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.     

山茱萸蛀果蛾幼虫触角和口器感器的超微形态

【目的】探索寄主范围不同的蛀果蛾科(Carposinidae)幼虫感器之间是否存在差异。【方法】采用扫描电子显微镜观察了为害山茱萸Cornus officinalis Sieb. et Zucc.的单食性蛀果害虫--山茱萸蛀果蛾Carposina coreana Kim老熟幼虫触角和口器感器的超微形态。【结果】山茱萸蛀果蛾幼虫触角柄节未见感器分布, 梗节上有2个刺形感器和3个锥形感器, 鞭节上有1个栓锥感器和3个锥形感器。口器上共有6种感器： 刺形感器数量多, 分布广; 栓锥感器主要分布在颚叶、 下颚须和下唇须上; 指形感器位于内唇和下颚须端节侧缘; 锥形感器和板形感器仅存在于下颚上; 内唇感器为内唇所特有。【结论】蛀果蛾幼虫触角和口器的感器与寄主范围之间未发现严格的对应关系。     

Morphology of antennal,maxillary palp and labial palp sensilla in different larval instars of the Asian long‐horned beetle,Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae)

The Asian long‐horned beetle (ALB) is one of the most important international trunk‐boring insect pests of forest trees, which has caused enormous losses in the forests of China, the USA and some countries in Europe. To investigate the morphology of the antennal, maxillary palp and labial palp sensilla in the five larval instars of the ALB, scanning electron microscopy was used to determine the typology, morphology, number and distribution of the sensilla. The antennae had two types of sensilla: the sensilla twig basiconica (s.t.b.) and sensilla basiconica. Three different types of sensilla were observed on the maxillary palps, which were the sensilla digitiformia, the sensilla chaetica and the s.t.b. The labial palps had two types of sensilla: the sensilla chaetica and the s.t.b. The s.t.b. had seven total subtypes, and the sensilla basiconica had two subtypes. The typology, quantity and distribution of sensilla on the antennae, maxillary palps and labial palps remained constant in the five larval instars, but the dimensions of all sensilla types increased throughout the development. We discussed the mechanoreception and the chemoreception of ALB larvae inside the host tree to provide a theoretical understanding and information for further research on the behaviour and the electrophysiology of this devastating forest pest.     

Comparative morphology of sensilla on antenna,maxillary palp and labial palp of larvae of Eucryptorrhynchus scrobiculatus (Olivier) and E. brandti (Harold) (Coleoptera: Curculionidae)

Eucryptorrhynchus scrobiculatus (Olivier) and E. brandti (Harold) are two wood boring pests of Ailanthus altissima (Mill.) Swingle (tree of heaven) and the variety Ailanthus altissima var. Qiantouchun. These beetles attack healthy trees and bore into roots and trunks during the larval stage. We studied the typology, distribution and morphostructure of the sensilla on the antennae, maxillary palps and labial palps of E. scrobiculatus and E. brandti larvae using scanning and transmission electron microscopy. The results showed the following: (i) the antennae of the two weevil larvae had two types of sensilla, sensilla basiconica (S.b.1 and S.b.2) and sensilla twig basiconica (S.tb.1‐S.tb.3), with S.tb.4 observed only on the antennae of E. brandti larvae; (ii) the maxillary palps had three types of sensilla, S.b.2, S.tb. (S.tb.2, S.tb.3 and S.tb.5) and digitiform sensilla; (iii) the labial palps had two types of sensilla, S.b.2 and S.tb. (S.tb.2, S.tb.3 and S.tb.5); (iv) the quantity and distribution of sensilla on the antennae, maxillary palps and labial palps remained constant between E. scrobiculatus and E. brandti larvae; and (v) sensilla basiconica had distinct sidewall pores, an apical pore was observed on sensilla twig basiconica, and digitiform sensilla were oval in shape, with a distinct apical pore. Based on the microstructure of the cuticle wall and dendrite, we hypothesized that these sensilla functioned as olfactory, gustatory and hygro‐/thermo‐receptors, respectively. We discuss the relationships among types of sensilla and the types of damage caused by the larvae inside the host tree to understand olfactory and gustatory receptor mechanisms. The results of this study will provide a firm basis for future electrophysiological studies.     

Ultrastructure and Comparative Morphology of Mouth-part Sensilla in Ground Beetle Larvae (Insecta, Coleoptera, Carabidae)

Labial and maxillary palps in 22 species of ground beetle larvae revealed the presence of four different types of sensilla: sensilla digitiformia, sensilla campaniformia, sensilla basiconica and sensilla chaetica. Using transmission electron microscopy techniques, the role of most of them was defined: sensilla campaniformia and sensilla chaetica are mechanoreceptors; while sensilla basiconica are chemoreceptors. Sensilla digitiformia can be both mechanoreceptors and chemoreceptors, though hygroreception may also be postulated on the basis of their abundance on the mouthparts of some hygrophilous species that depend on damp or wet patchy biotopes/seasons. The number and location of the sensory structures has been found to vary among the investigated taxa. The differences are related to the larval behavioural types, and are an adaptive response to different lifestyles, feeding habits and use of space.     

Sensilla on the palps and legs of the adult soft tick argas persicus oken (IXODOIDEA: ARGASIDAE) and their projections to the central nervous system

The sensory structures present on the palps and legs of adult Argas persicus Oken (Ixodoidea: Argasidae) were studied by light, scanning and transmission electron microscopy. The number, distribution, surface morphology and the fine structure of the prominent sensilla present on these appendages were determined. The palps have 2 morphologically prominent types of sensilla: one with a grooved surface of the hair and the other having a non-grooved hair. The TEM distinguishes at least 4 prominent subtypes in grooved sensilla with single or double lumina and dendrites occupying the periphery of the central lumen or distributed all over the central lumen. Amongst the sensilla with non-grooved hair-shaft, a rare type of Olfactory Mechanoreceptive (OM) sensillum was found on the palps and the first legs of A. persicus. At the base of the hair-shaft, the OM sensillum has 2 mechanosensory dendrites. The hair-shaft of the sensillum has a porous cuticle, characteristic of an olfactory sensillum. The lumen of the hair-shaft is invested with branching dendrites from 3–8 neurons, which are surrounded by 4 sheath cells. The sensilla on the legs, including those present in the Hallers organ, are of at least 3 prominent categories. (i) Single wall with un-innervated hair-shaft. (ii) Single wall, multiporous sensillum with dendrites present in the hair shaft. (iii) Double walls with spoke channels and dendrites present in the central lumen. Sensory projections from the crown of sensilla located on the distal end of the palp extend to the palpal and suboesophageal (SOG) ganglia. Projections in the SOG extend further to the contralateral side. Sensilla in the Hallers organ project to the first pedal ganglion and to the anterodorsal region of supraoesophageal ganglion. As expected, the primary sensory projections from the sensilla of the other 3 legs extend to the respective pedal ganglia.     

Sensilla of the antennae and the labial and maxillary palps of Blattella germanica (L.) (Dictyoptera: Blattellidae): Their classification and distribution

The various sensilla on the antennae and on the labial and maxillary palps of Blattella germanica (L.) were studied. Thick-walled chemoreceptors with fluted shafts and articulated bases are located on the antennae and on the labial and maxillary palps. Thin-walled chemoreceptors, without fluted shafts or articulated bases, are restricted to the flagellar segments of the antennae and to the distal segments of the palps. Antennae of adult males have more thin-walled chemoreceptors than do those of females. Hair-plate sensilla are found at the scape-head and scape-pedicel joints, and at the joints of segments on the palps. Campaniform sensilla are concentrated as a ring around the distal margin of the pedicel, and are also scattered singly on the scape, pedicel, and flagellar segments of the antennae, and on the first segment of the maxillary palps. Occasionally, a few sensilla coeloconica and cold receptor sensilla are found on the antennal flagellum.     

Sensing the Underground - Ultrastructure and Function of Sensory Organs in Root-Feeding Melolontha melolontha (Coleoptera: Scarabaeinae) Larvae

Introduction

Below ground orientation in insects relies mainly on olfaction and taste. The economic impact of plant root feeding scarab beetle larvae gave rise to numerous phylogenetic and ecological studies. Detailed knowledge of the sensory capacities of these larvae is nevertheless lacking. Here, we present an atlas of the sensory organs on larval head appendages of Melolontha melolontha. Our ultrastructural and electrophysiological investigations allow annotation of functions to various sensory structures.

Results

Three out of 17 ascertained sensillum types have olfactory, and 7 gustatory function. These sensillum types are unevenly distributed between antennae and palps. The most prominent chemosensory organs are antennal pore plates that in total are innervated by approximately one thousand olfactory sensory neurons grouped into functional units of three-to-four. In contrast, only two olfactory sensory neurons innervate one sensillum basiconicum on each of the palps. Gustatory sensilla chaetica dominate the apices of all head appendages, while only the palps bear thermo-/hygroreceptors. Electrophysiological responses to CO₂, an attractant for many root feeders, are exclusively observed in the antennae. Out of 54 relevant volatile compounds, various alcohols, acids, amines, esters, aldehydes, ketones and monoterpenes elicit responses in antennae and palps. All head appendages are characterized by distinct olfactory response profiles that are even enantiomer specific for some compounds.

Conclusions

Chemosensory capacities in M. melolontha larvae are as highly developed as in many adult insects. We interpret the functional sensory units underneath the antennal pore plates as cryptic sensilla placodea and suggest that these perceive a broad range of secondary plant metabolites together with CO₂. Responses to olfactory stimulation of the labial and maxillary palps indicate that typical contact chemo-sensilla have a dual gustatory and olfactory function.     

Ultrastructure of sensilla on the maxillary and labial palps of three species (Coleoptera: Staphylinidae: Staphylininae)

Most species of Staphylinidae are predators in an agroecosystem. They acquire prey information from their environment through receptors. In this study, the sensilla on maxillary and labial palps of Philonthus kailiensis, Philonthus lewisius and Quedius robustus were examined with scanning electron microscopy to identify and analyse the external morphology and distribution of the sensilla to enhance our knowledge of the sensilla of Staphylinidae and provide a rationale of taxonomical studies on the two genus. Results showed that the sensilla are classified into six types: Böhm bristles, sensilla chaetica, sensilla furcate, sensilla coeloconica, sensilla placodea and sensilla basiconica. No sexual dimorphism exists among the three species. The relationships and functions of sensilla on maxillary and labial palps were also speculated. There may be a certain correlation between the sensilla on maxillary and labial palps of the staphylinid and its habitat.     

Morphology,distribution, ultrastructure,and possible function of the external sensilla on antennae and mouthparts of Echinothrips americanus Morgan (Thysanoptera: Thripidae)

To better understand the semiochemical detection and reception mechanisms that involved in intra- and interspecific communication, host selection and mating behavior of Echinothrips americanus (Thysanoptera: Thripidae), scanning electron microscopy was used to examine the external morphology, distribution and ultrastructure of the sensilla on antennae and mouthparts. According to serial SEM images, seven types of antennal sensilla in total were observed in both sexes. Sensilla on mouthparts were observed concentrating on the maxillary palps, labial palps, and paraglossa, which is consistent with the previous conclusions. Possible function of the external sensilla is also discussed.     

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.     

Sexual dimorphism of adult labial palps of the peach fruit moth Carposina sasakii Matsumura (Lepidoptera: Carposinidae) with notes on their sensilla

The labial palps and their sensilla of the peach fruit moth Carposina sasakii Matsumura, a serious pest of pome fruits in eastern Asia, were investigated using light microscopy and scanning and transmission electron microscopy. The labial palps are three‐segmented and exhibit distinct sexual dimorphism in length: much longer in the female than in the male. Four types of sensilla were found on the labial palps: campaniform, squamiform, chaetic and flattened sensilla. The campaniform sensilla are present on the first segment alone. The squamiform sensilla are located on all the three segments. The chaetic sensilla are mainly present on the third segment. The flattened sensilla are grooved with wall pores and situated in a labial palp‐pit organ, which is located at the apex of the distal segment of the labial palp. The sexual dimorphism of the labial palp and the labial palp‐pit organ was briefly discussed.     

Relationship between the olfactory sensilla of Papilio demoleus L. larvae and their orientation responses to different odours

Papilio demoleus larvae showed maximum attraction to odours of citral, cirtonellal and citronellol, slightly less to geraniol and 1-limonene, and low attraction to hydroxy-citronellal and geranyl acetate. These chemicals (except the last) are the main odorous constituents of the insect's host plant (Citrus) leaves. Phellandrene was almost inert, whereas farnesol and d-limonene elicited a low, and linalool, eugenol and clove oil a high repulsion. Larvae deprived of one antenna and both maxillary palps were similar to normal larvae in their orientational responses. Normal larval responses changed with the inactivation of one or more of the three specific antennal sensilla. A full complement of the three sensilla was not essential for the normal larval response to certain chemicals. Any of the sensilla singly or in combination with any other sensillum could mediate the normal larval response (attraction) to citral and geraniol. For a few other chemicals, certain specific sensilla, singly or in a combination of two, mediated the normal response. Only for d-limonene were all three sensilla essential for the normal response.     

Olfactory sensilla on the antenna and maxillary palp of the sheep head fly,Hydrotaea irritans (Fallen) (Diptera : Muscidae)

Antennae and maxillary palps of both sexes of the Sheep Head fly Hydrotaea irritans (Diptera : Muscidae) were investigated using scanning electron microscopy to describe the types, morphology, and distribution of olfactory sensory structures. Only socketed bristles and microtrichia were found on the scape of the antennae. These structures were also observed on the pedicel together with a group of 7–8 as yet undescribed sensilla, whose function is unknown. Olfactory sensilla were not found on these 2 segments or on the arista. Large numbers of olfactory sensilla and microtrichia were present on the funiculus. The former included sensilla trichodea (thick-walled, multiporous sensilla), sensilla styloconica and 6 types of sensilla basiconica (thin-walled, multiporous sensilla), 4 of which occurred individually and 2 of which were found in groups. An olfactory pit containing groups of thin-walled multiporous sensilla was located on the dorsomedian side of the funiculus. All sensilla basiconica were classified on morphological characteristics. The maxillary palps were covered with microtrichia and socketed bristles, but only 1 type of olfactory sensillum was found. This was a type of sensillum basiconicum that differed from any of those found on the antennae. No differences were found in sensilla diversity and distribution between males and females.     

The quill mite <Emphasis Type="Italic">Syringophilopsis fringilla</Emphasis> (Fritsch) (Acari: Trombidiformes: Syringophilidae): the structure of sensory organs providing feeding of the parasite in the feather quill

The structure of the sensory organs situated on palps and chelicerae of the quill mite Syringophilopsis fringilla (Fritsch, 1958) was examined with the use of scanning and transmitting electron microscopy. The tarsal segment of the palps bears 8 sensilla of three types: two contact chemo-mechanoreceptor sensilla, a single chemoreceptor (olfactory) sensillum, and five tactile mechanoreceptor sensilla. All other sensilla situated on basal palpal segments and on cheliceral stylets are represented exclusively by tactile mechanoreceptors. A proprioceptor sensillum was revealed in the movable digit of chelicerae; the modified cilia of dendrites of 5 sensory neurons of this sensillum run inside the inner non-sclerotized core of the stylet and end at different levels in its apical part, attaching to electron-dense rods connected with a sclerotized sheath of the stylet. The authors assume that the proprioceptor sensillum of the stylet detects the strength of the pressure of the stylet of the movable digit on the quill wall during its piercing, and palpal sensilla determine the optimal place for this process.     

Ultrastructure du labium de la larve du Speophyes lucidulus delarouzeei (Coleoptera,Catopidae)

We successively examined the two main parts of the labium: the ligula and the palps. The organs located on the ligula have a simple innervation and may represent various types of mechanoreceptors. The palps are crowned by 13 different sensilla which have various receptions (mechanoreception, olfaction, gustation). Several described sensilla hold an unknown function.     

Structural and functional aspects of sense organs on the maxillary palps of Calliphora vicina

The maxillary palps of the blowfly Calliphora vicina Robineau-Desvoidy are shown to bear, in addition to long mechanoreceptive hairs, small sensilla basiconica ccontaining three neurons. The electrical responses obtained with a simple qualitative olfactometer indicate an olfactory function. The palpal sensilla showed high sensitivity to cycloheptanon, whereas the antennal organs were more strongly stimulated by heptylalcohol, which indicates the presence of carrion receptors.     

The integument and sensilla of the pregenital abdomen of the Desert locust (Schistocerca gregaria) (Orthoptera: Acrididae)

The integument and sensilla of the abdominal segments II–VII, together with the tracheal and nerve supply, are described in so far as they can be seen using whole mounts. Such a method often enables the neurons of the sensilla to be seen clearly and to be associated definitely with a certain cuticular structure. The sensilla are compared with those already known from the palps, and it is concluded that probably all those on the abdomen also occur on the palps.     

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.     

Fine structure and primary sensory projections of sensilla on the maxillary palp of Drosophila melanogaster Meigen (Diptera : Drosophilidae)

Three types of hairs were identified on the maxillary palp of Drosophila melanogaster Meigen (Diptera : Drosophilidae): (i) single-walled, multiporous sensilla basiconica, which constitute 75% of the innervated hairs; (ii) thick walled non-porous sensilla trichodea, which make up the remaining 25% of the innervated hairs; and (iii) numerous spinules, which are un-innervated. These sensilla basiconica uniformly contain 2 bipolar sense cells, whereas sensilla trichodea have a single dendrite with a tubular body at the base of each hair. A majority of the sensilla basiconica is located on the distal half of the dorsal surface, whereas sensilla trichodea are positioned on the tip and entire ventrolateral ridge of the palp. Approximately 125 axons of the sense cells join to form a single nerve. The structure of sensilla basiconica and sensilla trichodea suggests that they are olfactory and mechanosensory respectively. The contact chemoreceptors (gustatory sensilla) are conspicuously absent on the maxillary palp.Golgi silver impregnations and cobalt fills show that the primary sensory fibres from sensilla trichodea and sensilla basiconica on the maxillary palp project in the posterior suboesophageal ganglion (SOG) and the antennal lobe respectively. A single fibre projects separately either in the SOG or in the antennal lobe. In the antennal lobe, the input received from sensilla basiconica is usually bilateral and at least 5 glomeruli are innervated symmetrically on either side from both the palps.This study suggests that the sensory neurons are capable of making selective projections in the specific regions of the brain. Accordingly, the fibres from a sensillum project to the brain with respect to their functions and the individual glomeruli represent functional units of the brain, receiving inputs in a characteristic combination.