The sensory systems and feeding behavior of leafhoppers. I. The aster leafhopper,Macrosteles fascifrons stål (homoptera,cicadellidae)

The ultrastructure of the sensilla, and other structures, within the stylets and precibarium of Macrosteles fascifrons were examined by transmission and scanning electron microscopy. Precibarium is a new term, defined here, for the canal that precedes the cibarium inside the leafhopper head. Within the precibarium are found 20 chemosensilla and a previously undescribed structure, the precibarial valve. Twelve mechanosensilla, three in each stylet, are found within the maxillary and mandibular stylets. The relationship between all of these structures and feeding by the insect is detailed in a feeding mechanism hypothesis. It is concluded that leafhoppers (and probably all homopterans) utilize the precibarial chemosensilla alone for gustatory discrimination, the stylet sensilla for proprioception, and the precibarial valve for regulation of fluid uptake and compartmentalization of the sensilla.     

Fine structure and sensory apparatus of the mouthparts of the pear psyllid,Cacopsylla chinensis (Yang et Li) (Hemiptera: Psyllidae)

The pear psyllid, Cacopsylla chinensis (Yang et Li) (Hemiptera: Psyllidae), is one of the most significant economic pests of pear in China, causing direct damage through feeding by the highly specialized piercing–sucking mouthparts. The ultrastructural morphology and sensory apparatus of the mouthparts of the adult were examined using scanning and transmission electron microscopy. The piercing–sucking mouthparts of C. chinensis are composed of a three-segmented labium with a deep groove in the anterior side, a stylet fascicle consisting of two mandibular and two maxillary stylets, and a pyramid-shaped labrum. Proximal to the labium, the stylet fascicle forms a large loop within a membranous crumena. Mandibles, with more than ten teeth on the external convex region, can be seen on the distal extremity. Smooth maxillary stylets are interlocked to form a larger food canal and a smaller salivary canal. One dendritic canal housing 2 dendrites is also found in each mandible. Two types of sensilla trichodea, four types of sensilla basiconica, single as well as groups of sensilla campaniformia, and oval flattened sensilla occur in different locations on the labium, whereas a kind of sensilla basiconica is at the junction of the labrum and anteclypeus. Sensilla trichodea and sensilla campaniformia, always present with denticles, are present on the middle labial segment. Three types of sensilla basiconica, two types of sensilla trichodea and two oval flattened sensilla are located on the distal labial segment. The mouthpart morphology and abundance of sensilla located on the labium in C. chinensis are illustrated, along with a brief discussion of their taxonomic and putative functional significance.     

Ultrastructure of the mouthparts of adult sweetpotato whitefly,Bemisia tabaci Gennadius (Homoptera: Aleyrodidae)

The fine structure of the mouthparts of the whitefly, Bemisia tabaci Gennadius (Homoptera: Aleyrodidae), was examined by scanning and transmission electron microscopy. Adult whitefly mouthparts are similar to those of other homopterans, especially aphids, being composed of the labrum, the labium, and the stylets. The stylet bundle is the feeding organ of the whitefly and is composed of 2 mandibular stylets and 2 maxillary stylets. Mandibular stylets, which are located on the outer aspect of the stylet bundle, each contain 2 dendrites. The tips of the mandibular stylets are curved inward, and there are barb-like ridges on the lateral aspects, which probably function in piercing and cutting plant tissues and in anchoring the stylets in the tissues. The maxillary stylets are not innervated and are interlocked to form 2 separate compartments, the food canal and salivary canal. At the distal end of the interlocked maxillary stylets, there is a small depression, which may allow for mixing of the salivary canal and food canal components. Movement of the B. tabaci stylets during feeding is discussed in comparison with other homopterans.     

Mouthpart morphology and stylet penetration of host plants by the glassy-winged sharpshooter, Homalodisca coagulata, (Homoptera: Cicadellidae)

The ultrastructural morphology of the mouthparts of the glassy-winged sharpshooter, Homalodisca coagulata, and method of plant penetration was examined using light microscopy, scanning electron microscopy, and transmission electron microscopy methods. The gross morphology of the labrum, labium, and stylet fascicle was consistent with what has been described for other plant-sucking homopterans. The ultrastructural examination of the mouthparts revealed unique details that have previously gone unreported. Several types of sensilla-like structures having the form of pegs and multi-lobed objects were identified on the outer surfaces of the labrum and within the labial groove. Dendritic canals terminated in an extensive network of smaller canals at the distal tip of the maxillary stylets below a series of surface denticles suggesting that this area may have a sensory function associated with locating xylem elements of host plants. Examination of salivary sheath pathways established that 65% of the plant penetrations by this insect terminated in the xylem vessels of the host plant. Probing by the insect was largely intracellular and terminal branching of a single probe site was common. Plant surface feeding sites varied with the stage of development which correlates with the depth of the xylem vessels and the length of the maxillary stylets of the various instars.     

Morphology of the mouthparts of the spittlebug Philagra albinotata Uhler (Hemiptera: Cercopoidea: Aphrophoridae)

Mouthparts associated with feeding behavior and feeding habits are important sensory and feeding structures in insects. To obtain a better understanding of feeding in Cercopoidea, the morphology of mouthparts of the spittlebug, Philagra albinotata Uhler was examined using scanning electron microscopy. The mouthparts of P. albinotata are of the typical piercing–sucking type found in Hemiptera, comprising a cone-shaped labrum, a tube-like, three-segmented labium with a deep groove on the anterior side, and a stylet fascicle consisting of two mandibular and two maxillary stylets. The mandibles consist of a dorsal smooth region and a ventral serrate region near the apical half of the external convex region, and bear five nodules or teeth on the dorsal external convex region on the distal extremity; these are regarded as unique features that distinguish spittlebugs from other groups of Hemiptera. The externally smooth maxillary stylets, interlocked to form a larger food canal and a smaller salivary canal, are asymmetrical only in the internal position of longitudinal carinae and grooves. One dendritic canal is found in each maxilla and one in each mandible. Two types of sensilla trichodea, three types of sensilla basiconica and groups of multi-peg structures occur in different locations on the labium, specifically the labial tip with two lateral lobes divided into anterior sensory fields with ten small peg sensilla arranged in a 5 + 4 + 1 pattern and one big peg sensillum, and posterior sensory fields with four sensilla trichodea. Compared with those of previously studied Auchenorrhyncha, the mouthparts of P. albinotata may be distinguished by the shape of the mandibles, the multi-peg structures and a tooth between the salivary canal and the food canal on the extreme end of the stylets. The mouthpart morphology is illustrated using scanning electron micrographs, and the taxonomic and putative functional significance of the different structures is briefly discussed.     

Precibarial and cibarial chemosensilla in the whitefly,Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae)

The internal anatomy of the anterior alimentary canal of the whitefly, Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) B-biotype, was examined by light, scanning, and transmission electron microscopy to elucidate the location and number of precibarial and cibarial gustatory sensilla. Elucidation of the epipharyngeal organ complex within the precibarium revealed 10 precibarial sensilla located proximal to where the paired maxillary stylets diverge on their retraction. The sensory organ complex within the cibarium consists of 8 sensilla, 6 on the epipharyngeal sclerite with 2 found within the hypopharyngeal sclerite. Fine structure investigation revealed the individual neurons to terminate at sensillar pores, which allow direct contact with passing fluids, thus supporting a chemosensory function. Ultrastructure of the neurons is similar to that of precibarial and cibarial gustatory chemosensilla found in other piercing-sucking insects. Their importance to whitefly feeding is discussed.     

Pronymphs,hatching, and proboscis assembly in leafhoppers and froghoppers (Hemiptera,Cicadellidae and Aphrophoridae)

Pharate 1st instar nymphs enclosed in the embryonic cuticle, referred to as pronymphs, were studied in a froghopper Aphrophora pectoralis Mats. (Aphrophoridae) and the leafhoppers Oncopsis flavicollis (L.), Populicerus populi (L.), Alebra wahlbergi (Boh.), Igutettix oculatus (Lindb.), and Scenergates viridis (Vilb.) (Cicadellidae). The species vary in the relative length of the pronymphal antennae and details of sculpturing of the cephalic region. No egg bursting structures were observed, except small denticles on the crown region of S. viridis pronymphs. Rudimentary mandibular and maxillary stylets of a pronymph are external, short, tubular appendages containing tips of the corresponding nymphal stylets, whose more basal parts develop inside of the head. Casting off of the embryonic cuticle results in the nymphal stylets being passively pulled out and assuming a close-set parallel orientation. Once the sheaths of unsclerotized cuticle secreted by the peripodial epithelium and enveloping each developing stylet have been cast off with the exuviae, the bare stylets become squeezed and interlocked into a functional bundle. The roles of the maxillary plates, clypeus, labrum, and labium in the stylet bundle assembly are discussed. The process repeats after each molt.     

Opening mechanism of the mouth of the hematophagous hemipteran, Triatoma infestans

A morphological study of the tips of the stylets in an haematophagous hemipteran has been performed with a scanning microscope in order to determine both the relative positions of the mouthparts during a meal, and the means by which the ‘functional mouth’ can open. If the stylets of Triatoma are examined following severance of the labium, differences in the morphology and relative position of the two maxillary tips are observed. When, prior to a meal, the insect explores the medium with its mouthparts, the tips of its maxillary stylet are united. By contrast, when the bug is pumping food the left stylet is retracted relative to the right stylet and its tip is bent outwards.We have studied the mechanics of the system which allows the tip of the left maxillary to rock, resulting in the opening of the alimentary canal. Finally, we have re-examined the stylet movements of dissected animals in the light of these new morphological findings.     

Fine structure of the mouthparts of Diostrombus politus and Proutista moesta (Hemiptera: Derbidae)

Insect mouthparts are important sensory and feeding structures, morphological studies of this organ can provide additional data for phylogenetic studies. The planthopper superfamily Fulgoroidea is among the dominant groups of phytophagous insects, however, the mouthparts ultrastructure of this superfamily remains unsatisfactorily studied. This study investigates the ultrastructure of the mouthparts of two species in the family Derbidae (Hemiptera: Fulgoroidea), Diostrombus politus Uhler and Proutista moesta (Westwood), using a scanning electron microscope. The results show that these two derbids are of a typical piercing-sucking type found in Hemiptera. They consist of a cone-shaped labrum, a three-segmented labium and a stylet fascicle with two interlocked maxillary stylets incompletely wrapped by two mandibular stylets. The arrangement of the sensilla on the labial tip differ slightly between the two derbid species, and the subapical labial sensilla are likely different among genera in the family Derbidae.     

Morphological description of the mouthparts of the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae)

Scanning (SEM) and transmission (TEM) electron microscopy were used to elucidate the morphology of the rostrum, as well as the mandibular and maxillary stylets of the psyllid Diaphorina citri, vector of phloem-inhabiting bacteria associated with citrus huanglongbing (HLB) disease. D. citri has a cone-shaped rostrum that extends behind the pair of prothoracic coxae. The stylet bundle comprises a pair of mandibular (Md) and maxillary (Mx) stylets with a mean length of 513.3 μm; when retracted, their proximal portions form a loop and are stored in the crumena (Cr). Serial cross-sections of the rostrum revealed that the mandibles are always projected in front of the maxillary stylets. The two maxillary stylets form the food and salivary canals, with diameters of 0.9 μm and 0.4 μm respectively. These two canals merge at the end of the stylets forming a common duct with a length of 4.3 μm and a mean diameter of 0.9 μm. The acrostyle, a distinct anatomical structure present in the common duct of aphid maxillary stylets, was not observed by TEM in the ultrathin cross-sections of the common duct (CD) of D. citri. This study provides new information on D. citri mouthparts that may help to understand the feeding behaviour of this important vector of HLB-associated bacteria.     

The sensory systems and feeding behavior of leafhoppers. II. A comparison of the sensillar morphologies of several species (Homoptera: Cicadellidae)

The ultrastructure of the sensilla, and other structures, within the precibaria of eight species from three subfamilies of leafhoppers (Homoptera: Cicadellidae) were examined with scanning electron microscopy. The types and grouping of the 20 precibarial sensilla in seven of these species were similar to those observed previously in Macrosteles fascifrons Stål. Oncometopia nigricans (Walker) also displayed similar sensilla groups; however, it had 30 sensilla. The species examined differed chiefly in the exact location and arrangement of the sensilla. The possible significance of the differences relative to leafhopper feeding is discussed. The precibarial chemosensilla may provide chemosensory evaluation of fluid in the food canal and precibarium prior to ingestion or egestion.     

Oviposition behaviour in Lygus rugulipennis: a morpho-functional study

Before oviposition, a Lygus rugulipennis (Poppius) (Heteroptera: Miridae) female explores the substrate with her mouthparts, performing ‘probing’ behaviour which eventually leads to a choice of oviposition site. In this study, morphological and behavioural observations were carried out in order to define the mechanisms through which female bugs recognise suitable oviposition sites. The morphological study was conducted using electron‐microscopy techniques, while the behavioural experiments aimed at the temporary (using ZnSO₄) or permanent (i.e., cauterization of the rostrum and ablation of both stylets and labium) inactivation of sensory structures located in the labium tip and in the stylets, which are probably involved in oviposition site selection. The tip of the labium of L. rugulipennis females is characterised by the presence of 11–12 uniporous gustatory sensilla which are innervated by 3–6 sensory neurones. One aporous mechanoreceptor is located ventrally on both areas of the labium tip. Other aporous mechanosensilla are found more proximally on the labium. ZnSO₄ labium tip treatment did not affect oviposition site selection, while stylet amputations, as well as rostrum cauterisations, resulted in almost complete oviposition failure. Labium tip‐ablated females oviposited similarly to control females. These results suggest that the sensory neurones associated with the stylets are involved in the location of the oviposition site. Uniporous gustatory sensilla on the labium tip are not involved in the final steps of the oviposition behaviour. However, they seem to play a role in assessing the suitability of the substrate as a food source.     

Development of the mouthparts in embryos of Haplothrips verbasci (Osborn) (Insecta,Thysanoptera, Phlaeothripidae)

The asymmetric “punch and suck” mouthparts of larval Haplothrips verbasci develop from paired appendages in the late, post-anatrepsis embryo similar to those of other insects. Later, the labrum flexes ventrally over the stomodaeum, the right mandibular appendage degenerates, the maxillary appendages divide into inner (lacinial) and outer (stipital) lobes, and the hypopharynx arises from the venters of the mandibular and maxillary segments. All cephalic segments consolidate anteriorly prior to katatrepsis, their appendages flex ventrally, and the labial appendages fuse medially to form the labium and the primordia of the salivary glands and valve. The left mandible and the lacinial lobes of the maxillae invaginate into the head during and after katatrepsis to form the mandibular and maxillary stylet-secreting organs and these later deposit the cuticle of their respective stylets. Cuticle of the mandibular lever is deposited by labral cells at the apex of the mandibular sheath during and after hatching. That of each maxillary lever is secreted simultaneously into the lumen of a ventrally-directed diverticulum developing from stipital cells at the apex of each maxillary sheath. Shortly after katatrepsis, the maxillary and labial palpi originate respectively from cells in the outer wall of each stipital lobe and at the apex of the labium. Muscles of the mouthparts arise after katatrepsis from cephalic mesoderm and are fully-differentiated before cuticle of the mandibular and maxillary levers has been deposited. Gnathal morphogenesis in embryos of H. verbasci resembles that occurring in bug embryos and provides additional evidence that Thysanoptera and Hemiptera evolved from a common psocopteroid stem species having small, paired, biting and chewing mandibles and well developed lacinial stylets.     

Pathway phase waveform characteristics correlated with length and rate of stylet advancement and partial stylet withdrawal in AC electrical penetration graphs of adult whiteflies

A technique was developed for measuring the length of stylet insertion during adult whitefly probing. The distance that the labium shortens during a probe was shown to be equal to the length of stylets that were inserted into the plant tissue. The length of labial shortening then was measured in high-magnification video recordings of adult female silverleaf whitefly, Bemisia argentifolii, in conjunction with recording electrical penetration graphs (EPGs – AC method). Using a split-screen device, video images of the whitefly's labium during a probe and the EPG waveforms produced during the probe were recorded simultaneously on the same video tape. On playback, changes in labial length could be measured during specific EPG waveforms to determine the length of stylet insertion that occurred during the waveforms. The focus of the study was on two characteristics of the pathway phase sawtooth waveform: the frequency of voltage peaks and the increase in voltage level that occurs over time during sawtooth waveforms. The rate of stylet penetration was significantly and positively correlated with frequency of sawtooth waveform voltage peaks (r ²=0.33) and the length of stylet penetration was significantly and positively correlated (second-order polynomial) with the relative difference in voltage level between the beginning and end of the sawtooth waveform (r ²=0.43). Stylet advancement did not appear to occur during the few low-flat waveforms (unknown behavioral correlation) and high-flat waveforms (phloem phase) that were observed. Voltage drops occur sporadically during sawtooth waveforms, and these were associated with partial stylet withdrawal (indicated when the labium increased in length, but the probe was not terminated) with an accuracy of 99%.     

Sensory receptors associated with the stylets and cibarium of the rice brown planthopper,Nilapavarta lugens

Summary The stylets of Nilapavarta lugens consist of two maxillae that interlock to form separate food and salivary ducts partially surrounded by two mandibles. The ultrastructure of the sensory innervation of the stylets is described. Each maxilla possesses five neurones which extend to the tip of the stylet. The mandibles also contain five neurones, four of which are paired. The paired neurones comprise a shorter dendrite extending part of the way along the stylet and a longer one extending to the tip. The possible functions of these neurones are discussed. Gustatory receptors are located in the small passageway leading from the food duct to the cibarium. The receptors are in two distinct groups on the epipharyngeal side and one group on the hypopharyngeal side of the food canal. Two to five neurones innervate each receptor which connects to the food canal via a small pore.     

Morphology of the sweet potato whitefly,Bemisia tabaci (Homoptera,Aleyrodidae) relative to virus transmission

 The stylet bundle of the sweet potato whitefly, Bemesia tabaci, consists of paired mandibles and maxillae. The latter interlock to form the food and salivary canals. Its salivary system consists of paired primary and accessary glands in the thorax. Primary and accessory gland ducts on each side of the nerve cord fuse to form lateral ducts that course anteroventrally to the midline and continue in parallel down the hypopharynx to eventually fuse to form the single afferent duct of the salivary pump. Saliva exiting the pump via the efferent duct enters the salivary canal of the maxillae. Food from the maxillary food canal passes from the antecibarium to the postcibarium or sucking pump and, per os, to the pharynx and esophagus of the foregut. The esophagus extends from the head to the base of the abdomen where it and the anterior midgut intimately mingle with the anterior hindgut to form a filter chamber. The midgut then proceeds dorsocaudally before looping anteroventrally to join the hindgut. The latter gives off two fingerlike Malpighian tubules before entering the filter chamber, whence it proceeds dorsocaudally to the anus within the vasiform orifice. Where possible, the morphology of Bemisia is discussed in relation to plant virus transmission and the morphologies of more thoroughly studied homopteran vectors such as aphids and leafhoppers. Accepted: 9 July 1996     

The mechanism of stylet movement in Psylla malt Schmidberger (Homoptera:Psyllidae)

The stylet movements in protracting, retracting and non-progressing stylet bundles of fifth stage nymphs of Psylla mali are described, together with observations on the role of the labium.     

Studies on the tardigrades. I. Fine structure of the anterior foregut of Milnesium tardigradum Doyère

The fine structure of the anterior foregut of the tardigrade Milnesium tardigradum is presented. The oral region consists of a terminal mouth opening surrounded by six plate-like lips lying within a circlet of six prominent papillae. The buccal cavity is enclosed within a thick cuticular tube which possesses appendage structures, the stylet sheaths, stylet supports and paired protrusible stylets. Two large salivary glands envelop the buccal structures and contain voluminous amounts of secretory product. The arrangement, possible functions and phyletic significance of these structures are discussed.     

Mouthparts and stylet penetration of the lac insect Kerria lacca (Kerr) (Hemiptera:Tachardiidae)

Hitherto less known aspects on mouthpart morphology and penetration mechanism of the lac insect Kerria lacca have been explored. Unique details of the mouthparts, i.e. morphology of labium and stylets and salivary sheath have been brought out. The gross morphology of the mouthparts though resembled other plant sucking homopterans; a two-segmented labium with symmetrically distributed six pairs of contact-chemoreceptors on its surface was distinct; the mandibular stylets had serrations on its extreme apical region, while the maxillary stylets had their external surface smooth with parallel longitudinal grooves on their inner surface. Formation of flanges, salivary sheath and penetration pathway observed along with probing and penetration of the stylets intracellularly up to the phloem cells, as illustrated herein, are the addition to the existing knowledge on the structural details of the mouthparts and the feeding behavior thereupon.