Social wasps perform a variety of tasks with their mouthparts. Female workers use them to feed on carbohydrate-rich fluids, to build nests by collecting wood fibers and forming paper, to hunt and manipulate insect prey for feeding larvae as well as for brood care. Since male wasps neither feed on insects nor participate in nest building, sex-specific differences in mouthpart morphology are expected. Despite these different applications, general mouthpart morphology of male and female wasps from the genus Vespula was similar. However, males possessed significantly shorter mandibles with fewer teeth than females. Furthermore, the adductor muscles of the mandibles were distinctly smaller in males than in females. Male wasps showed a higher number of sensilla on the mandibles and the labial palpi. Mouthpart dimorphism and functional morphology of fluid uptake are discussed.

mandible, sensilla, morphology, feeding, social insects, sexual dimorphism

Insect mouthparts are composed of a set of homologous organs that are derived from appendages of head segments adapted to various tasks in context of feeding, defence and nesting. The mouthparts are composed of an unpaired labrum plate in front of the mouth, paired mandibles and paired maxillae as well as an unpaired labium extending from the last head segment (Snodgrass 1935, Seifert 1995). In general, the mandibulate mouthparts of Hymenoptera are characterized by the labio-maxillary complex which is formed by components of the labium and the maxillae (Duncan 1939, Krenn et al. 2005). This unique functional unit of the mouthparts as well as the four-segmented labial palpus are regarded as autapomorphies of the Hymenoptera (Krenn 2007). Adaptations of the labio-maxillary complex for nectar feeding evolved several times independently in many Hymenoptera (Jervis 1998, Jervis and Vilhelmsen 2000). Especially in social wasps, the mouthparts are functionally versatile allowing their use in various kinds of tasks that are reflected by the well-developed biting mandibles and the labio-maxillary complex which is used to take up nectar and other kinds of fluids (Schremmer 1962).

Social wasps collect two main kinds of food. Adult wasps nourish themselves with liquid carbohydrates obtained from honeydew, ripe fruits, flower nectar and sometimes tree sap (Matsuura and Yamane 1990). Female wasps are involved in brood care, nest building and hunting prey, while male wasps do not forage (Schremmer 1962, Spradbery 1973). Females prey mainly on other insects, bite off the wings, legs, and head of the captured prey and convert the remaining parts into a meatball, which is fed to the larvae in the nest (Berland 1928, Schremmer 1962). In addition to supplying themselves and their brood with food, female wasps use their mouthparts for cutting and scraping off plant fibers during nest building, for picking up soil and stones when colonizing underground cavities, as well as for the uptake of water. Hence the mandibles and labio-maxillary complex can be compared to a set of microtools for different kinds of tasks. By contrast, male wasps are not involved in brood care and feed on nectar obtained from flowers with freely accessible nectaries (Schremmer 1962, Matsuura and Yamane 1990).

The mouthparts of some Vespula species were previously examined in detail (Kirmayer 1909, Duncan 1939, Spradbery 1973). They consist of the large biting mandibles and the labio-maxillary complex (Fig. 1). Each maxilla consists of the slender cardo and the flat stipes with the small lacinia, the lateral galea and the 6-segmented maxillary palpus. The labium can be divided into the submentum, forming the lateral connection to the cardines, the roof-shaped mentum and the prementum bearing the 4-segmented labial palpi as well as the median ligula, composed of the united glossae and paired paraglossae (Duncan 1939, Seifert 1995). The labrum (termed as epipharynx in Seifert 1995) is situated under the frontal rim of the clypeus (termed as labrum in Seifert 1995).

Figure 1. 

Head of Vespula germanica (LM). A. Female worker in frontal view; 1, 2, 3 measuments taken to compare head size. B. Male in frontal view. C. Female worker in lateral view. D. Male in ventral view; cl – clypeus, gl – glossa, lp – labial palpus, ma – mandible, mxp – maxillary palpus, pa – paraglossa.

Wasps from the genus Vespula are widely distributed in the Northern hemisphere (Greene 1991, Kimsey and Carpenter 2012). During the last decades, researchers focused mainly on behavioural studies of these social wasps (e.g., Matsuura and Yamane 1990, Mauss 2007). The principle composition of the mouthparts is well studied and was found to be very similar in female workers and queens (Kirmayer 1909, Duncan 1939, Spradbery 1973). However, the mouthparts of male wasps were not studied in detail.

The present study used various morphological methods including scanning electron microscopy and micro CT to investigate the micromorphology of the mouthparts in two species of the genus Vespula. Detailed examination of the cuticle structures including the sensilla allowed conclusions on the functional morphology of the various parts. Special emphasis is laid on the differences between females (workers and queens) and male wasps. Fundamental sex-specific differences in mouthpart morphology can be expected because of characteristic differences in behaviour of each sex.

No differences in head and mouthpart morphology were found between V. vulgaris and V. germanica (Fig. 1). The heads of male wasps were slightly larger (males: 3.23 ± 0.38 mm, N = 9; females: 3.08 ± 0.21 mm, N = 9), but no significant differences between sexes were found (Z = - 0.97, p = 0.33, N = 18). Female workers had significantly longer mandibles than males (males: 1.88 ± 0.11 mm, N = 9; females: 2.07 ± 0.13 mm, N = 9; Z = - 2.87, p = 0.003, N = 18). The distance between the scapus and the distal ridge of the clypeus was similar in males and females (males: 1.85 ± 0.16 mm, N = 9; females: 1.79 ± 0.13 mm, N = 9; Z = - 0.88, p = 0.38, N = 18).

The mouthparts of both sexes in V. vulgaris and V. germanica are characterized by large toothed mandibles and the labio-maxillary complex which is folded posteriorly under the head behind the mandibles (Fig. 1C). The labrum can only be observed when the mandibles are open. The proximal part of the labrum is entirely concealed behind the clypeus; the distal part of the labrum is well equipped with sensilla trichodea (Fig. 2B).

Figure 2. 

Mandibles and labrum (SEM, LM). A. Mandibles (ma) overlapping in repose in front of the clypeus (cl); co – compound eye, gl – glossa. B. Open mandibles (ma), labrum (lr) and glossa (gl) underneath (male wasp). C. Mandible of female (LM), short bristles and mola (mo). D. Mandible of male (LM), long bristles and inconspicuous inner teeth.

The dentate mandibles are heavily sclerotized and shaped like a gouge in both sexes (Fig. 2C, D). The mandibles have sharp distal margins; they are slightly convex on their lateral sides and concave on the medial sides. In repose, one mandible is folded over the other (Fig. 2A). The right mandible folds over the left in 11 (including 5 males) out of 18 wasps, whereas 7 wasps (including 4 males) fold the left mandible over their right one. The cutting edge of the incisive part bears three frontal teeth and a curved proximal cutting edge (Fig. 2C, D). In female workers and queens, two additional teeth and edges with stout bristles are present on the median side of the mandible that is not visible from frontal side (Fig. 2C). In comparison to the incisive part the molar region of the mandible is rather small in females and reduced in male wasps (Fig. 2C, D).

The mandibles bear bristle-shaped sensilla and sensilla campaniformia towards the teeth on the frontal side (Fig. 2). The mandibles of males are almost entirely covered with long sensilla trichodea (Fig. 2B). Their sensory bristles are rough and some are as long as the mandible. Mandibles of female workers show a lower number of sensilla. Their bristles are smooth and shorter, measuring only half of the mandible length (Fig. 2C) in contrast to males (Fig. 2D).

The comparison of the head anatomy in female workers and males showed that the muscles of the mandibles were remarkably smaller in males (Fig. 3). Despite both portions of the adductor of the mandible (Musculus craniomandibularis internus) had the same origin and attachment sites, the volume of both was much smaller in males than in females. Especially the median portion of the adductor muscle was very small in males. The volume of the abductor muscle (Musculus craniomandibularis externus) was slightly smaller in male wasps than in workers (Fig. 3).

Figure 3. 

Head anatomy of a female worker (left) and a male individual (right) of V. germanica (micro CT). Adductor of the mandible (red) is much bigger in females than in males; abductor muscle (blue) is slightly bigger in females; ma – mandible.

The labio-maxillary complex of both sexes is retracted in an oval depression on the posterior part of the head capsule in repose (Fig. 4). The components of this functional unit are firmly connected to ensure that the complex extends and retracts as a unit. In the extended position, the ligula (i.e., glossa plus paraglossae) is longer than the mandibles (Fig. 1B, D). In retracted position, the glossa and paraglossae are folded backwards under the head (Figs 1C, 4A).

Figure 4. 

Labio-maxillary complex (SEM), head in posterior view. A. Maxilla and labium in resting position, ligula (gl – glossa and paraglossa) folded, female worker; c – cardo, lp – labial palpus, m – mentum, mxp – maxillary palpus, prm – prementum, st – stipes. B. Extended ligula, labial palpus (lp) and maxillary palpus (mxp), male; gl – glossa, pa – paraglossa.

The cardo is a roughly triangular sclerite that connects the rest of the labio-maxillary complex with the head. The flat stipes is medially uplifted with the median side next to the labium (Fig. 4A). A few bristle-shaped sensilla are distributed over the lateral surface of the stipes. Lacinia and galea are weakly sclerotized and bear a high number of sensory bristles in both sexes (Fig. 5A). The lacinia is a short lobe positioned medially and covered by the larger flat galea from the lateral and ventral sides. The lacinia shows long bristle-shaped sensilla on the ridge that borders the galea. The galea is subdivided and bears a high number of long bristle-shaped sensilla on the edge and shorter ones over the entire outer surface; sensilla campaniformia occur medially (Fig. 5C).

Figure 5. 

A. Maxilla (LM); c – cardo, ga – galea, l – lacinia, mxp – maxillary palpus, st – stipes. B. Fifth segment of maxillary palpus equipped with various sensilla (SEM); sba – sensillum basiconicum, str – sensillum trichodeum. C. Sensilla at the distal edge of galea (ga) (SEM); arrow indicates terminal pore; sca – sensillum campaniformium, sch – sensillum chaeticum.

All six segments of the maxillary palpus vary with respect to length and distribution of sensory bristles (Fig. 4B). The first two segments are cylindrical in shape and possess a few bristle-shaped sensilla. Segments three to six are club-shaped and have smaller diameters proximally than distally. In comparison to segments one and two, the number of bristle-shaped sensilla increases distinctly in segments three to six including an increasing number of sensilla basiconica (Fig. 5B). The maxillary palpi bear a much higher number of sensilla than the labial palpi, although the types of sensilla are the same (Fig. 4B).

The basal sclerites of the labium are embraced laterally by the well sclerotized two stipites and cardines (Fig. 4A). The mentum is heavily sclerotized and has the shape of a trough, whereas the prementum and the submentum are less sclerotized. The prementum is beset with a small number of bristle-shaped sensilla on the median surface (Fig. 4A). At its distal end the prementum bears the four-lobed ligula composed of the central bilobed glossa as well as the two slimmer and shorter paraglossae laterally on each sides (Figs 1D, 6A). The whole complex of the glossae and paraglossae is folded up behind the mandibles in resting position or extended in the feeding position in males and females (Figs 1B, D; 4). While the ventral cuticle is more or less smooth, the dorsal surface of the glossae and paraglossae is covered with numerous spatula-shaped microtrichia (Fig. 6A–C). Each microtrichium is relatively thin at the base but broadens towards its tip, which is curved backwards and appears hook-shaped (Fig. 6B, C). These spatula-shaped microtrichia are arranged in 25–30 rows and form a large cuticular surface. The microtrichia on the paraglossae are similar but their basis is almost as broad as the tip.

Figure 6. 

Labium (SEM). A. Extended ligula (gl – glossa, pa – paraglossa) in posterior view, acrosomal buttons (ab) at the apex; prm – prementum. B. Apex of glossa (gl), spatula shaped microtrichia (mi) of the dorsal side; pa – paraglossa, sba – sensillum basiconicum. C. Distal edge of the paraglossa with rows of microtrichia (mi) and sensilla basiconica (sba); ab – acrosomal button. D. Third segment of labial palpus (lp), female with thorn-shaped sensillum basiconicum (sba) and sensilla trichodea (str).

Ventrally the glossae and paraglossae each bear an apical brownish cuticular thickening, termed the acroglossal button (Duncan 1939), which has a smooth surface in both sexes (Figs 4B, 5A). On the distal and lateral sides of the acroglossal buttons, a single row of sensilla basiconica is situated (Fig. 6C). In addition, a row of long, flat cuticle structures are present. These microtrichia extend from the edges of the glossae and paraglossae (Fig. 6A–C). The distal rim of the glossae and the tips of the paraglossae bear one row of sensilla basiconica (Fig. 6B). These sensilla basiconica which are positioned close to the acroglossal button have a small socket and a terminal pore whereas the sensilla basiconica found on the acroglossal button lack a socket and a terminal pore (Fig. 6C).

The two labial palpi insert at the prementum where it borders the mentum (Fig. 4). Each palpus consists of four segments bearing some bristle-shaped sensilla and few sensilla basiconica (Fig. 4B). Both the second and the third segment additionally have a large thorn-shaped bristle in females (Fig. 6D), which is less conspicuous in males. Female wasps have one sensillum basiconicum both on the second and third segment of the labial palpus whereas male wasps have 6 to 8 sensilla basiconica at the end of the third segment.

We thank Volker Mauss (Staatliches Museum für Naturkunde, Stuttgart, Germany) for providing male Vespula wasps. We are grateful to Daniela Gruber of the electron microscopy laboratory (CIUS) and Brain Metscher (Department of Theoretical Biology) at the Faculty of Life Scienes (University of Vienna, Austria) as well as to Stephan Handschuh (VetCORE, University of Veterinary Medicine, Vienna) who helped with the µCT imaging.