Mouthparts of flower-visiting insects

This review deals with the morphology and function of adult insect mouthparts modified to feed on nectar, pollen or petals. Specialization to nectar-feeding is evident in formation of proboscides of various lengths and designs. Proboscides of many Hymenoptera and Diptera function according to adhesion mechanisms that load nectar onto extensible apical mouthpart regions before fluid is conveyed along the food canal to the mouth by capillarity and suction. Predominantly suctorial proboscides evolved once in Lepidoptera, probably twice in Coleoptera, variously in some Hymenoptera and several times with similar design in Diptera. Many of them are particularly long and have sealed food tubes, specialized apical regions, new proboscis resting positions and modified feeding movements. Mouthparts of obligate pollen-feeding insects can be characterized by modified mandibles, specialized bristles for pollen manipulation and elaborate feeding movements. Often saliva is crucial for pollen retention and ingestion. In Coleoptera, intact pollen is gathered by sweeping movements of mouthparts; in Diptera, it is suspended in saliva prior to suction. Pollen is crushed by asymmetrical mandibles in aglossatan Lepidoptera and one group of basal Hymenoptera. Pollen-piercing mouthparts occur in Thysanoptera and one group of Diptera. Some butterflies and few Diptera extract nutrients from pollen by mixing it externally with saliva on their mouthparts. No mouthpart specializations to petal-feeding are reported in flower-visiting insects.     

Presence and distribution of sensory structures on the mouthparts of self-medicating moths

Unique structures often accompany unusual feeding behaviors in erebid moths. We test whether self-medicating (e.g., pharmacophagous) adult tiger moths have specialized structures on their mouthparts. We examined mouthparts of pharmacophagous and non-pharmacophagous adults using scanning electron microscopy (SEM). Self-medicating adults had significantly higher numbers of chemosensory structures when compared with non-self-medicating adults. Putative olfactory sensilla are reported on the proboscis of Nyctemera coleta and pollen grains were found adhered to the proboscis of Nyctemera secundiana. Sensilla on the observed tiger moth proboscides may play a role in the recognition of pyrrolizidine alkaloid plants by pharmacophagous adults.     

Presence and distribution of sensory structures on the mouthparts of self-medicating moths

Unique structures often accompany unusual feeding behaviors in erebid moths. We test whether self-medicating (e.g., pharmacophagous) adult tiger moths have specialized structures on their mouthparts. We examined mouthparts of pharmacophagous and non-pharmacophagous adults using scanning electron microscopy (SEM). Self-medicating adults had significantly higher numbers of chemosensory structures when compared with non-self-medicating adults. Putative olfactory sensilla are reported on the proboscis of Nyctemera coleta and pollen grains were found adhered to the proboscis of Nyctemera secundiana. Sensilla on the observed tiger moth proboscides may play a role in the recognition of pyrrolizidine alkaloid plants by pharmacophagous adults.     

A revision of the genus Paradoxostoma Fischer (Crustacea; Ostracoda) in British waters

Species of the genus Paradoxostoma Fischer are an important component of marine and estuarine ostracod faunas throughout the world. This revision of the genus in British waters deals with 17 species of which six are described as new. Each species is diagnosed and illustrated in detail, and comments are made on their ecology and distribution. The specialized mouthparts which characterize the genus are illustrated by means of the scanning electron microscope for the first time. A key to the genus is given.     

Pollen grains adhere to the moist mouthparts in the flower visiting beetle Cetonia aurata (Scarabaeidae, Coleoptera)

Flower visiting beetles possess numerous structural adaptations of their mouthparts to adhere and ingest pollen grains. Using a Cryo-SEM approach the examination of the mouthparts in rapidly frozen Cetonia aurata (Scarabaeidae) indicates a previously unknown technique of pollen uptake in Coleoptera. Cryo-SEM micrographs of the mouthparts reveal a fluid covering the bristles on the buccal surface. In this way the bristles of the galeae form a wet brush which represents the primary organ of pollen uptake. The fluid improves adhesion of pollen to bristles lacking any specialized adhering surface or highly sculptured cuticle as present in other pollen feeding Coleoptera. The well developed mola region of the otherwise non-biting mandibles of C. aurata indicates that these beetles open pollen grains mechanically before ingestion. Examination of gut content demonstrated that crushed and intact pollen occur in all regions. The Cryo-SEM method represents a new approach to study functional morphology including the interaction of microstructures and fluids on cuticular surfaces of insects. Handling editor: Gimme Walter     

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.     

Function and functional groupings of the complex mouth apparatus of the squat lobsters Munida sarsi Huus and M. tenuimana G.O. Sars (Crustacea: Decapoda).

Like all other decapods, the anomuran squat lobsters Munida sarsi and M. tenuimana have a mouth apparatus composed of six pairs of mouthparts plus labrum and paragnaths (upper and lower lips). To study the functional significance of this complexity, we examined the mouthparts with scanning electron microscopy and also observed their function directly, under laboratory conditions, using macro-video equipment. No differences were found between the two species. The movement patterns of the mouthparts are described in detail and illustrated as serial drawings. Proceeding from maxillipeds 3 towards the mandibles, the movement pattern gets increasingly stereotypical, with the mandibles performing but a single movement in a medio-lateral plane. From morphology, the mouthparts are subdivided into 20 parts, but from the functional analyses the 20 parts form 8 functional groups: 1, transporting mouthparts (maxilliped 2 endopod and maxilliped 3 endopod); 2, transporting-aligning mouthparts (maxilliped 1 basis); 3, sorting-aligning mouthparts (maxilla 1 basis and maxilla 2 basis); 4, current-generating mouthparts (flagella of maxilliped 2 and maxilliped 3 exopods); 5, cutting-crushing mouthparts (incisor and molar processes, labium, and mandibular palp); 6, ingesting mouthparts (maxilla 1 coxa, maxilla 2 coxa, and maxilliped 1 coxa); 7, respiratory mouthparts (scaphognathite, maxilliped 1 epipod, and maxilliped 2 and maxilliped 3 exopods); and 8, dorso-ventral mouthparts (maxilla 1 endopod, maxilla 2 endopod, maxilliped 1 endopod, and maxilliped 1 exopod). These groupings apply mostly to the processes of food handling and have little significance with respect to grooming. When comparing our results to the literature on other decapods, we found much resemblance to conditions in other anomurans.     

The mouth apparatus of Lithodes maja (Crustacea: Decapoda) – form,function and biological role

Being able to utilize many different food resources is probably an important aspect of the success of decapod crustaceans which fill a wide range of various ecological niches worldwide. The phenomenon is facilitated by the complex mouth apparatus found in this group, whose representatives possess six pairs of mouthparts– mandibles, maxillae 1, and maxillae 2 and three maxillipeds, the first three pairs of thoracic appendages which are also specialized to food manipulation. These six pairs are able to perform a number of movements for transporting, aligning, crushing and cutting. Studies into the functional morphology of mouthparts have already been carried out in some decapod species. This study focuses on Lithodes maja, a species of the hitherto understudied king crabs (Lithodidae), chosen on the grounds of their remarkable evolutionary history as ‘derived hermit crabs’. Individuals were filmed while being presented with different kinds of food. To obtain structural information on the individual mouthpart elements as naturally arranged in relation to one another, the shape of the mouthparts was 3D‐reconstructed from micro‐CT scans. These data were complemented by scanning electron microscopy, to analyse the surface structures in detail. There is evidence that the various elements of the mouthparts of L. maja can be sorted into six functional groups: (i) transporting mouthpart elements, (ii) aligning/sorting mouthpart elements, (iii) clutching/holding mouthpart elements, (iv) tearing/cutting/crushing mouthpart elements, (v) current‐generating mouthpart elements and (vi) grooming mouthpart elements. According to our 3D reconstruction, there only seem to be minor differences in morphology and relative position between the mouthparts of L. maja and those of the closely related species, Pagurus bernhardus.     

Striking convergence in the mouthpart evolution of stream-living algae grazers

This scanning-electron microscopic study demonstrates the convergent evolution of the mouthparts of various herbivorous stream animals (insects from different orders, an isopod, snails, fish, and a tadpole) feeding on epilithic algal pastures. This food source is rich but is often difficult to harvest. Nevertheless, a large number of species can live on it because they have evolved highly specialized mouthparts. There are four functional problems that an algae grazer has to solve: the algae must be removed from the stone, they have to be collected and crushed, and a current shield is needed to prevent the water flow sweeping away the food. Among the 30 algae grazers examined in this study, a limited number of morphological solutions have been found for each of these adaptational problems. There are multiple evolutionary pathways for mouthpart adaptation and even closely related species have often evolved different types of tools for the same function. This refects the existence of a certain amount of evolutionary scope. Such freedom of evolution is present, however, only at the beginning of the adaptiogenesis of an algae grazer. Once one of the evolutionary pathways is taken, further improvement of the mouthparts is possible only by the refinement of the ‘chosen’ type of tools. The consequence of this is that a large number of astonishing convergences have occurred in algae grazers that have independently trodden the same evolutionary pathway.     

RNAi analysis of Deformed, proboscipedia and Sex combs reduced in the milkweed bug Oncopeltus fasciatus: novel roles for Hox genes in the hemipteran head

Insects have evolved a large variety of specialized feeding strategies, with a corresponding variability in mouthpart morphology. We have, however, little understanding of the developmental mechanisms that underlie this diversity. Until recently it was difficult to perform any analysis of gene function outside of the genetic model insects Drosophila melanogaster and Tribolium castaneum. In this paper, we report the use of dsRNA-mediated interference (RNAi) to dissect gene function in the development of the milkweed bug Oncopeltus fasciatus, which has specialized suctorial mouthparts. The Hox genes Deformed (Dfd), proboscipedia (pb) and Sex combs reduced (Scr) have previously been shown to be expressed in the gnathal appendages of this species. Strikingly, the milkweed bug was found to have an unusual expression pattern of pb. Here, by analyzing single and combination RNAi depletions, we find that Dfd, pb and Scr are used in the milkweed bug to specify the identity of the mouthparts. The exact roles of the genes, however, are different from what is known in the two genetic model insects. The maxillary appendages in the bug are determined by the activities of the genes Dfd and Scr, rather than Dfd and pb as in the fly and beetle. The mandibular appendages are specified by Dfd, but their unique morphology in Oncopeltus suggests that Dfd's target genes are different. As in flies and beetles, the labium is specified by the combined activities of pb and Scr, but again, the function of pb appears to be different. Additionally, the regulatory control of pb by the other two genes seems to be different in the bug than in either of the other species. These novelties in Hox function, expression pattern and regulatory relationships may have been important for the evolution of the unique Hemipteran head.     

Hunting and predation in a fiddler crab

Fiddler crabs are known primarily to be deposit feeders. They eat detritus, bacteria, and other small particles of organic material found in the sandy or muddy substrate on which they live. They have highly specialized mouthparts used to separate edible matter from nondigestable material. Here we provide evidence of cannibalism and predation in a fiddler crab, Uca annulipes. We additionally provide the first evidence of a fiddler crab hunting shrimp and insects. This study is an exemplary reminder that, even though an animal may have evolved highly specialized feeding traits, this need not preclude it from opportunistically acting as a generalist feeder.     

Les pieces buccales et leurs recepteurs sensoriels chez l'imago de Micropterix calthella L. (Lepidoptera : Micropterigidae)

The aim of our study is to describe the mouthparts of Micropterix calthella (Lepidoptera) and their sensilla by the scanning electron microscope (SEM). The imaginal mouthparts are primitive. They are well adapted for collecting and grinding pollen of Ranunculus flowers. The maxillary palps show specialized structures for collecting pollen: mushroom-shaped hairs and blade-like structures. The brushes on the epipharynx, the teeth on the mandibles and the triturating basket on the hypopharynx grind the pollen to powder before absorption.Sensilla of different types have been observed on the mouthparts. The labrum, galeae, laciniae, and labial palps possess sensilla chaetica. Epipharynx, galeae, laciniae, and hypopharynx show sensilla basiconica. Sensilla trichoidea have been observed on the laciniae and sensilla campaniformia on the maxillary palps and the hypopharynx. At the top of each maxillary palp is a perforated area of unknown function. Two cavities are present at the distal extremity of each labial palp: one with sensilla coeloconica and the other with a perforated heart-shaped organ. The mushroom-shaped hairs, the blade-like structures, and the perforated heart-shaped organs have not yet been described in other insects.     

The morphology of mouthparts,wings and genitalia of Paleozoic insect families Protohymenidae and Scytohymenidae reveals new details and supposed function

Megasecoptera is an extinct group of insects with specialized rostrum-like mouthparts, which is a synapomorphy shared with all members of the Late Paleozoic Palaeodictyopterida, and markedly slender wings that are unable to flex backwards. Here we describe the close up morphology of Protohymenidae and Scytohymenidae and uncover new aspects of the endoskeleton (tentorium) of the head, structure of the mouthparts with discernible proximal part of stylets controlled by muscles, surface of compound eyes that consist of a hexagonal pattern of large facets, structure and microstructures on the wings and reconstruct male and female external genitalia using ESEM and light stereomicroscopy. Furthermore, we describe Protohymen novokshonovi sp. n. based on an exceptionally well preserved fossil from the early Permian at Tshekarda in Russia, which shows crucial details, and the earliest species of Protohymenidae, Carbohymen testai gen. et sp. n. from a late Carboniferous siderite nodule at Mazon Creek in Illinois, USA. Our comparative study confirmed a set of structural and microstructural details on their wings, such as the composite anterior wing margin, development of an apical cell and the previously unknown external genitalia. Based on the results and comparison of homologous structures known primarily for extant relatives, such as mayflies and dragonflies, we outline for the first time the function of the mouthparts, in particular, the stylets, structure of the tentorium, vision provided by large hexagonal ommatidia and male copulatory structures bearing curved claspers for holding a female during copulation and penial lobes with seminal grooves.     

Observations on mouthparts of Dermatobia hominis (Linneaus Jr., 1781) (Diptera: Cuterebridae) by scanning electron microscopy

The ultrastructure of the mouthparts of Dermatobia hominis was studied using scanning electron microscopy. The morphological characteristics of the segments, articulations, sensory organs, and pilose covering are described. Mechanoreceptors of the long trichoid sensillum and smaller trichoid sensillum types were observed, as well as labellar gustatory receptors of the basiconic sensillum type, which differed between the sexes. These observations are discussed with reference to the current literature on the morphology and sense organs of dipteran mouthparts, and the prevailing view that the adult mouthparts of this species are non-functional is challenged.     

Comparative morphology and evolutionary pathways of the mouthparts in spore-feeding Staphylinoidea (Coleoptera)

This study surveys the external morphology of the mouthparts in the guild of spore‐feeders among the coleopterous superfamily Staphylinoidea, evaluating the influence of different phylogenetic and ecological starting points on the formation of their mouthparts. Our emphasis is on a scanning electron microscope analysis (SEM) of the involved trophic structures in spore‐feeding larvae and adults of the Ptiliidae, Leiodidae and Staphylinidae, describing the fine structure of their main functional elements. Functionally, mouthpart structures resemble brushes, brooms, combs, rakes, rasps, excavators, knives, thorns, cram‐brushes, bristle troughs, blocks and differently structured grinding surfaces. Their different involvement in the various aspects of the feeding process (i.e. food gathering, transporting, channelling and grinding) is deduced from our SEM analyses plus direct video observations. We infer five different patterns of food transport and processing, discriminating adults of ptiliids, leiodids plus staphylinids (excluding some aleocharines), several aleocharine staphylinids, and the larvae of leiodids and staphylinids. The structural diversity of the mouthparts increases in the order from (1) Ptiliidae, (2) Leiodidae towards (3) Staphylinidae, reflecting the increasing systematic and ecological diversity of these groups. Comparisons with non‐spore‐feeders show that among major lineages of staphylinoids, shifts from general microphagy to sporophagy are not necessarily constrained by, nor strongly reflected in, mouthpart morphology. Nevertheless, in several of these lineages the organs of food intake and grinding have experienced particular fine‐structural modifications, which have undergone convergent evolution, probably in response to specialized mycophagy such as spore‐feeding. These modifications involve advanced galeal rakes, galeal or lacinial ‘spore brushes’ with arrays of stout bristles, reinforced obliquely ventrad orientated prosthecal lobes and the differentiations of the molar grinding surfaces into stout teeth or tubercles. In addition, several staphylinids of the tachyporine and oxyteline groups with reduced mandibular molae have evolved secondary trituration surfaces, which in some aleocharines are paralleled by considerable re‐constructions of the labium–hypopharynx.     

Bimodal Pollination by Wasps and Beetles in the African Milkweed Xysmalobium undulatum

It has been suggested that flowers of some plants are specialized for pollination by two unrelated species (or functional groups) of pollinators. However, evidence for 'bimodal pollination systems' has been extremely limited. Studies of the milkweed Xysmalobium undulatum in South Africa showed that its flowers are visited by a range of different insects (representing 18 families), but only two groups, represented by the chafer beetle Atrichelaphinis tigrina and pompilid wasps in the genus Hemipepsis , effect pollination. Experiments showed that both these pollinator groups are effective in removing and inserting pollinia. Pollinia are attached to clypeal hairs and mouthparts on the wasps and tarsal hairs and spines on the beetles. Although considerably less abundant than the beetles, Hemipepsis spp. wasps move more quickly among flowers and appeared to be more effective pollinators overall. Experimental hand-pollinations conducted in the field showed that X. undulatum is genetically self-incompatible and thus completely reliant on pollinators for reproduction. We conclude that X. undulatum has a bimodal pollination system, specialized for pollination by Hemipepsis pompilid wasps and the chafer beetle A. tigrina .     

The development and evolution of insect mouthparts as revealed by the expression patterns of gnathocephalic genes

To understand better both the development and evolution of insect mouthparts, we have compared the expression pattern of several developmentally important genes in insects with either mandibulate or stylate-haustellate mouthparts. Specifically, we examined the expression of the proboscipedia (pb) and Distal-less (Dll) gene products as well as three regulators of pb, Sex combs reduced (Scr), Deformed (Dfd), and cap 'n' collar (cnc). These genes are known to control the identity of cells in the gnathal segments of Drosophila melanogaster and would appear to have similar conserved functions in other insects. Together we have made an atlas of gene expression in the heads of three insects: Thermobia domestica and Acheta domestica, which likely exemplify the mandibulate mouthparts present in the common insect ancestor, and Oncopeltus fasciatus, which has piercing-sucking mouth parts that are typical of the Hemiptera. At the earliest stages of embryogenesis, only the expression of pb was found to differ dramatically between Oncopeltus and the other insects examined, although significant differences were observed later in development. This difference in pb expression reflects an apparent divergence in the specification of gnathal identity between mandibulate and stylate-haustellate mouthparts, which may result from a "phylogenetic homeosis" that occurred during the evolution of the Hemiptera.     

Specialization for pollination by beetles and wasps: the role of lollipop hairs and fragrance in Satyrium microrrhynchum (Orchidaceae)

Exposed nectar presentation is a key trait in flowers specialized for pollination by short-tongued insects. We investigated the pollination of Satyrium microrrhynchum, a rare South African orchid in which nectar is secreted as droplets on long floral hairs ("lollipop hairs") at the mouth of a shallow labellum. Our observations indicate that this orchid is pollinated specifically by two insect species: a cetoniid beetle (Atrichelaphinus tigrina) and a pompilid wasp (Hemipepsis hilaris). Both insects have short mouthparts and remove nectar from the hairs with sweeping motions of their mouthparts. Pollinaria become attached to the upper surface of their heads while they feed on the nectar. Beetles damage the hairs while feeding, which may explain the positive relationship between hair damage and pollination success in plants of S. microrrhynchum from populations where beetles were common. The orchid has cryptic green-yellow flowers with spectral reflectance similar to that of its leaves. The fragrance from plants in three populations, analyzed using gas chromatography coupled to mass spectrometry, was dominated by various terpenoids; linalool was the most abundant. Plants in different populations emitted similar compounds, but eugenol and derivatives of this compound were found in only one of the three populations. In an electrophysiological study (gas chromatography coupled to electroantennography), using antennae of A. tigrina, clear signals were elicited by some of the floral scent compounds.     

Morphology of the head of <Emphasis Type="Italic">Sericoderus lateralis</Emphasis> (Coleoptera,Corylophidae) with comments on the effects of miniaturization

The mouthparts and musculature of the head of Sericoderus lateralis are described. It is shown that the mouthparts of minute beetles preserve their complex structure and are not significantly affected by miniaturization. Such stability allows these features to be used in macrosystematics of groups with variable body size.