the external morphology of nymph and adult Frankliniella occidentalis sensilla on antennae, compound eyes, legs, mouthparts, wings and tail. The results show that three main types of sensilla are located on the antennae: sensilla trichodea, sensilla chaetica, and sensilla basiconica. Among them, sensilla trichodea are the most abundant, followed by sensilla chaetica. Sensilla basiconica on antennae are divided into seven sub-styles, including longer sensilla (L-sensilla basiconica, long sensilla basiconica), shorter sensilla (angle sensilla basiconica, bud sensilla basiconica), and thicker and bigger sensilla (stick sensilla basiconica, fork sensilla basiconica, and finger sensilla basiconica). Only two fork sensilla basiconica were found, located on the dorsal part of the first flagellum subsegment and the ventral part of the second flagellum subsegment, respectively. Seven sensillum types were found on the legs: sensilla trichodea, sensilla chaetica, sensilla basiconica, sensilla ear washing buob-shaped, mamillary sensilla, sensilla campaniform, and Böhm bristle. About 60% of them are sensilla chaetica. Only one sensillum type was found on compound eyes: sensilla chaetica. In addition, some sensillum types were also found on the mouthparts, wings and tail, respectively. In the study, we observed the type, morphology, and distribution of sensilla on antennae, legs, compound eyes, and other regions of nymph and adult F. occidentalis, forming a base for future electrophysiological and behavior experiments on F. occidentalis.

Scanning Electron Microscope Study of Antennae and Mouthparts in the Pollen-Beetle Meligethes (Odonthogethes) chinensis (Coleoptera: Nitidulidae: Meligethinae).

Simple SummaryThe present paper is aimed to further explore the structure of the antennae and mouthparts of specialized beetle species living on flowers, as well as the functions of their associated sensilla. In this study, we used scanning electron microscopy (SEM) to observe and describe for the first time the fine morphology of sensilla on the antennae and mouthparts of the pollen-beetle Meligethes (Odonthogethes) chinensis, a common Chinese species associated with flowers of Rosaceae. The results show that there are six types and twelve subtypes of sensilla on male antennae; seven types and fourteen subtypes on female antennae; seven types and seventeen subtypes on male mouthparts; seven types and sixteen subtypes on female mouthparts. The sensilla on the antennae and mouthparts of Meligethinae that feed on pollen were finally compared with similar sensilla known to occur in other insects, in order to obtain more insights on the evolution of these sensorial structures in specialized flower-inhabiting insects.Meligethes (Odonthogethes) chinensis is a common Chinese phytophagous species in the family Nitidulidae. Its main larval host plant is Rubus idaeus L. (Rosaceae), and adults feed on pollen and other floral parts. In this study, we used scanning electron microscopy (SEM) to observe and study the fine morphology of sensilla on the antennae and mouthparts of M. chinensis. The results show that there are six types and twelve subtypes of sensilla on male antennae; seven types and fourteen subtypes on female antennae; seven types and seventeen subtypes on male mouthparts; seven types and sixteen subtypes on female mouthparts. Sensilla coeloconica (SCo) are found on the female antennae of M. chinensis only, and they are also reported on the antennae of Nitidulidae for the first time. SCo2 on the labrum present sexual dimorphism, and one subtype of sensilla basiconica (SB6) is presented on the tip of maxillary and labial palps of the male only, while other types of sensilla are very similar on the mouthparts of male and female. Finally, by comparing similar sensilla in other insects, we also attempted to discuss the functions of all sensilla on the antennae and mouthparts of M. chinensis.

Sample Preparation Method of Scanning and Transmission Electron Microscope for the Appendages of Woodboring Beetle.

This report described sample preparation methods that scanning and transmission electron microscope observations, demonstrated by preparing appendages of the woodboring beetle, Chlorophorus caragana Xie & Wang (2012), for both types of electron microscopy. The scanning electron microscopy (SEM) sample preparation protocol was based on sample chemical fixation, dehydration in a series of ethanol baths, drying, and sputter-coating. By adding Tween 20 (Polyoxyethylene sorbitan laurate) to the fixative and the wash solution, the insect body surface of woodboring beetle was washed more cleanly in SEM. This study's transmission electron microscopy (TEM) sample preparation involved a series of steps including fixation, ethanol dehydration, embedding in resin, positioning using fluorescence microscopy, sectioning, and staining. Fixative with Tween 20 enabled penetrate the insect body wall of woodboring beetle more easily than it would had been without Tween 20, and subsequently better fixed tissues and organs in the body, thus yielded clear transmission electron microscope observations of insect sensilla ultrastructures. The next step of this preparation was determining the positions of insect sensilla in the sample embedded in the resin block by using fluorescence microscopy to increase the precision of target sensilla positioning. This improved slicing accuracy.

Antennal morphology and localization of a general odorant-binding protein in the great wax moth, Galleria mellonella (Lepidoptera: Pyralidae)

The great wax moth, Galleria mellonella (L.), is a globally distributed pest for bee hives and, therefore, of significant importance for apiculture. In this study, the antennal morphology of G. mellonella was elucidated by light microscopy (LM) and scanning electron microscopy (SEM). Moreover, the putative function of the sensilla was studied by in situ hybridization of an odorant-binding protein (OBP)-encoding gene. Thus, an OBP subclass called general odorant-binding protein (GOBP) was used. Currently, GOBPs are related to the transport of sex pheromone and general volatiles in the sensilla of insects. Results indicate sexual dimorphism, with longer antennae for females than males. Sensilla morphology was similar to that reported in other moths, especially pyralids, with a total of seven types of sensilla, namely chaetica (SCH), trichodea (STR), coeloconica (SCO), styloconica (STY), auricilica (SAU), basiconica (SBA) and squamiformia (SSQ). Böhm’s bristles (BB) were also found. As expected due to the inverse sexual communication of G. mellonella, a higher abundance of pheromone-related STR subtype I, were determined in female compared to male antennae. More interestingly, we report the presence of a GOBP-encoding gene, found mainly in female STR and SCH. Therefore, the cross information between reported sensilla function and that of OBPs provides evidence to support not only the olfactory function of STR and SCH, but also the uncommon sexual communication that G. mellonella has developed.

Structure of Antennal Pseudoplacoid Sensilla in the Caddisfly Philopotamus montanus Donovan (Trichoptera, Philopotamidae)

The structure of pseudoplacoid sensilla characteristic of Amphiesmenoptera was studied by SEM and TEM methods by the example of the mushroom-like sensilla in Philopotamus montanus Don., a member of the primitive family Philopotamidae. These sensilla were found to be different from the externally similar placoid sensilla in the presence of a socket-like depression and a sensillar stem arising from it. The expanded terminal part filled with the dendrites of the sensory neurons has numerous pores on its upper and lower surfaces. The sensillar dendrites have subterminal expansions filled with electron-transparent fluid, while their thin terminal parts have electron-dense central elements. The pseudoplacoid sensillum of Ph. montanus comprises three sensory neurons. The mushroom-like pseudoplacoid sensilla of Ph. montanus are compared with chemoreceptive sensilla of other insects.

Effects of force detecting sense organs on muscle synergies are correlated with their response properties

Sense organs that monitor forces in legs can contribute to activation of muscles as synergist groups. Previous studies in cockroaches and stick insects showed that campaniform sensilla, receptors that encode forces via exoskeletal strains, enhance muscle synergies in substrate grip. However synergist activation was mediated by different groups of receptors in cockroaches (trochanteral sensilla) and stick insects (femoral sensilla). The factors underlying the differential effects are unclear as the responses of femoral campaniform sensilla have not previously been characterized. The present study characterized the structure and response properties (via extracellular recording) of the femoral sensilla in both insects. The cockroach trochantero-femoral (TrF) joint is mobile and the joint membrane acts as an elastic antagonist to the reductor muscle. Cockroach femoral campaniform sensilla show weak discharges to forces in the coxo-trochanteral (CTr) joint plane (in which forces are generated by coxal muscles) but instead encode forces directed posteriorly (TrF joint plane). In stick insects, the TrF joint is fused and femoral campaniform sensilla discharge both to forces directed posteriorly and forces in the CTr joint plane. These findings support the idea that receptors that enhance synergies encode forces in the plane of action of leg muscles used in support and propulsion.

Antennal Sensilla and Sexual Dimorphism of the Parasitoid Trichospilus pupivorus (Hymenoptera: Eulophidae)

Sensory structures (sensilla) of insects are present in high number in the antennae are important for perceiving environmental cues. Thus, sensilla play an important role in the localization, discrimination, and acceptance of a possible host by parasitoid insects. The sensilla, classified according to their shape, size, and distribution, may also show sexual dimorphism in insects. The types and distribution of antennal sensilla in female and male parasitoid Trichospilus pupivorus (Ferriere, 1930) (Hymenoptera: Eulophidae) were evaluated. T. pupivorus females had longer antennae than males. Both males and females have ten sensilla types with higher abundance of placoid sensilla in females, which suggest a possible functional dimorphism.

Retraction Note to: Involvement of a Specific Chemosensory Protein from Bactrocera dorsalis in Perceiving Host Plant Volatiles.

Insects have evolved many physiological and behavioral adaptations to recognize external complex chemicals. Olfaction plays an important role in perceiving volatile chemicals, utilizing them to locate host sites, conspecifics, and enemies. Chemosensory proteins (CSPs) are present in high concentrations within the sensory sensilla of insects and are endowed with a heterogeneous range of functions. However, direct evidence for the involvement of CSPs in olfactory function is still lacking. In this study, a fluorescence-based ligand binding assay using Bdor-CSP2 illustrated its ability to bind the majority of the selected ligands of different shapes and chemical structures that are ecologically significant, host plant volatiles of Bactrocera dorsalis. RNAi-mediated silencing coupled with electrophysiological tests showed lower electrophysiological responses to (3Z)-hex-3-en-1-ol, trans-2-hexenal, 6-methylhept-5-en-2-one, and 3-methylbutyl acetate in dsBdor CSP2 treated flies compared with the untreated controls. The reduced expression of Bdor-CSP2 by RNA interference was confirmed by semi-quantitative PCR, real-time quantitative PCR and Western blot, which suggested the RNAi-treatment was responsible for the observed reduction of antennal responses in EAG recordings. These data suggest that the expression of Bdor-CSP2 is necessary for the recognition of antennal responses to some plant host volatiles by B. dorsalis.

Novel synthetic compounds enhance the attractiveness of host-plant volatiles: An opportunity to boost detection and monitoring of Asian citrus psyllid?

Author(s): Patt, J.; Woods, D.; Dimitratos, S.; Meikle, W.; Stockton, D.; Lapointe, S.; Mafra-Neto, A. | Abstract: In the absence of pheromone attractants, host-plant volatiles offer the most likely means of improving capture levels of ACP with sticky cards and other types of visual traps. However, developing scent lures that can compete with the attractiveness of actual host-plants, especially those in flush, is challenging. We are developing a new class of synthetic scent lures that may enhance the attractiveness of naturally-occurring host-plant volatiles. These compounds are synthetic ligands that bind to chemosensory proteins (CSPs) found in the olfactory sensilla of target insects. These ligands may mimic naturally-occurring odorants and function as super-stimuli because of their strong affinity to CSPs. In our study, CSPs from ACP antennae were identified based on their reactivity to petitgrain oil (an essential oil extracted from sour orange leaves), an ACP attractant. Two behavioral assays were used to assess the biological activity of several candidate ligands. One assay measured ACP probing frequency into a line of emulsified wax (SPLAT®, ISCA Technologies) containing a test ligand, the other assay measured the retention time of psyllids in an airstream carrying the ligand. One ligand, nicknamed ‘Titan’, was more stimulatory than limonene, a common citrus volatile, while a mixture of Titan and limonene was significantly more stimulatory than either alone. Subsequent assays showed that Titan was as stimulatory to ACP as the odor emitted by flushing sprigs of orange jasmine, a favored host-plant. These results indicate that CSP ligands may synergize the attractiveness of naturally-occurring citrus volatiles and boost their effectiveness as scent lures for ACP.

Positive force feedback in development of substrate grip in the stick insect tarsus

The mechanics of substrate adhesion has recently been intensively studied in insects but less is known about the sensorimotor control of substrate engagement. We characterized the responses and motor effects of tarsal campaniform sensilla in stick insects to understand how sensory signals of force could contribute to substrate grip. The tarsi consist of a chain of segments linked by highly flexible articulations. Morphological studies showed that one to four campaniform sensilla are located on the distal end of each segment. Activities of the receptors were recorded neurographically and sensilla were identified by stimulation and ablation of their cuticular caps. Responses were characterized to bending forces and axial loads, muscle contractions and to forces applied to the retractor apodeme (tendon). The tarsal sensilla effectively encoded both the rate and amplitude of loads and muscle forces, but only when movement was resisted. Mechanical stimulation of the receptors produced activation of motor neurons in the retractor unguis and tibial flexor muscles. These findings indicate that campaniform sensilla can provide information about the effectiveness of the leg muscles in generating substrate adherence. They can also produce positive force feedback that could contribute to the development of substrate grip and stabilization of the tarsal chain.

The antennal sensilla of Melipona quadrifasciata (Hymenoptera: Apidae: Meliponini): a study of different sexes and castes

The sensilla of insects are integumental units that play a role as sensory structures and are crucial for the perception of stimuli and for communication. In this study, we compared the antennal sensilla of females (workers and queens), males (haploid (n) and diploid (2n)), and queen-like males (QLMs, resulting from 2n males after juvenile hormone (JH) treatment) in the stingless bee Melipona quadrifasciata. Images of the dorsal antenna surfaces were acquired using a scanning electron microscope. As reported for other hymenopterans, this species exhibits a heterogeneous sensillar distribution along the antennae. Thirteen different types of sensilla were found in the antennae of M. quadrifasciata: trichodea (subtypes I to VI), chaetica (subtypes I and II), placodea, basiconica, ampullacea, coeloconica, and coelocapitula. Sensilla trichodea I were the most abundant, followed by sensilla placodea, which might function in olfactory perception. Sensilla basiconica, sensilla chaetica I, sensilla coeloconica, and sensilla ampullacea were found exclusively in females. In terms of the composition and size of the sensilla, the antennae of QLMs most closely resemble those of the 2n male, although QLMs exhibit a queen phenotype. This study represents the first comparative analysis of the antennal sensilla of M. quadrifasciata. The differences found in the type and amount of sensilla between the castes and sexes are discussed based on the presumed sensillary functions.

RETRACTED ARTICLE: Involvement of a Specific Chemosensory Protein from Bactrocera dorsalis in Perceiving Host Plant Volatiles

Insects have evolved many physiological and behavioral adaptations to recognize external complex chemicals. Olfaction plays an important role in perceiving volatile chemicals, utilizing them to locate host sites, conspecifics, and enemies. Chemosensory proteins (CSPs) are present in high concentrations within the sensory sensilla of insects and are endowed with a heterogeneous range of functions. However, direct evidence for the involvement of CSPs in olfactory function is still lacking. In this study, a fluorescence-based ligand binding assay using Bdor-CSP2 illustrated its ability to bind the majority of the selected ligands of different shapes and chemical structures that are ecologically significant, host plant volatiles of Bactrocera dorsalis. RNAi-mediated silencing coupled with electrophysiological tests showed lower electrophysiological responses to (3Z)-hex-3-en-1-ol, trans-2-hexenal, 6-methylhept-5-en-2-one, and 3-methylbutyl acetate in dsBdor CSP2 treated flies compared with the untreated controls. The reduced expression of Bdor-CSP2 by RNA interference was confirmed by semi-quantitative PCR, real-time quantitative PCR and Western blot, which suggested the RNAi-treatment was responsible for the observed reduction of antennal responses in EAG recordings. These data suggest that the expression of Bdor-CSP2 is necessary for the recognition of antennal responses to some plant host volatiles by B. dorsalis.

On optimizing therapies, Orai, and ORNs

On optimizing therapies, Orai, and ORNs

Force encoding in stick insect legs delineates a reference frame for motor control

The regulation of forces is integral to motor control. However, it is unclear how information from sense organs that detect forces at individual muscles or joints is incorporated into a frame of reference for motor control. Campaniform sensilla are receptors that monitor forces by cuticular strains. We studied how loads and muscle forces are encoded by trochanteral campaniform sensilla in stick insects. Forces were applied to the middle leg to emulate loading and/or muscle contractions. Selective sensory ablations limited activities recorded in the main leg nerve to specific receptor groups. The trochanteral campaniform sensilla consist of four discrete groups. We found that the dorsal groups (Groups 3 and 4) encoded force increases and decreases in the plane of movement of the coxo-trochanteral joint. Group 3 receptors discharged to increases in dorsal loading and decreases in ventral load. Group 4 showed the reverse directional sensitivities. Vigorous, directional responses also occurred to contractions of the trochanteral depressor muscle and to forces applied at the muscle insertion. All sensory discharges encoded the amplitude and rate of loading or muscle force. Stimulation of the receptors produced reflex effects in the depressor motoneurons that could reverse in sign during active movements. These data, in conjunction with findings of previous studies, support a model in which the trochanteral receptors function as an array that can detect forces in all directions relative to the intrinsic plane of leg movement. The array could provide requisite information about forces and simplify the control and adaptation of posture and walking.

Antennal carboxylesterases in a moth, structural and functional diversity

Pheromone-degrading enzymes (PDEs) are supposed to be involved in the signal inactivation step within the olfactory sensilla of insects by quickly degrading pheromone molecules. Because esters are widespread insect pheromone components, PDEs belonging to the carboxylesterase (CCE) family have been the most studied. However, only two CCEs were both identified at the molecular level and functionally characterized as PDEs until recently. In the pest moth Spodoptera littoralis, we have identified an unsuspected diversity of antennal CCEs, with a total number of 30 genes. Two CCEs, enriched in antennae and belonging to distinct clades, were shown to present different substrate specificities toward pheromone and plant compounds. A same CCE was also shown to efficiently degrade both pheromone and plant components. Our results suggest that the structural evolution of antennal CCEs reflects their functional diversity and that a complex set of CCE-mediated reactions take place is the olfactory organs of moths.