Antennal sensilla of whiteflies: Trialeurodes vaporariorum (Westwood), the glasshouse whitefly,Aleyrodes proletella (Linnaeus), the cabbage whitefly,and Bemisia tabaci (Gennadius), the tobacco whitefly (Homoptera : Aleyrodidae). Part 1: External morphology

Scanning electron microscopy has revealed the detailed structure of the antennae of three species of whitefly, Trialeurodes vaporariorum, Aleyrodes proletella, and Bemisia tabaci (Homoptera : Aleyrodidae). All 3 species have microtrichia and 5 types of sensilla on the antennae: chaetica, campaniform, basiconic, coeloconic, and pegs with digitate tips, the latter 3 of these being unique to the flagellum. The number and distribution of the sensilla unique to the flagellum vary among the species studied. The cuticle of the basiconic and the coeloconic sensilla is pitted and grooved, respectively, a prerequisite for an olfactory and/or a thermo-, hygroreceptive function. A sexual dimorphism does occur with respect to the position of the basiconic sensilla on flagella segment 5 of A. proletella, but not T. vaporariorum or B. tabaci.     

Morphological and ultrastructural characterization of olfactory sensilla in Drosophila suzukii: Scanning and transmission electron microscopy

Drosophila suzukii is a serious horticultural and quarantine pest, damaging various berry crops. Although the active use of olfactory communication in D. suzukii is well-known, their olfactory sensory system has not been comprehensively reported. Therefore, the present study was carried out to understand the morphology, distribution and ultrastructure of olfactory sensilla present in the antennae and maxillary palps of D. suzukii, through scanning electron microscopy (SEM) and transmission electron microscopy (TEM). The olfactory sensilla on the antennae of D. suzukii in both sexes could be classified into three major morphological types, basiconic, trichoid and coeloconic sensilla, according to their shapes. The antennal basiconic sensilla were further divided into three subtypes and the antennal trichoid sensilla into two subtypes, respectively, according to the size of individual sensillum. In contrast to the antennal olfactory sensilla showing diverse morphology, basiconic sensilla was the only type of olfactory sensilla in the maxillary palps of D. suzukii. The basiconic sensilla in the maxillary palps could be further classified into three subtypes, based on their size. Our SEM and TEM observations indicated that multiple nanoscale pores are present on the surface of all types of olfactory sensilla in the antennae and maxillary palps, except coeloconic sensilla. The difference in the morphological types and the distribution of olfactory sensilla suggests that their olfactory functions are different between antennae and maxillary palps in D. suzukii. The results of this study provide useful information for further studies to determine the function of olfactory sensilla in D. suzukii and to understand their chemical communication system.     

Comparison of the antennal sensilla of females of four fig-wasps associated with Ficus auriculata

A comparison was performed of the antennal sensilla of females of four chalcid wasp species Ceratosolen emarginatus Mayr, 1906, Sycophaga sp., Philotrypesis longicaudata Mayr, 1906, and Sycoscapter roxburghi Joseph, 1957, which are specific and obligatory associated with Ficus auriculata (Lour, 1790). The four species exhibit different oviposition strategies in the fig ovules where their offspring hatch and develop. Antennal sensilla morphology was evaluated using scanning electron microscopy. Females of the four species present 11 morphologically similar types of sensilla: trichoid sensilla, sensilla obscura, chaetica sensilla 1 and 2, which all have mechanosensory functions; uniporous basiconic sensilla, which are presumably contact chemosensilla; basiconic capitate peg sensilla, coeloconic sensilla 1, multiporous basiconic and placoid sensilla, which may be regarded as olfactory sensilla, and coeloconic sensilla 2 and 3, which are presumed to be proprioreceptors or pressure receptors. The four species have significant differences in the abundance and arrangement of trichoid sensilla and chaetica sensilla 1 on the flagellum. The coeloconic sensilla and sensilla obscura only occur on the antennae of C. emarginatus that enter figs. The chemosensilla which are presumably involved in host discrimination, i.e., basiconic sensilla, multiporous placoid sensilla and basiconic capitate peg sensilla, are similar in shape and configuration, although they present some differences in abundance. These findings provide practical information on the adaptations of fig wasps and the relationship between multisensory antennae and functions in fig wasp behaviour.     

Analysis of immunocytochemical staining patterns in the antennal system of Drosophila melanogaster

By immunizing mice with homogenized brains, heads, or a mixture of heads and antennae of D. melanogaster, we obtained six monoclonal antibodies (mabs) that bind to the olfactory system of Drosophila with various degrees of specificity. They can be divided into three groups with respect to their staining pattern: (1) The antibodies ca51/2, na21/2, and nb230 label both in the third (olfactory) antennal segment and in the visual ganglia. All of them bind to antennal structures that can be correlated with basiconic sensilla. The antibody ca51/2 labels sensory neurons of these sensilla. In the antenna of the lozenge ³ mutant, which lacks basiconic sensilla, no labeling is present. In Western blots ca51/2 recognizes in the antenna an antigen of 43.5 kDa, which is expressed in the antenna only in the presence of basiconic sensilla. The antibody na21/2 binds to basiconic and coeloconic sensilla, most likely to the apical part of sheath cells. In immunoblots it recognizes in the antenna two antigens of 42.2 kDa and 46.7 kDa. The latter appears to be correlated in the antenna with the presence of basiconic sensilla. (2) The staining pattern of antibody nc10 is associated with the sheath cells of basiconic and coeloconic sensilla. Moreover, nc10 binds to a subset of glomeruli in the antennal lobe. (3) The staining pattern of the antibodies VG2 and I24B5 is restricted to the antenna. I24B5 recognizes coeloconic sensilla and VG2 recognizes both coeloconic and basiconic sensilla. Staining patterns in both cases include sheath cells.     

Morphological and functional heterogeneity in olfactory perception between antennae and maxillary palps in the pumpkin fruit fly,Bactrocera depressa

The morphology and ultrastructure of the olfactory sensilla on the antennae and maxillary palps were investigated through scanning electron microscopy (SEM) and transmission electron microscopy (TEM), and their responses to five volatile compounds were measured using electroantenogram (EAG) and electropalpogram (EPG) techniques in the pumpkin fruit fly, Bactrocera depressa (Shiraki; Diptera: Tephritidae). Male and female B. depressa displayed distinct morphological types of olfactory sensilla in the antennae and maxillary palps, with predominant populations of trichoid, basiconic, and coeloconic sensilla. Basiconic sensilla, the most abundant type of olfactory sensilla in the antennae, could be further classified into two different types. In contrast, the maxillary palps exhibited predominant populations of a single type of curved basiconic sensilla. High‐resolution SEM observation revealed the presence of multiple nanoscale wall‐pores on the cuticular surface of trichoid and basiconic sensilla, indicating that their primary function is olfactory. In contrast, coeloconic sensilla displayed several longitudinal grooves around the sensillum peg. The TEM observation of individual antennal olfactory sensilla indicates that the basiconic sensilla are thin‐walled, while the trichoid sensilla are thick‐walled. The profile of EAG responses of male B. depressa was different from their EPG response profile, indicating that the olfactory function of maxillary palps is different from that of antennae in this species. The structural and functional variation in the olfactory sensilla between antennae and maxillary palps suggests that each plays an independent role in the perception of olfactory signals in B. depressa.     

External morphology of antennal sensilla of trichogramma australicum girault (Hymenoptera : Trichogrammatidae)

External morphology of antennal sensilla on female and male Trichogramma australicum (Hymenoptera : Trichogrammatidae) was examined using scanning electron microscopy. Antennae show strong sexual dimorphism in structure and types of sensilla. The female antenna displays 14 types of sensilla: basiconic capitate peg sensilla (types 1 and 2), campaniform sensilla, chaetica sensilla (types 1–3), coeloconic sensilla, falcate sensilla, placoid sensilla (types 1 and 2), styloconic sensilla and trichoid sensilla (types 1–3). The male antenna displays 12 types of sensilla: basiconic capitate peg sensilla (type 2), campaniform sensilla, chaetica sensilla (types 1–5), coeloconic sensilla, placoid sensilla (type 1), and trichoid sensilla (types 3–5). Falcate and styloconic sensilla occur only on the female antenna. Both sensilla probably are associated with host examination, host discrimination and oviposition behaviour. Male antennal trichoid sensilla types 4 and 5 are probably associated with courtship behaviour, because these types occur only on the male. We propose the term “falcate sensilla” for a unique female antennal sensilla; the number of falcate sensilla may be used for identification of Trichogramma spp. In addition, we report the presence of placoid sensilla type 2 and difference in structure of coeloconic sensilla in T. australicum. Variation in structure and position of antennal sensilla are discussed.     

Analysis of immunocytochemical staining patterns in the antennal system of Drosophila melanogaster

By immunizing mice with homogenized brains, heads, or a mixture of heads and antennae of D. melanogaster, we obtained six monoclonal antibodies (mabs) that bind to the olfactory system of Drosophila with various degrees of specificity. They can be divided into three groups with respect to their staining pattern: (1) The antibodies ca51/2, na21/2, and nb230 label both in the third (olfactory) antennal segment and in the visual ganglia. All of them bind to antennal structures that can be correlated with basiconic sensilla. The antibody ca51/2 labels sensory neurons of these sensilla. In the antenna of the lozenge ³ mutant, which lacks basiconic sensilla, no labeling is present. In Western blots ca51/2 recognizes in the antenna an antigen of 43.5 kDa, which is expressed in the antenna only in the presence of basiconic sensilla. The antibody na21/2 binds to basiconic and coeloconic sensilla, most likely to the apical part of sheath cells. In immunoblots it recognizes in the antenna two antigens of 42.2 kDa and 46.7 kDa. The latter appears to be correlated in the antenna with the presence of basiconic sensilla. (2) The staining pattern of antibody nc10 is associated with the sheath cells of basiconic and coeloconic sensilla. Moreover, nc10 binds to a subset of glomeruli in the antennal lobe. (3) The staining pattern of the antibodies VG2 and I24B5 is restricted to the antenna. I24B5 recognizes coeloconic sensilla and VG2 recognizes both coeloconic and basiconic sensilla. Staining patterns in both cases include sheath cells.     

Flagellar sensilla of the eusocial gall-inducing thrips Kladothrips intermedius and its kleptoparasite, Koptothrips dyskritus (Thysanoptera: Phlaeothripinae)

Insect antennal flagella host a multitude of sensory organs fulfilling different functions. Chemoreception, for example, is essential for insects in many contexts. Both olfaction and contact chemoreception are involved in host-plant selection, as well as in the integrity of insect societies, especially for nestmate recognition. Kladothrips intermedius is a eusocial gall-inducing thrips with two castes: dispersers and soldiers. Koptothrips dyskritus is a specialist in invading Kl. intermedius galls, killing the occupants, and thereby gaining the food and shelter offered by galls. In this study, we compared the morphology and ultrastructure of the flagellar sensilla of Kl. intermedius and Ko. dyskritus via scanning and transmission electron microscopy in order to facilitate future investigations of their sensory ecology, with an emphasis on chemical ecology. The two species show a very similar sensillar array. There are a few mechanosensory trichoid and a second type of mechanosensory sensilla, thermo-hygroreceptive sensilla, olfactory single-walled basiconic and double-walled coeloconic sensilla as well as contact chemoreceptive chaetic sensilla. The latter are sexually dimorphic in Kl. intermedius. Dispersers and soldiers of Kl. intermedius do not present noteworthy morphological differences, but the ultrastructural investigations revealed that soldiers have fewer ORNs, possibly an adaptation to their gall-cloistered lifestyle.     

Ultrastructure of antennal sense organs of small ermine moths,Yponomeuta spp. (Lepidoptera : Yponomeutidae)

The ultrastructure of antennal sensilla was investigated in males and females of 5 European Yponomeuta species. Three types of olfactory sensilla could be distinguished, i.e. sensilla trichodea, sensilla basiconica, and sensilla coeloconica. Sexual dimorphism in the number of cells innervating sensilla trichodea could be established in 3 species. Most of these sensilla in males of Y. vigintipunctatus, Y. rorellus, and Y. cagnagellus are associated with 3 sensory cells, whereas in females of these species these sensilla contain 2 sensory cells. In both males and females of Y. padeltus and Y. malinellus, the great majority of the sensilla trichodea is innervated by 3 cells. So-called sensilla chaetica type 1 show features typical of a combined mechano/contact-chemoreceptor. No structures indicating a sensory function were found in sensilla chaetica type 11. Sensilla styloconica contain 3 cells, the dendritic outer segment of one being lamellated; most likely, these cells have a thermo- and hygroreceptive function. The findings concerning the olfactory sensilla are discussed in the context of olfactory communication and reproductive isolation in European Yponomeuta.     

Fine structure of the antennal sensilla of the millipede Orthomorphella pekuensis (Polydesmida: Paradoxosomatidae)

The fine structural characteristics of various sensory receptors on the antenna of a millipede, Orthomorphella pekuensis, were observed with field emission scanning electron microscopy. The antenna of this millipede has eight segments, called articles. On the surface of the antenna, there are a variety of sensory receptors, including olfactory and mechanical receptors. According to their morphological and fine structural characteristics, we could identify four basic types of antennal sensillum: chaetiform sensilla (CS), trichoid sensilla (TS), basiconic sensilla (BS) and apical cone sensilla (AS). The BS are divided further into three subtypes: large basiconic sensilla (BS₁) on the 5th and 6th articles; small basiconic sensilla (BS₂) on the 5th article; and a distinct type of basiconic spiniform sensilla (BS₃) on the 7th article. The most prominent sensilla are four large AS on the distal tip of the 8th segment. Based on our results, we conclude that the main function of the CS and TS are related to mechanical reception, and that the BS and AS are likely to function in olfactory reception of volatile odors of plants, as these sensilla have base and apex pores, respectively.     

Morphology and ultrastructure of the chemosensory sensilla of larval antennae in the Colorado potato beetle, Leptinotarsa decemlineata Say (Coleoptera: Chrysomelidae)

The allocation, external morphology, and ultrastructure of various types of sensilla on the antennae have been studied in the larvae of the Colorado potato beetle (Leptinotarsa decemlineata Say) using scanning and transmission electron microscopy. It has been found that the larval antenna bears 11 sensilla of four morphological types: trichoid (five), basiconic (four), styloconic (one), and antennal cone (one). It has been shown that the sensilla are innervated by 2?C7 receptor cells: trichoid, by 2?C4 receptor cells; basiconic, by 4?C7 receptor cells; and styloconic, by 6 receptor cells. Judging by the specifics of their ultrastructural organization, the function of these sensilla is gustatory. The antennal cone is innervated by two receptor cells, and its function is olfactory.     

The organization of the chemosensory system in Drosophila melanogaster: a rewiew

This review surveys the organization of the olfactory and gustatory systems in the imago and in the larva of Drosophila melanogaster, both at the sensory and the central level. Olfactory epithelia of the adult are located primarily on the third antennal segment (funiculus) and on the maxillary palps. About 200 basiconic (BS), 150 trichoid (TS) and 60 coeloconic sensilla (CS) cover the surface of the funiculus, and an additional 60 BS are located on the maxillary palps. Males possess about 30% more TS but 20% fewer BS than females. All these sensilla are multineuronal; they may be purely olfactory or multimodal with an olfactory component. Antennal and maxillary afferents converge onto approximately 35 glomeruli within the antennal lobe. These projections obey precise rules: individual fibers are glomerulus-specific, and different types of sensilla are associated with particular subsets of glomeruli. Possible functions of antennal glomeruli are discussed. In contrast to olfactory sensilla, gustatory sensilla of the imago are located at many sites, including the labellum, the pharynx, the legs, the wing margin and the female genitalia. Each of these sensory sites has its own central target. Taste sensilla are usually composed of one mechano-and three chemosensory neurons. Individual chemosensory neurons within a sensillum respond to distinct subsets of molecules and project into different central target regions. The chemosensory system of the larva is much simpler and consists essentially of three major sensillar complexes on the cephalic lobe, the dorsal, terminal and ventral organs, and a series of pharyngeal sensilla.     

Sex-specific antennal sensory system in the ant <Emphasis Type="Italic">Camponotus japonicus</Emphasis>: structure and distribution of sensilla on the flagellum

The antennae are a critically important component of the ant’s highly elaborated chemical communication systems. However, our understanding of the organization of the sensory systems on the antennae of ants, from peripheral receptors to central and output systems, is poorly understood. Consequently, we have used scanning electron and confocal laser microscopy to create virtually complete maps of the structure, numbers of sensory neurons, and distribution patterns of all types of external sensilla on the antennal flagellum of all types of colony members of the carpenter ant Camponotus japonicus. Based on the outer cuticular structures, the sensilla have been classified into seven types: coelocapitular, coeloconic, ampullaceal, basiconic, trichoid-I, trichoid-II, and chaetic sensilla. Retrograde staining of antennal nerves has enabled us to count the number of sensory neurons housed in the different types of sensilla: three in a coelocapitular sensillum, three in a coeloconic sensillum, one in an ampullaceal sensillum, over 130 in a basiconic sensillum, 50–60 in a trichoid-I sensillum, and 8–9 in a trichoid-II sensillum. The basiconic sensilla, which are cuticular hydrocarbon-receptive in the ant, are present in workers and unmated queens but absent in males. Coelocapitular sensilla (putatively hygro- and thermoreceptive) have been newly identified in this study. Coelocapitular, coeloconic, and ampullaceal sensilla form clusters and show biased distributions on flagellar segments of antennae in all colony members. The total numbers of sensilla per flagellum are about 9000 in unmated queens, 7500 in workers, and 6000 in males. This is the first report presenting comprehensive sensillar maps of antennae in ants.     

The chemosensory system of the monophagus grasshopper,Bootettix argentatus bruner (Orthoptera : Acrididae)

Bootettix argentatus (Orthoptera : Acrididae) is a monophagous grasshopper in the subfamily Gomphocerinae. The numbers of chemoreceptors in most groups on the mouthparts increase with each molt and are generally similar in the 2 sexes. There are fewer sensilla in the A3 groups than in other gomphocerine grasshoppers, and the possibility that this is related to host-plant specificity is discussed. Only very small numbers of sensilla are present on the pulvillar pads of the tarsi and on the arolia. The number of sensilla on the antennae is proportional to the length of the flagellum and coeloconic sensilla comprise 30–35%. Most of the remainder are multiporous basiconic sensilla. Adult males have more antennal sensilla than adult females.     

Antennal sensilla and sexual dimorphism of the adult ladybird beetle Semiadalia undecimnotata Schn. (Coleoptera: Coccinellidae)

The antennal receptors of the adult male and female ladybird beetle, Semiadalia undecimnotata (Coleoptera: Coccinellidae), were examined by scanning and transmission electron microscopy. Twelve types of receptors were characterized and grouped into 5 morphological classes: Böhm, trichoid, coeloconic, basiconic, and chetiform sensilla. Sensory function was determined on the basis of sensillar ultrastructure and electrophysiological response. Olfactory sensilla are confined in both sexes to the 2 terminal antennal segments. In contrast, gustatory and mechanosensitive organs are present along the entire length of the antennae. Sexual dimorphism of antennal receptors is limited to the latter 2 functional classes. The principal characteristics of this dimorphism are the following: a) males possess 540 sensilla (all types), while females possess only 500; b) males exhibit 2 types of taste receptors not present in females; c) females exhibit one type of mechanoreceptor absent in males; d) the 3 sex-specific types of sensilla, which occupy the same position in males and females, are confined to the inner side of the antennae. The possible role of male-specific sensilla in intersexual communication is discussed.     

Characterization of olfactory sensilla of Stomoxys calcitrans and electrophysiological responses to odorant compounds associated with hosts and oviposition media

Stable flies, Stomoxys calcitrans L. (Diptera: Muscidae), are economically important biting flies that have caused billions of dollars in losses in the livestock industry. Field monitoring studies have indicated that olfaction plays an important role in host location. To further our understanding of stable fly olfaction, we examined the antennal morphology of adults using scanning electron microscopy techniques. Four major types of sensillum were found and classified as: (a) basiconic sensilla; (b) trichoid sensilla with three subtypes; (c) clavate sensilla, and (d) coeloconic sensilla. No significant differences between male and female flies in abundances (total numbers) of these sensillum types were observed, except for medium-sized trichoid sensilla. The distinctive pore structures found on the surface of basiconic and clavate sensilla suggest their olfactory functions. No wall pores were found in trichoid and coeloconic sensilla, which suggests that these two types of sensillum may function as mechano-receptors. Details of the distributions of different sensillum types located on the funicle of the fly antenna were also recorded. Electroantennogram results indicated significant antennal responses to host-associated compounds. The importance of stable fly olfaction relative to host and host environment seeking is discussed. This research provides valuable new information that will enhance future developments in integrated stable fly management.     

Morphology and distribution of antennal sensilla in the pine wood nematode insect vectors Monochamus alternatus Hope and Monochamus saltuarius Gebler (Coleoptera: Cerambycidae)

As insect vectors of pine wood nematodes, Monochamus alternatus Hope and Monochamus saltuarius Gebler have different levels of attractiveness to semiochemicals. Although active use of chemical communication in both species is well known, there was no report on the differences in morphology and distribution of antennal sensilla between the two Monochamus species. The present study was carried out to explore the morphology, distribution, and ultrastructure of antennal sensilla of the two species using scanning and transmission electron microscopy. The overall shapes of the antennae were not different between M. alternatus and M. saltuarius. However, both M. alternatus and M. saltuarius exhibited sexual dimorphism overall. The antennae of each species were composed of the scape, pedicel, and nine flagellomeres, with four morphological types of sensilla: trichodea, basiconica, chaetica, and coeloconica. The four types occurred in varying numbers and distributions. The sensilla chaetica type was the most abundant in both species. Three types of sensilla (trichodea, basiconica, and chaetica) could be subdivided according to the two Monochamus species; sensilla trichodea could be divided into two subtypes, and sensilla basiconica and sensilla chaetica into three. All sensilla basiconica subtypes were multiporous, indicating that their primary function was olfactory. Sensilla trichodea subtype 2 was uniporous, indicating that the function of these sensilla might be gustatory. The morphological information obtained in our study provides a basis for future investigation of the sensory physiological function of each type of sensilla in the two species.     

A comparative ultrastructural and behavioral study of the antennal sensory sensilla of the parasitoid Cardiochiles nigriceps (hymenoptera:Braconidae)

Scanning and transmission electron microscopy studies were conducted on the antennal sensory sensilla of the hymenopteran parasitoid, Cardiochiles nigriceps Viereck, of the family Braconidae. Distinct morphological differences were found between the chemoreceptors of the male and female. Curved, non-fluted, thin-walled sensilla were found to be very abundant on the male and restricted in location and number on the female. Trichoid, placoid and fluted basiconic sensilla were numerous on the antennal flagella of both sexes. Smooth basiconic sensilla were restricted in number to one per flagellar segment in both sexes. Behavioral data suggest that bent-tipped, thick-walled sensilla unique to the female are involved in detecting a chemical(s) emitted from the host, Heliothis virescens (Fab.).     

Antennal sensilla of the click beetle,Melanotus villosus (Geoffroy) (Coleoptera: Elateridae)

The typology, number and placement of antennal sensilla of the click beetle Melanotus villosus (Geoffroy) (Coleoptera: Elateridae) were studied using scanning electron microscopy. On both the males and females the antennae are made up of the scape, pedicel and nine flagellomeres. Two types of basiconic sensilla, three types of trichoid sensilla, one type of styloconic sensilla, one type of chetoid sensilla, dome-shaped sensilla, grooved pegs, and Böhm sensilla all appear on the antennae of the beetles of both sexes, with the exception of trichoid sensilla type II, whose large number (average of 1635 hairs per antenna) was found only in male beetles. Sensilla trichodea type II evidently respond to the sex pheromone produced by the female beetle. Unlike the other two click beetles, studied up till now, Agriotes obscurus and Limonius aeruginosus, the trichoid and basiconic sensilla of M. villosus, whose proven or assumed function is olfactory, are located predominantly on the flagellomeres ventral extensions. It is assumed that the placement of the olfactory sensilla, mainly on the ventral side of M. villosuss antennae, and their more or less even distribution on the flagellomeres, can be seen as morphological adaptation of this species of insect, whose specific behavioural reaction of olfactory searching is flying, both before and after contact with an odour plume.