Groundplan Anatomy of the Proboscis of Butterflies (Papilionoidea, Lepidoptera)

The anatomy of the proboscis was studied in representatives of all major subfamilies of Papilionoidea and several outgroup taxa which included Hesperiidae, Hedylidae and Geometroidea. In all species the cross-sectional outline of the tapering proboscis continuously changes from proximal to the tip while the central food canal, formed by the concave medial galeal walls, retains its oval shape. Each galea contains three types of muscles, a branching trachea, nerves, sensilla, and at least one longitudinal septum. We focused on the varying arrangement and distribution of the intrinsic galeal muscles from the basal galeal joint to the tip region. The plesiomorphic condition of the galeal composition of Papilionoidea is regarded to include one basal intrinsic muscle in the basal joint region and two series of intrinsic muscles, i.e. the lateral intrinsic galeal muscles and the median intrinsic galeal muscles, both series extending from the proximal region to the tip region. The plesiomorphic arrangements of the intrinsic muscle series are found in all representatives of Papilionidae, in one species of Lycaenidae (sensu lato), in many Nymphalidae (sensu lato), and in all outgroup species. Three apomorphic character states are distinguished regarding the presence and extension of the median intrinsic galeal muscles. (1) Present up to 35% of the proboscis length and absent distally in Pieridae, Lycaeninae (Lycaenidae), Satyrinae (Nymphalidae), and Danainae (Nymphalidae). (2) Present in the proximal third of the proboscis and again near the tip between 80 and 90% of the proboscis length in the examined Heliconiinae (Nymphalidae). (3) Completely absent, as in one lycaenid species from the subfamily Riodininae.     

Functional morphology of the feeding apparatus and evolution of proboscis length in metalmark butterflies (Lepidoptera: Riodinidae)

An assessment of the anatomical costs of extremely long proboscid mouthparts can contribute to the understanding of the evolution of form and function in the context of insect feeding behaviour. An integrative analysis of expenses relating to an exceptionally long proboscis in butterflies includes all organs involved in fluid feeding, such as the proboscis plus its musculature, sensilla, and food canal, as well as organs for proboscis movements and the suction pump for fluid uptake. In the present study, we report a morphometric comparison of derived long‐tongued (proboscis approximately twice as long as the body) and short‐tongued Riodinidae (proboscis half as long as the body), which reveals the non‐linear scaling relationships of an extremely long proboscis. We found no elongation of the tip region, low numbers of proboscis sensilla, short sensilla styloconica, and no increase of galeal musculature in relation to galeal volume, but a larger food canal, as well as larger head musculature in relation to the head capsule. The results indicate the relatively low extra expense on the proboscis musculature and sensilla equipment but significant anatomical costs, such as reinforced haemolymph and suction pump musculature, as well as thick cuticular proboscis walls, which are functionally related to feeding performance in species possessing an extremely long proboscis. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 291–304.     

Vergleichende Morphologie des Schmetterlingsrüssels und seiner Sensillen — Ein Beitrag zur phylogenetischen Systematik der Papilionoidea (Insecta, Lepidoptera)

Comparative morphology of the butterfly proboscis and its sensilla — a contribution to the phylogenetic systematics of Papilionoidea (Insecta, Lepidoptera) The morphology of the proboscis was investigated in more than 70 European representatives of Papilionoidea using light microscopy and scanning electron microscopy. The composition of the proboscis wall, its surface structures, as well as the shape and distribution of the different types of sensilla are compared. Special attention is given to the tip region and the diversity of the sensilla styloconica. Plesiomorphic features of the proboscis of Papilionoidea were found to include vertically extended exocuticular ribs composing the galeal wall, cuticular spines restricted to the ventral side of the proximal galea, and two rows of fluted sensilla styloconica restricted to the tip region. Apomorphic features of the proboscis in Papilionidae are three rows of small sensilla styloconica. The presence of cuticular spines all over the galeae was identified as an autapomorphy of Pieridae. Possible apomorphies of Nymphalidae are oblique exocuticular ribs of the galeal wall and the great number and length of the sensilla styloconica (significant at p < 0.01, t-test). A possible synapomorphy of Lycaenidae and Riodinidae are cuticlar spines up to the distal galeae. Distinct transformation series of sensilla styloconica give evidence that divergent evolutionary trends led from fluted shafts to a multitude of other shapes in Papilionidae, Nymphalidae (sensu lato), and Lycaenidae. Long smooth-shafted, club-shaped sensilla styloconica, bearing apical spines, are found in Nymphalinae, Apaturinae and Limenitidinae. Highly derived sensilla styloconica evolved in Heliconiinae and Melitaeini, which are arranged in only one row in both taxa. Their shafts are smooth, flattened and bear an excentral sensory cone. Further apomorphic character states are dented flutes which evolved several times, independently from each other in Satyrinae, Lycaeninae and Riodinidae. The results are discussed in a systematical context and provide the basis for a better understanding of the function of different morphological structures of the proboscis in feeding.     

Functional morphology and movements of the proboscis of Lepidoptera (Insecta)

Summary The mouthparts of Lepidoptera were investigated in a number of species by morphological and cinematographical methods. Both the galeae (which compose the proboscis) and the basal maxillary components (stipites) were studied in the resting position, in motion, and during feeding. In the resting position the proboscis is coiled so tightly that the surfaces of the consecutive coils are in close contact and the outermost coil touches the ventral side of the head. Cuticular processes of the galeal wall interlock between the coils in this position. In the investigated species they occur on the galeal wall and on the ventral side of the head in varying number and distribution. By the extension of the basal galeal joint, the coiled proboscis is released from its resting position and is elevated continuously. It uncoils in 3–5 steps which effect the entire length simultaneously. Each uncoiling step occurs synchronously with a compression of the stipital tubes on either side of the body. These compression movements pump hemolymph into the galeae. In all investigated Lepidoptera the uncoiled proboscis shows a distinct downward bend at a certain point which is also detectable in anaesthetized or freshly killed animals in some species. This feeding position and the movements of the uncoiled proboscis are similar in all species despite the intrinsic galeal muscles being variously arranged in the galeal lumen in different Lepidoptera. When comparing cross-sections through corresponding regions of coiled and uncoiled proboscises, the curvatures of the dorsal galeal walls remain unchanged. Coiling of the proboscis starts at the tip and progresses to the base. After coiling the proboscis tightly beneath the head, the diameter of the spiral widens due to its elastic properties until the proboscis props itself against the ventral side of the head. This elastic effect combined with the interlocking cuticular processes seems to be responsible for the resting position of the proboscis.Abbreviations an antenna - bre bend region - ca cardo - ci cibarium - cl clypeus - co complex eye - cp cuticular process - dre distal region - esm external tentoriostipital muscle - fc food canal - fst flat part of the stipes - ga galea - hs horizontal septum - igm intrinsic galeal muscles - ism internal tentoriostipital muscle - la labium - lap labial palpus - lr labrum - mxp maxillary palpus - ne nerve - pi pilifer - pom primary oblique galeal muscles - pr proboscis - pre proximal region - sa salivarium - se sensillum - som secondary oblique galeal muscles - st stipes - stl stipital lamella - te tentorium - tr trachea - tst tubular part of the stipes - vm ventral membrane - vs vertical septum     

A comparative survey of proboscis morphology and associated structures in fruit-piercing, tear-feeding, and blood-feeding moths in Calpinae (Lepidoptera: Erebidae)

Functional feeding categories for adult species of Calpinae are described. Structures associated with the proboscis were examined using exemplar species in fruit-piercing, blood-feeding, and tear-feeding species using both light microscopy and SEM methods. At least three genera currently placed in Calpini, and several others in related groups lack specialized piercing structures. The proboscis of the tear-feeding species, Hemiceratoides hieroglyphica, is equipped with specialized cuticular hooks not yet observed in other tear-feeding species. Tearing hooks moveable by blood pressure are restricted to Calpini species, and little additional variation within this taxon exists, suggesting proboscis morphology may not be strongly correlated with feeding behavior (e.g., fruit piercing vs. blood feeding). A glossary of terms and character codings for proboscis structures is provided, and morphologies for all included calpine taxa are described. We discuss the taxonomic significance of proboscis morphology in Calpinae and the evolutionary implications of their associated feeding behaviors. This survey indicates morphology provides powerful prediction, but not proof of lepidopteran adult food habits.     

Moth pollination of Metaplexis japonica (Apocynaceae): pollinaria transfer on the tip of the proboscis

Asclepiad pollinaria (including pollen masses) attach to diverse body parts of flower visitors in many ways. In this paper, we observed nocturnal moths (Lepidoptera: Pyralidae and Noctuidae) transporting the pollinaria of the Japanese species Metaplexis japonica (Thunb.) Makino (Apocynaceae: Asclepiadoideae) on the tip of the proboscis. Flowers of this species may induce nectar-feeding moths to pull out the proboscis along a guide rail (anther slit), thus clipping the pollinaria onto the tip of the proboscis and transferring the pollinaria to the next flower. The transfer of pollinaria on the unique vector of a moth proboscis tip is an interesting pollination mechanism among previously reported entomophiles.     

Proboscis musculature in the butterfly Vanessa cardui (Nymphalidae, Lepidoptera): settling the proboscis recoiling controversy

Krenn, H. W. 2000. Proboscis musculature in the butterfly Vanessa cardui (Nymphalidae, Lepidoptera): settling the proboscis recoiling controversy. —Acta Zoologica (Stockholm) 81 : 259–266 The proboscis of Vanessa cardui (Nymphalidae) contains two basal galeal muscles and two different series of numerous oblique muscles. Both muscle series extend from the proximal region up to the tip‐region; the individual muscles of each series run a constant course throughout the proboscis. In contrast to other butterflies, the knee bend region does not have additional types of muscles. The analysis of shock‐frozen proboscises reveals that the dorsal wall is arched outwardly in the uncoiled, feeding position whereas in the coiled, resting position the dorsal proboscis wall is flat or concave. This results in a significantly greater cross‐sectional area due to the significantly greater dorso‐ventral diameter in uncoiled proboscises. After freezing the proboscis in its distal region, it can still be uncoiled, however, it cannot be fully recoiled. These morphometric and experimental results indicate that the oblique proboscis muscles are responsible for recoiling the proboscis to the resting position.     

柑桔吸果夜蛾的头部内骨骼、肌肉系统和口器构造与成虫取食习性的关系

吸果夜蛾的取食习性与头部内骨骼、肌肉和口器构造的特点有如下的关系:1.嗜食健果类型:幕骨强大,为着生肌肉提供较大的面积。头部肌肉发达。口器强角质化,端部具有适于穿刺果皮的附属物。2.兼食性类型:幕骨强大,头部肌肉发达程度常界于第一和第三类型之间。口器端部锐利,角质比较强。3.间接取食类型:幕骨不发达,着生肌肉的面积较小。头部肌肉较纤细。口器端部钝或膜质状,角质化程度弱。此外,下颚茎节外形及颊宽的特征,可以将嗜食健果类型的夜蛾与其他两类型的夜蛾区分开来。     

Structure of the lepidopteran proboscis in relation to feeding guild

Most butterflies and moths (Lepidoptera) use modified mouthparts, the proboscis, to acquire fluids. We quantified the proboscis architecture of five butterfly species in three families to test the hypothesis that proboscis structure relates to feeding guild. We used scanning electron microscopy to elucidate the fine structure of the proboscis of both sexes and to quantify dimensions, cuticular patterns, and the shapes and sizes of sensilla and dorsal legulae. Sexual dimorphism was not detected in the proboscis structure of any species. A hierarchical clustering analysis of overall proboscis architecture reflected lepidopteran phylogeny, but did not produce a distinct group of flower visitors or of puddle visitors within the flower visitors. Specific characters of the proboscis, nonetheless, can indicate flower and nonflower visitors, such as the configuration of sensilla styloconica, width of the lower branches of dorsal legulae, presence or absence of dorsal legulae at the extreme apex, and degree of proboscis tapering. We suggest that the overall proboscis architecture of Lepidoptera reflects a universal structural organization that promotes fluid uptake from droplets and films. On top of this fundamental structural organization, we suggest that the diversity of floral structure has selected for structural adaptations that facilitate entry of the proboscis into floral tubes. J. Morphol. 277:167–182, 2016. © 2015 Wiley Periodicals, Inc.     

Proboscis sensilla in Vanessa cardui (Nymphalidae, Lepidoptera): functional morphology and significance in flower-probing

 Morphology and distribution of the proboscis sensilla in Vanessa cardui have been investigated in order to contribute to the understanding of flower-probing behaviour in butterflies. The proboscis has a bend region approximately one-third of the length from the base. A short tip region is characterized by rows of intake slits leading into the food canal. Along the dorsal, lateral and ventral sides of the proboscis, sensilla trichodea, sensilla basiconica and sensilla styloconica are distributed in varying patterns depending on their distance from the b ase. The medial food canal bears one longitudinal row of sensilla basiconica only. The bristle-shaped sensilla trichodea are longer in the proximal region of the proboscis and become gradually shorter towards the tip. They are most frequent in number near to the bend region and near the beginning of the tip region. Sensilla basiconica arranged in longitudinal rows increase in number the more distal they are on the proboscis. The tip region is characterized by rows of sensilla styloconica on the dorsal side whereas the sensilla trichodea are mostly restricted to the ventral side. The ultrastructure suggests that the aporous sensilla trichodea function as mechanosensilla while the uniporous sensilla basiconica act as contact chemosensilla. The sensilla styloconica are regarded as bimodal contact chemo/mechanosensilla since their sensory cones are equipped with a single terminal pore and a tubular body at the base. The mouthpart sensilla appear to provide tactile cues on the positioning of the proboscis and on the degree of its insertion into a floral tube. Furthermore, they receive chemical stimuli on the availability of nectar and on the immersion status of the food canal. Accepted: 12 September 1997     

Mouthparts of heliconius butterflies (LEPIDOPTERA : NYMPHALIDAE) : a search for anatomical adaptations to pollen-feeding behavior

Proboscis length, the length of the tip, the number and length of the various sensilla throughout the proboscis, and the size and shape of the labial palpi were compared in 25 species of pollen-feeding and non-pollen-feeding Heliconiinae (Lepidoptera, Nymphalidae). The mouthparts of pollen-feeding species (all belonging to the genera Heliconius and Laparus) do not have structures exclusive to them. However, in comparison with non-pollen-feeding Heliconiiti, the pollen-feeding species have a significantly longer proboscis without elongation of the tip-region ; the bristle-shaped sensilla trichodea were found to be significantly more numerous and longer on the proximal and mid-region of the proboscis, while the sensilla of the tip-region are significantly shorter. In addition to these proboscis features, the labial palpi were shorter in the pollen-feeding species, which is likewise possibly associated with pollen-feeding behavior. The biological role of these features is discussed and the evolution of this unique feeding behavior among Lepidoptera is considered in the context of the phylogenetic relationships among genera of Heliconiini.     

Morphology and function of the proboscis in Bombyliidae (Diptera, Brachycera) and implications for proboscis evolution in Brachycera

Based on serial semithin sections and SEM photographs of representatives of European Bombyliinae and Anthracinae, the mouthparts of Bombyliidae are studied and compared with the relevant data from literature on other families of Diptera Brachycera. The three moving units of the proboscis (clypeo-cibarial region, haustellum-maxillary base region, and labella) and their structures and muscles are described. Functions and possible movements are inferred from the structures observed. Articulations both between the parts of the organ and to the head capsule enable the fly to retract its proboscis into a resting position. Proboscis movement from a resting to a feeding position encompasses the following submovements: rotating of the basal clypeo-cibarial region (= fulcrum) against the head capsule, folding of the haustellum-maxillary base region against the fulcrum, evagination and invagination of the labial base, and the labella movements. This is a novelty as compared to the rigid proboscis of Tabanidae and agrees largely with the conditions in the Cyclorrhapha. The evolution of these novelties and their functional significance are discussed. The fulcrum, as well as the haustellum-maxillary base, as the new moving units are deduced from the plesiomorphic state as present in Tabanidae by fusions of sclerites, shifts of musculature and formation of new articulations. Accepted: 5 April 2000     

Contribution of the maxillary muscles to proboscis movement in hawkmoths (Lepidoptera: Sphingidae)--an electrophysiological study

The role of the maxillary muscles in the uncoiling and coiling movements of hawkmoths (Sphingidae) has been examined by electromyogram recordings, combined with video analysis. The maxillary muscles of adult Lepidoptera can be divided into two groups, galeal and stipital muscles. The galea contains two basal muscles and two series of oblique longitudinal muscles, which run through the entire length of the galea. Three muscles insert on the stipes, taking their origin on the tentorium and on parts of the cranium and gena, respectively. Proboscis extension is initiated by an elevation of the galea base caused by the basal galeal muscles. The actual uncoiling of the proboscis spiral is accompanied by rapid compressions of the stipites which are caused by two of the stipital muscles. The study provides strong support for the hypothesis that uncoiling is brought about by an increase of hemolymph pressure by the stipites forcing hemolymph into the galeae. Recoiling is caused by the contraction of both sets of oblique longitudinal galeal muscles supported by elasticity of the galea cuticle. Finally, the remaining stipital muscle pulls down the galea base which brings the coiled proboscis back to its resting position where it is held in the U-shaped groove of the labium without further muscle activity.     

Morphology of the pretarsus of the sawflies and horntails (Hymenoptera: 'Symphyta')

The pretarsal structures have been studied in representatives of 13 families of 'Symphyta' by means of light microscopy. The pretarsal sclerites (manubrium, planta, and unguitractor) vary in shape among different families. The shape of the manubrium is triangular in representatives of Xyelidae and Orussidae and bifurcated in those of Tenthredinoidea. For representatives of Siricomorpha, an elongated shape of the manubrium is typical with such variations, as distally expanded, proximally expanded, clavate, spear-shaped. Plantae of different Symphyta vary in shape and level of sclerotization. In representatives of Siricidae, the female manubrium and arolium are significantly reduced, and arcus and dorsal plates are completely absent. Siricid males possess all pretarsal sclerites and a well-developed arolium. Auxiliary sclerites are absent in representatives of Orussidae. Trichoid sensilla are absent on the plantae in representatives of Cephidae and Orussidae. Other studied Symphyta possess two trichoid sensilla on the planta. Representatives of all investigated families bear two campaniform sensilla on the manubrium, with the exception of Siricidae having three sensilla. Kinematics of the pretarsus with bifurcated manubrium are modeled and discussed.     

三种夜蛾成虫口器感器的超微形态

为确定不同种类夜蛾口器及其感器在超微结构上的差异, 采用扫描电子显微镜对棉铃虫Helicoverpa armigera (Hübner)、 烟夜蛾H. assulta (Guenée)和银纹夜蛾Argyrogramma agnata (Staudinger)3种鳞翅目(Lepidoptera)夜蛾科(Noctuidae)重要农业害虫雌、 雄成虫口器感器的超微形态进行了观察和比较。结果表明： 3种夜蛾雌、 雄成虫口器感器类型均无明显差异。棉铃虫和烟夜蛾口器感器在类型和形状上十分类似, 均具有毛形、 锥形和栓锥形感器; 喙管末端的栓锥感器粗、 密, 棱纹明显。银纹夜蛾口器感器与两种铃夜蛾区别明显, 除上述3类感器外, 还具有腔锥形感器; 其喙管末端的栓锥感器细、 疏, 棱纹不明显。结果显示口器感器可用于夜蛾的分类及亲缘关系研究。     

Morphology of sensory papillae on the feeding proboscis of cone snails (Mollusca,Gastropoda)

Cone snails, predatory marine gastropods, have developed a specialized prey capture method in which a long, distensible proboscis is used to identify prey and inject venom via a hydraulically propelled hollow radular tooth. Using brightfield, epifluorescence, confocal, and transmission and scanning electron microscopy, we describe the morphology of ciliated sensory structures concentrated on the tip of the proboscis. The number and morphology of these sensory papillae are linked to the type of preferred prey: cone snails feeding on worms and mollusks have short, cone or finger‐shaped papillae, whereas fish‐hunting cone snails have long tubular papillae in addition to short conical papillae. Sensory papillae are well positioned to provide information necessary to locate, identify, and dispatch prey. Proboscis tips and their sensory papillae regenerated within 10 d following experimental ablation, and snails with regenerated proboscis tips were able to locate and envenomate prey. The remarkable intrageneric variation found in the morphology of these sensory structures is probably linked to the specialized prey that cone snail species have evolved to hunt.     

The anatomy and ultrastructure of the suctorial organ of Solifugae (Arachnida)

Solifugae possess an evertable, adhesive pedipalpal organ (suctorial organ) at the tip of the distal tarsus of each pedipalp that is unique among arachnids. When inverted inside the pedipalp, the suctorial organ is covered with two cuticular lips, a dorsal upper lip and a ventral lower lip, but it can be protruded rapidly in order to facilitate grasping prey or climbing on bushes or even climbing on smooth surfaces due to its remarkable adhesive properties. In this study, the suctorial organs of different species from old world families Galeodidae and Karschiidae and new world families Ammotrechidae and Eremobatidae were investigated by means of light microscopy, scanning and transmission electron microscopy. In all representatives, the suctorial organ is formed by an evertable, cuticular pad with a complex internal stabilizing structure. The procuticle of this pad consists of a lattice-like basal plate and numerous stalked structures connected to this basal plate. The shafts of the stalked structures are regularly organized and ramify apically. The surface of the suctorial organ is constituted of a very thin epicuticle overlaying the ramifying apices forming ridges and furrows on the ventral side of the suctorial organ.     

Proboscis sensilla of the black cutworm Agrotis ypsilon (Rottemberg) (Lepidoptera: Noctuidae)

Proboscis sensilla are important for feeding biology in Lepidoptera, and are also valuable characters for species recognition and phylogenetic analysis. However, proboscis has not been satisfactorily explored in many groups in Lepidoptera so far. Here we examined the proboscis sensilla of the black cutworm Agrotis ypsilon (Rottemberg), a cosmopolitan agricultural pest of great economic significance, using scanning electron microscopy. Three types of sensilla were found on the proboscis: sensilla chaetica, sensilla basiconica, and sensilla styloconica. Sensilla chaetica occur only on the external surface of the proboscis and become shorter and more scattered toward the tip. Sensilla basiconica are arranged in longitudinal rows on the external proboscis and one longitudinal row in the inner food canal. Sensilla styloconica are the most characteristic sensilla on the proboscis, consisting of a single sensory cone inserted at the top of a stylus with six or seven longitudinal ribs, and are concentrated on the tip region, and are much longer and more numerous in females than in males. The role of proboscis sensilla in the feeding habit prediction is briefly discussed.     

Morphological fine tuning of the feeding apparatus to proboscis length in Hesperiidae (Lepidoptera)

The form and function of the hesperiid feeding apparatus was studied in detail. The butterflies in the family Hesperiidae are of particular interest because the longest proboscis ever recorded in Papilionoidea was found in the Neotropical genus Damas. We focused on the functional morphology by comparing proboscis morphology as well as size and composition of both the stipes pump and the cibarial suction pump in skippers with short and extremely long proboscis. Results revealed that all studied Hesperiidae have the same proboscis micromorphology and sensilla endowment regardless of the proboscis length. However, the numbers of internal muscles of the proboscis, the morphology of the stipes pump as well as the pumping organs for nectar uptake are related to the proboscis length. We conclude that the low number of tip sensilla compared to proboscis length is responsible for remarkably longer manipulation times of long‐proboscid species during flower visits. The organs for proboscis movements and nectar uptake organs are well tuned to the respective proboscis length and are accordingly bigger in species with a proboscis that measures twice the body length.     

Adhesion and Suction Functions of the Tip Region of a Nectar-drinking Butterfly Proboscis

In this study,we investigated the dynamic functions of the tip region of the butterfly proboscis through which liquid is sucked during liquid feeding.The microstructures and flow patterns in the tip region of the proboscis were in vivo analyzed.The tip region can be divided into two functional sections:namely adhesion and suction sections.The liquid adheres to the adhesion section during liquid suction.Although the tip region has numerous slits connected to food canal of the proboscis,liquid is mainly sucked through the suction section,which section is submerged in the fluid pulled by the adhesion section and then successfully imbibes liquid.To check the dynamic functions of the tip region,we fabricated a suction tip model having adhesion and suction parts.The in vitro model experiments show that the hydrophilicity of the adhesion part and the existence of the suction inlet improve the liquid uptake driven by a suction pump.This study may provide insights for the biomimetic design of nectar-feeding butterflies.