Evolution of the suctorial proboscis in pollen wasps (Masarinae, Vespidae) Harald W. Krenn a, * , Volker Mauss b , John Plant a a Institut fu ¨r Zoologie, Universita ¨t Wien, Althanstraße 14, A-1090, Vienna, Austria b Staatliches Museum fu ¨r Naturkunde, Abt. Entomologie, Rosenstein 1, D-70191 Stuttgart, Germany Received 7 May 2002; accepted 17 July 2002 Abstract The morphology and functional anatomy of the mouthparts of pollen wasps (Masarinae, Hymenoptera) are examined by dissection, light microscopy and scanning electron microscopy, supplemented by field observations of flower visiting behavior. This paper focuses on the evolution of the long suctorial proboscis in pollen wasps, which is formed by the glossa, in context with nectar feeding from narrow and deep corolla of flowers. Morphological innovations are described for flower visiting insects, in particular for Masarinae, that are crucial for the production of a long proboscis such as the formation of a closed, air-tight food tube, specializations in the apical intake region, modification of the basal articulation of the glossa, and novel means of retraction, extension and storage of the elongated parts. A cladistic analysis provides a framework to reconstruct the general pathways of proboscis evolution in pollen wasps. The elongation of the proboscis in context with nectar and pollen feeding is discussed for aculeate Hymenoptera. q 2002 Elsevier Science Ltd. All rights reserved. Keywords: Mouthparts; Flower visiting; Functional anatomy; Morphological innovation; Evolution; Cladistics; Hymenoptera 1. Introduction Evolution of elongate suctorial mouthparts have occurred separately in several lineages of Hymenoptera in association with uptake of floral nectar. They can be found, for example, in various ‘symphytans’ (Jervis and Vilhelmsen, 2000), parasitoid Apocrita (Jervis, 1998), sphecids (Ulrich, 1924), Scoliidae, Sapygidae, Tiphiidae (Osten, 1982, 1991) and in many bees (Michener, 1944, 2000). In Vespidae, despite the fact that the adults of both sexes obtain at least some nourishment from floral nectar (Kugler, 1970; Proctor et al., 1996), a very long elongate suctorial proboscis is not common, except in Eumeninae (Osten, 1982) and Masarinae. The Masarinae, or pollen wasps, are unique among the vespids for their bee-like habits of provisioning each larval brood cell with pollen and nectar. Female pollen wasps use their mouthparts to gather pollen and nectar from flowers and for nest construction (Gess and Gess, 1992; Gess, 1996, 2001; Mauss, 1996, 2000; Mauss and Mu ¨ller, 2000). Some have very long proboscides; however, in contrast to bees, the proboscis is formed only by the glossa and, in some species, it is looped back into the prementum when in repose (Bradley, 1922; Schremmer, 1961; Richards, 1962; Osten, 1982; Carpenter, 1996/1997; Gess, 1998). The traditional classification of the Masarinae, dating back to Saussure (1854), was based on the misunderstanding that the glossa of one group (based on Paragia ) cannot be retracted at all and the glossa of the other group (based on Masaris ) can be retracted into the prementum. Carpenter’s (1996/1997) study of the Paragiina clarified the morpho- logical misunderstanding and demonstrated that the glossa in all groups is retractable. The separation of the Masarinae into two main lineages, the Paragiina and Masarina, however, was upheld in that study by other features. Currently the Masarinae contains 14 genera with about 300 species (Carpenter 1982, 2001) and is divided into the Gayellini and Masarini. The latter tribe consists of Paragiina (Australian region only), Masarina (widespread except Australia) and Priscomasarina, which was estab- lished to accommodate a newly discovered species from Namibia (Gess, 1998, Fig. 1). The evolution of an elongate proboscis occurred at least twice in the Masarinae. Elongation of the proximal part of 1467-8039/02/$ - see front matter q 2002 Elsevier Science Ltd. All rights reserved. PII: S1467-8039(02)00025-7 Arthropod Structure & Development 31 (2002) 103–120 www.elsevier.com/locate/asd * Corresponding author. Tel.: þ43-1-4277-54497; fax: þ 43-1-4277- 9544. E-mail addresses: [email protected] (H.W. Krenn), volker. [email protected] (V. Mauss).
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Evolution of the suctorial proboscis in pollen wasps (Masarinae
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Evolution of the suctorial proboscis in pollen wasps
montanum L. (Lamiaceae) (C. tuberculifer )) was indirect;
pollen was brushed from the anthers or from parts of the
Fig. 1. Dendrogram showing hypothesized phylogeny of Masarinae,
combined from Carpenter (1982, 1989, 1993, 1996) and Gess (1998).
Taxa in bold type are investigated in this study.
H.W. Krenn et al. / Arthropod Structure & Development 31 (2002) 103–120104
body and brought between the mouthparts by movements of
the forelegs, the distal parts of which form pollen brushes.
Although nectar uptake is difficult to verify, it can be
supposed to occur at several zygomorphic flowers with a
deep tubular corolla (Marrubium supinum L., Nepeta
nepetella L. (both Lamiaceae) (C. hispanicus ); Teucrium
montanum (C. tuberculifer ); Echium vulgare L. (Boragina-
ceae), Dorycnium hirsutum (C. lusitanicus )). The glossa
was never extended before the wasp had put its head into the
corolla of these flowers, but on some occasions it could be
observed that the glossa was still somewhat extended when
the wasp pulled its head back. The glossa was always
completely retracted shortly thereafter and wasps never flew
off with extended mouthparts. Ceramius fonscolombei was
observed to visit the easily accessible flowers of Reseda,
presumably for nectar uptake, since its short proboscis could
be seen extended toward the nectar-bearing dorsal enlarge-
ment on the disc of the flower, with the mandibles slightly
opened.
Ceramius uses water to moisten the soil during particular
stages of nest construction (Gess and Gess, 1992; Gess,
1996, 2001; Mauss and Muller, 2000). To collect water the
females of C. hispanicus (Fig. 3), C. lusitanicus and C.
fonscolombei landed at the edge of a water site or on damp
soil. They opened their mandibles and extended the glossa.
The extension process was very rapid. During the following
period of water uptake only the distal tip of the glossa
reached the wet surface. Normally the proboscis was
slightly bend ventrad. The distal bifurcated section of the
glossa was straight and parallel. On a few occasions the
proboscis was bend slightly dorsally in C. lusitanicus with
the distal tip lying on the ground. The posture of the wasp
depends on the length of its glossa. Females of C.
fonscolombei with a short proboscis lowered their heads
close to the water surface, while individuals of C.
hispanicus and C. lusitanicus with a long proboscis raised
their heads above the main body axis (Fig. 3). When
imbibing water the outer surface of the glossa appears to be
covered with adherent water which resulted in shiny
reflections.
3.2. Mouthpart morphology
The gross morphology of the head, mandibles and
maxillae is briefly summarized for the investigated
Masarinae. The surface of the head and exposed areas of
the mouthparts are covered with long unbranched bristles.
Viewed frontally, the clypeus projects over the labrum.
Long bristles of the labrum protrude from under the clypeus
(Figs. 4 and 8). When the mandibles are closed, they
obscure the frontal view of the maxillae and labium except
for the tips of the glossa and palpi. The labium and maxillae
are visible from the posterior view of the head (Fig. 7). The
basal parts of the maxilla, i.e. the cardo and stipes, lie
between the labium and the head. The stipes is arched and
tilted at a slight angle against the labium. Proximally it is
attached to the apex of the cardo and distally it bears the
lacinia, galea, and maxillary palpus which has six segments
in P. namibiensis and five in P. decipiens. The lacinia is a
large, flat lobe overlapping the anterior part of the galea.
The distal portion of the galea is composed of several plates,
one of which bears on the inner surface a longitudinal row of
bristles. Pollen grains are commonly found on this galeal
comb. The inner surface of the galea is basally continuous
with the preoral cavity, which is formed by the epipharynx,
the underside of the labrum and the large muscular
hypopharynx. The hypopharynx contains the voluminous
infrabuccal pouch, which in some specimens was filled with
pollen (Figs. 6 and 13). Parts of the lacinia and galea, which
are positioned near the infrabuccal pouch are responsible for
pushing pollen grains into the mouth (Fig. 6).
The short-tongued mouthparts of P. namibiensis and P.
Figs. 2 and 3. Fig. 2: Ceramius lusitanicus female collecting pollen with mandibles and maxillae at a flower of Helianthemum organifolium (Lam.) Pers. Fig. 3:
C. hispanicus female imbibing water from moist soil with extended glossa (arrow).
H.W. Krenn et al. / Arthropod Structure & Development 31 (2002) 103–120 105
decipiens correspond in many features to the plesiomorphic
condition for vespids, e.g. Euparagiinae (Bradley, 1922),
Eumeninae (Richards, 1962; Osten, 1982) and Vespinae
(Kirmayer, 1909; Brocher, 1922; Duncan, 1939). The labial
palpus is 4-segmented, the glossa is bifid and has a length of
approximately 1.5 mm in P. decipiens (Figs. 4 and 5). The
glossa is short compared to the prementum, whereas the
paraglossae are relatively large and conspicuous (Fig. 5).
The prementum is elongate and u-shaped with large median
arches adjoining the hypopharynx on its lateral edges. The
glossa emerges from the distal end of the prementum and is
flanked by the paraglossa, which arise from the paraglossal
sclerite. Intermediate the glossa and the prementum on the
posterior side is the large and strongly flexible ‘posterior
lingual plate’ (Duncan, 1939) which arises out of the apical
prementum and leads into the short glossal rod; intermediate
on the anterior side is the ‘anterior lingual plate’ (Duncan,
1939) which is characterized by its lateral arms.
While the mandibles and maxillae are similar in form and
function in all investigated Masarinae major differences
occur in the morphology of the glossa which forms the
principle organ of fluid uptake. The plesiomorphic glossa of
vespids and basal pollen wasps can be morphologically
divided into a proximal section and a distal, often bilobed or
bifurcated section with the acroglossal buttons. The anterior
surface of the glossa bears transverse rows of flattened hair-
like cuticular structures, however, in the Masarini these are
modified into lamella-shaped plates. The lamellae in
Priscomasaris transverse the entire glossal surface, while
in Paragia, they are divided medially into two rows
extending from the glossal base to the tips of the deeply
bifid glossa (Fig. 5). The food canal of the proximal section
of the glossa is a deep longitudinal pocket set between the
lateral rows of lamellae. On the anterior surface of each
glossal lobe, the lamellae arch toward the hair-like cuticular
structures emerging from the posterior surface and together
they form a narrow food canal (Fig. 5). An acroglossal
button with associated sensilla is located on the posterior
apex of each glossal lobe. The paraglossa are elongate,
extending beyond the proximal section of the glossa, and
Figs. 4–6. Fig. 4: Head of P. decipiens (Paragiina); mandibles (md) are open and the glossa (gl) is extended. Clypeus (cl) partly covers the labrum (lr). Fig. 5:
Bifurcate glossa (gl) of P. decipiens (Paragiina) in dorsal view; paraglossae (pgl) lie laterally at the basis of the glossa; dorsal side of glossa bears transverse
cuticular lamellae which enclose the food canal of the bifid distal region. Fig. 6: Longitudinal section through head of P. namibiensis (Priscomasarina). Glossa
(gl) folded under the preoral cavity (poc). Infrabuccal pouch (ibp) filled with pollen grains; m. intralabialis posterior (mip) folds the posterior lingual plate (plp)
against the prementum (pr); glossa rod (glr) is bent in posterior direction. Extension of the glossa is achieved by contraction of m. intralabialis anterior (mia)
which permits the anterior lingual plate (alp) to revert back to its extended position parallel to the prementum.
H.W. Krenn et al. / Arthropod Structure & Development 31 (2002) 103–120106
their concave median surfaces laterally embrace the base of
the glossa (Fig. 5). In both species, glossa and paraglossae
fold together in repose (Fig. 7).
The plesiomorphic resting position of the labium is a z-
shaped fold (Figs. 6 and 7). When folded, the glossal base
frontally closes the preoral cavity (Figs. 6 and 7). In this
position the glossa is bent toward the hypopharynx at a right
angle to the prementum. The posterior lingual plate is flexed
against the prementum and the short glossal rod bends the
distal bifurcated section of the glossa in the opposite
direction (Fig. 6).
The musculature of the labium which is considered
responsible for direct movements of the glossa is diagramed
in Fig. 7. The muscles are labeled according to origin and
attachment sites and numbered after Matsuda (1965) with
regard to probable homology within the Hymenoptera.
Comparison of serial head sections with the glossa in
retracted and extended positions enabled us to draw
conclusions on the functional mechanism of glossal move-
ments. The glossa is folded primarily by contraction of
musculus intralabialis posterior (M42), which folds back
the posterior lingual plate, and by contraction of m.
craniolabialis anterior (M34), which draws back the
anterior lingual plate (Fig. 7B). Extension of the glossa is
achieved by m. intralabialis anterior (M43) which permits
the anterior lingual plate to revert back to its extended
position parallel to the prementum, and by m. craniolabialis
posterior (M35), which originates on the clypeus and
extends at a right angle to the prementum. Its contraction
pulls the proximal prementum toward the proboscidial fossa
of the head capsule and probably thus contributes to initial
extension of the glossa (Fig. 7D).
Proboscis of Ceramius species. The major modification
in the labium of Ceramius species, as compared to P.
decipiens, regards glossal length, formation of a closed food
tube, increased flexibility at the articulation between the
basal glossa and prementum, and the resting position of the
glossa. We investigated two species of Ceramius, the
relatively short-tongued C. fonscolombei (glossal length
2 mm) and the long-tongued C. hispanicus with a glossal
length of 5.6 mm (^0.2; n ¼ 10). In both species, the
cuticular structures of the glossa build an enclosed median
food tube along its entire length and it can be retracted into
the prementum. Despite variation in glossal length, the
functional mechanisms presumed to be responsible for
retraction and protraction appear identical, at least with
regard to internal anatomy.
The elongate suctorial glossa of Ceramius and most other
higher Masarina can be functionally and morphologically
divided into three sections: a short proximal section, a long
middle section, and a distal, usually bifurcated, section
(Fig. 10). The proximal section of the glossa encompasses
the posterior articulation to the prementum (Fig. 9). The
distal prementum connects via the ‘hinge plate’ (Duncan,
1939) to the well-sclerotized posterior lingual plate which is
continuous with the glossal rod. The internal elastic glossal
rod extends the entire length of the glossa to the bifurcated
section. The anterior side of the proximal glossa is
connected to the anterior lingual plate by a thin and flexible
cuticle which allows the glossa to telescope under the
anterior lingual plate. Distally, the anterior lingual plate is
forked to embrace the lateral base of the glossa which itself
is adjoined to the paraglossal sclerite as well as to the lateral
prementum processes. The posterior and lateral sides of the
glossa are characterized by an elastic cuticular membrane
up to the middle of the glossa (Fig. 16).
Fig. 7. Schematic drawing of head of P. decipiens (Paragiina). Striped muscles indicate those responsible for glossal retraction (A, B), and glossal extension (C,
D). (A) Posterior view, glossa retracted. (B) Longitudinal section of head; glossa retracted by contraction of m. intralabialis posterior (mip) and m.
craniolabialis anterior (mca). (C) Posterior view, glossa extended. (D) Longitudinal section of head, glossa extended by contraction of m. intralabialis anterior
H.W. Krenn et al. / Arthropod Structure & Development 31 (2002) 103–120 107
The food tube of the middle section is formed by two
longitudinal and adjacent rows of lamellae on the anterior
surface. The arching lamellae of each row overlap the
preceding ones and the two rows come together to form a
completely closed median food tube that extends the entire
length of the glossa (Figs. 11 and 16). The broad surfaces of
the plates are finely sculptured, a feature that may help to
ensure a tight closure between the plates yet permit
flexibility (Fig. 11). In the proximal section of the glossa,
the food canal widens, the lamellae are larger and the two
rows do not overlap as tightly as in the middle section. The
proximal widening opens into the preoral cavity which is
covered by the labrum and distal parts of the maxilla. At the
bifurcated section of the glossa, the food tube splits and
continues along each glossal lobe (Figs. 12 and 16). Each
food canal in this section is formed by the strongly curved
and overlapping lamellae on the anterior side, while the
posterior side is formed by additional cuticular structures
that curve upward from the underside of the glossa, together
enclosing a narrow canal along the inner margin of each
glossal lobe (Fig. 16). They have small spines, possibly to
increase surface area. Fluids are probably taken up through
the slits between the lamellae and between the hair-like
structures (Fig. 12). The acroglossal buttons are reduced in
size and bear numerous short conical sensilla each with a
single terminal pore.
In the retracted position, the glossa is almost entirely
withdrawn into the prementum and lodged underneath the
anterior lingual plate (Figs. 8, 9, 14 and 16). The glossa rod
is connected to the prementum by the intervening hinge
plate and posterior lingual plate which permits two 908
flexions of the glossa (Fig. 9). First is the flexion of the hinge
plate on the prementum, and second the flexion between the
hinge plate and posterior lingual plate, together they result
in a reversal of the direction of the glossa (Figs. 13 and 14).
At about one third of its length the retracted glossa bends
about 1508 forward so that its anterior surface lies directly
under the anterior lingual plate, the tips of the glossal lobes
lie between the maxillae and mandibles. The membranous
cuticle of the proximal glossa half is pulled into the
prementum and forms a cavity (Fig. 14). In cross-section,
the prementum is strongly u-shaped to provide space for the
loop of the retracted glossal rod.
The anterior side of the glossa, which is connected to the
median area of the anterior lingual plate, retracts tele-
scopically through the forked arms of the anterior lingual
plate. The flexible sleeve-like anterior surface of the glossa
invaginates at the distal end of anterior lingual plate (Figs.
13 and 14), extending back beneath the plate near to
salivarium where it turns forward. The anterior lingual plate
extends as a long and narrow sclerite to the proximal end of
the prementum (Figs. 13 and 14). The paraglossae are short
and can be only partially retracted.
The pronounced difference in labial musculature
between P. decipiens and the Ceramius species concerns
the course of the m. intralabialis anterior (M43). This
muscle extends between the inner premental margin and the
anterior lingual plate. In Ceramius it is fan-shaped due to
the strongly u-shaped prementum and the elongation of the
anterior lingual plate. One part of this muscle extends from
the proximal end of the prementum to the anterior lingual
plate at a right angle to the course of the prementum (Figs.
13 and 14). Another part extends from the lateral margin of
the prementum to the anterior lingual plate at an oblique
angle. Further portions of this muscle extend between the
premental processes and the lateral arms of the anterior
lingual plate. Together with the shape of the prementum, the
thin fan-shaped muscles form a deep cavity or pouch in
which the glossa retracts (Fig. 14).
A functional model for the mechanism of extension and
retraction of the glossa (Fig. 17) was derived from
dissections and comparison of the sectional series in
specimens with the proboscis in retracted and extended
positions (Figs. 14 and 15). In Ceramius the contraction of
the fan-shaped m. intralabialis anterior (M43) constricts the
space between anterior lingual plate and the prementum and
squeezes the premental pouch which envelopes the glossa
(Fig. 15). In this manner, the glossa rod is moved forward
out of the pouch. Contraction of the anterior part of these
muscles forces the entire anterior lingual plate forward, and
the anterior side of the glossa turns inside out. Due to its
elastic properties the glossa immediately projects forward to
its full extent, as determined in freeze-killed and thawed
specimens. The role of the m. craniolabialis posterior
(M35) is not entirely clear. Its contraction may pull the
prementum deeper into the head cavity which would
contribute to the compression of the space between
prementum and anterior lingual plate (Fig. 17). Opening
of the mandibles is a likely precondition for glossal
extension. According to the field observations the mandibles
were always observed to be open when the glossa was
extended (Fig. 3).
During the initial phase of retraction of the glossa, the
posterior lingual plate is folded back into the prementum by
Figs. 8–12. Fig. 8: Head of C. hispanicus (Masarina) in frontal view. Mandibles (md) closed; glossa retracted into prementum. Clypeus (cl) covers the labrum.
Fig. 9: C. hispanicus (Masarina); distal portion of the labium in lateral view; left mandible and maxilla removed. Glossa retracted into prementum (pr), only
glossal tips (gl) visible; posterior lingual plate (plp) at a right angle to hinge plate (hp) which is at a right angle to prementum. Clypeus (cl), mandible (md),
labial palpus (lp), maxillary palpus (mxp). Fig. 10: Head of C. hispanicus (Masarina) in lateral view. Glossa (gl) extended; hinge plate (hp) and posterior lingual
plate (plp) are extended outward forming the articulation of the glossa (gl) and prementum (pr); glossa tip (glt) is bifurcated; paraglossa (pgl) is short. Fig. 11:
Cross cut through the middle section of the glossa. Overlapping cuticle lamellae form the food tube (ft) along the anterior side; the glossa rod (glr) provides
stability to the glossa. Fig. 12: Bifurcate glossal tip in C. hispanicus. Each glossal half has a separate food canal formed by spiny cuticular structures; tip bears
acroglossal button (ab).
H.W. Krenn et al. / Arthropod Structure & Development 31 (2002) 103–120108
H.W. Krenn et al. / Arthropod Structure & Development 31 (2002) 103–120 109
Figs. 13–16. Fig. 13: Ceramius fonscolombei (Masarina), longitudinal section through head. Relatively short glossa (gl) is held in resting position. Posterior
lingual plate (plp) is folded and glossal rod (glr) is retracted into the prementum (pr). Anterior lingual plate (alp) is longer than retracted glossa. Paraglossa
(pgl), clypeus (cl) and labrum (lr) form frontal closure of the preoral cavity (poc); distal plates of maxillae (mx) transport pollen into the infrabuccal pouch
(ibp). Fig. 14: C. hispanicus (Masarina), longitudinal sections through the prementum (pr) with retracted glossa (gl). Glossal rod (glr) articulates with
prementum via posterior lingual plate (plp) and hinge plate (hp); glossal tip (glt) at same level as paraglossa (pgl); long anterior lingual plate (alp) give
H.W. Krenn et al. / Arthropod Structure & Development 31 (2002) 103–120110
contraction of m. intralabialis posterior (M42) (Fig. 17). At
a particular point the elastic properties of the glossal rod
force the glossa to suddenly slip into the premental pouch.
The membranous cuticle of the anterior side invaginates
under the anterior lingual plate. The posterior side turns into
the prementum by the double flexion of the glossa (Fig. 17).
Contraction of m. craniolabialis anterior (M34) pulls back
the anterior lingual plates and the lateral glossal base (Fig.
17).
Proboscis of higher Masarina. In most of the higher
Masarine taxa, the glossa is longer relative to body length
than in the previously discussed species. In J. braunsi and
M. familiaris the glossa has a length of 3.0–3.3 mm which
is equal to one third body length. In Quartinioides sp. it is
about 4.9–5.0 mm long which is about as long as the body.
The principle morphology of the glossae and the basic
mechanism of retraction in all investigated higher Masarina
is the same as described for Ceramius. The glossa is
retracted between the prementum and the anterior lingual
plate, but due to its great length the looped glossa extends
beyond the proximal end of the prementum to a varying
degree in the different species. A sac formed by mem-
branous cuticle (‘glossal sac’, Richards, 1962) is visible on
the posterior side of the head as a lightly colored sac behind
the more darkly sclerotized prementum.
In J. braunsi, as in Ceramius, the glossa lies in one great
loop within the prementum and protrudes beyond the
proximal end of the prementum and cardines (Fig. 18). The
musculature of the labium does not envelope the sides of
the glossal pouch. The m. intralabialis anterior (M43) is
attachment site of m. intralabialis anterior (mia); m. intralabialis posterior (mip) attaches at posterior lingual plate. Fig. 15: C. hispanicus (Masarina),
longitudinal sections through prementum (pr), glossa (gl) extended. The two articulations between prementum and hinge plate (hp) and between hinge plate
and posterior lingual plate (plp) are extended. Anterior lingual plate (alp) pressed against prementum due to contraction of m. intralabialis anterior (mia) and
m. craniolabialis posterior (mcp); m. craniolabialis anterior (mca) attaches at anterior lingual plate. Fig. 16: C. hispanicus (Masarina), cross-sections through
the glossa in (A) the proximal half, (B) the distal half, and (C) the tip region. Cuticular structures of the lateral glossal wall form the food tube (ft) on the anterior
side of the glossa. The glossal rod (glr) stiffens the glossa on the posterior side. The lumen of the glossa (gll) is voluminous in the proximal half and narrow
distally; the bifid tip region has a double food tube formed by curved cuticular structures from both sides of the glossa.
Fig. 17. Model of the functional mechanism of glossal movement in Ceramius. (A) Glossa retracts by contraction of m. intralabialis posterior (mip) and m.
craniolabialis anterior (mca).(B) Glossa unfolds by contraction of m. intralabialis anterior (mia) and m. craniolabialis posterior (mcp). Areas of articulation
between prementum (pr) and hinge plate (hp) and between hinge plate and posterior lingual plate (plp) are extended. Arrows indicate movements of
mouthparts.
H.W. Krenn et al. / Arthropod Structure & Development 31 (2002) 103–120 111
smaller and extends only into the proximal third between the
anterior lingual plate and the prementum. This muscle is
composed of two portions, one runs obliquely in the
posterior direction to the proximal/median region of the
prementum, the other portion extends in a lateral direction
and inserts on the lateral margin of the prementum.
In M. familiaris the glossa sac is remarkably enlarged
and arches over the hypostomal bridge. Due to the
transparency of the cuticle, the loop of the glossal rod is
visible from outside. The stipites have processes directed
toward the median sides behind the proximal end of the
prementum. In Celonites peliostomi the glossal sac is large
and extends well beyond the head.
In Quartinioides sp. the prementum is rather flat, broad
and rounded on the posterior side and extends with two
slender arms over the lateral sides. No glossal sac is present.
In comparison to the short body length, the glossa of
Quartinioides sp. is extremely long and very thin, being
about ten times as long as the prementum. The bifurcate
section makes up about 85% of total glossal length.
Longitudinal sections through the head reveal that the
glossa retracts into several longitudinal and transversal
loops within the prementum (Fig. 19). In this species, as in
the examined Jugurtia and Masarina, the m. intralabialis
anterior (M43) is weak and does not envelope the glossal
pouch.
3.3. Cladistics
The Masarinae have been subjected to previous cladistic
analyses. In Carpenter’s (1982) phylogenetic study, which
was based on 50 characters and numerous vespid taxa
including the pollen wasps, the superfamily Vespoidea was
reduced to the single family Vespidae with the following
(Stenogastrinae þ (Polistinae þ (Vespinae))))). The
Euparagiinae were removed from the masarids leaving
two tribes of pollen wasps, the Gayellini and Masarini. The
Gayellini were analyzed by Carpenter (1989). Carpenter
(1993) presented a dendrogram of the Masarinae, based on
about 50 unpublished characters in which Paragia þ
Metaparagia were the sister-group to the remainder of the
Masarini. In an analysis of the Australian species of pollen
wasps, Carpenter (1996/1997) separated the Masarini into
Figs. 18 and 19. Fig. 18: Longitudinal section through head of J. braunsi (Masarina). Glossal rod (glr) is retracted into a loop which bulges beyond the
prementum (pr) and cardo (c). Posterior lingual plate (plp) is folded backward by m. intralabialis posterior (mip); hinge plate (hp) is bent against the
prementum. Micrograph is composite of photos of two sections from the same series. Fig. 19: Longitudinal section through head of Quartinioides sp.
(Masarina). The glossa (gl) is retracted in several loops into the prementum (pr); glossal tip (glt) frontally covered by distal plates of the maxillae (mx).
m.intralabialis posterior (mip).
H.W. Krenn et al. / Arthropod Structure & Development 31 (2002) 103–120112
two subtribes, Paragiina (containing Paragia and Meta-
paragia ) and Masarina. The analysis of Gess (1998) with
consideration of 17 characters split the Masarini into three
subtribes with Priscomasaris as only member of a new
subtribe, Priscomasarina, which formed a sister group
relation to remaining subtribes, Paragiina þ Masarina.
The present analysis utilizes 28 characters (Table 1)
many of which are adopted from Gess (1998) and Carpenter
(1982, 1996/1997). Three multistate characters (11, 12, 15)
representing transformation series were coded as additive.
Euparagia (Euparagiinae) was selected as the outgroup.
Computer analysis on the data matrix of Table 2 using
NONA (Goloboff, 1993) yields one cladogram (Fig. 20)
with a step length of 49, consistency index of 0.79 and
retention index 0.81. Cladograms were examined and
characters plotted using WinClada (Nixon, 2000).
The cladogram in Fig. 20 confirms the tribal and
subtribal arrangement of taxa as presented in Gess (1998).
The clade Paragiina þ Masarina is supported by two
synapomorphies, both features of the glossa, i.e. food
canal of proximal glossa formed by lamellae (character 11,
state 2), and the presence of a food canal on the glossal lobes
(character 12, state 2). A processed male foretrochanter
(character 18) was regarded as another potential synapo-
morphy in the analysis of Gess (1998), however, the
character plotting is equivocal in this study, since it is
present in Paragia and Ceramius but not the other
investigated Masarina.
The cladistic analysis shows that the trend toward
elongation of the proboscis is accompanied by morphological
innovations, such as the presence of lamellae on the anterior
glossa (character 11, state 1) leading to the formation of a
median food canal between the lamellae (character 11, state
2). Both states are necessary preconditions for the formation
Table 1
List of characters and character coding used in cladistic analysis of Fig. 20
4. Number of male antennal articles: (0) thirteen; (1) twelve
5. Female mandibles: (0) quadridentate; (1) tridentate; (2) bidentate. Polarity as in Gess (1998)
Mouthparts
6. Paraglossa: (0) about as long as or longer than proximal section of glossa; (1) shorter; (2) reduced or absent
7. Prementum: (0) longer or about as long as proximal section of glossa; (1) shorter than proximal section of glossa
8. Glossa: (0) shorter than head length; (1) longer than head length; (2) about as long or longer than body
9. Glossa retractable into prementum: (0) partially; (1) almost fully with one loop; (2) almost fully and coiled into several loops
10. Glossal sac: (0) absent; (1) moderate in size; (2) large extending beyond cardo. Ceramius was coded with state one; however, state two may be present in
some species
11. Glossal anterior surface with: (0) transverse rows of hairs; (1) transverse rows of lamellae; (2) median food canal formed by non-overlapping lamellae; (3)
median food tube formed by overlapping lamellae. Additive
12. Glossal lobe: (0) without processes; (1) with two rows of flattened processes forming a sponge-like extension; (2) flattened processes overlap and curve
together to form a tube. Additive
13. Anterior lingual plate: (0) short; (1) long and narrow sclerite to the proximal end of the prementum
14. Acroglossal buttons: (0) present; (1) absent
15. Maxillary palpi: (0) six-segmented; (1) three-segmented; (2) two-segmented; (3) one-segmented. Additive. Character is variable in Paragiina and
Ceramius
Mesosoma
16. Pretegular carina: (0) present; (1) absent. Polarity as in Carpenter (1996/1997) and Gess, 1998)
17. Propodeal spiracle: (0) lateral; (1) more or less dorsal
18. Male foretrochanter: (0) without process; (1) with process
Forewing
19. Marginal cell: (0) not narrower basally than apically; (1) 2r-rs curving basal to insertion of RS so that it is narrower
20. Submarginal cell number: (0) three; (1) two
21. CuA2 and A: (0) angled where meeting; (1) rounded together
22. First discal cell: (0) shorter than subbasal cell; (1) as long or longer than subbasal cell
23. CuA: (0) diverging from M þ CuA; (1) distal to insertion of cu-a; (2) based to insertion of cu-a
24. Cu-a: (0) transverse; (1) inserted on CuA and aligned with A
25. Longitudinal folding: (0) absent; (1) present
Hindwing
26. Free apical section of A: (0) present; (1) absent
27. Jugal lobe: (0) present; (1) reduced
Biology
28. Larvae feed on: (0) insect prey; (1) pollen and nectar
H.W. Krenn et al. / Arthropod Structure & Development 31 (2002) 103–120 113
Table 2
Distribution of 28 characters (Table 1) used in cladistic analysis (Fig. 20). Character numbers in bold type
Head Mouthparts
Clypeal
dorsal
margin, 1
Shape of
clypeus,
2
Eye
margin-
ation,
3
Number
of
antennal
articles,
4
Female
mandibles,
5
Para-
glossa
length,
6
Premen-
tum
length,
7
Glossa
length,
8
Glossa
retracted
into
premen-
tum,
9
Glossal
sac,
10
Lamellae
on glossa,
11
Glossal
lobe
with
food
tube,
12
Anterior
lingual
plate, 13
Acro-
glossal
buttons,
14
Maxillary
palpi
segment
number,
15
Euparagia 0 0 0 0 2 0 0 0 0 0 0 0 0 0 0
Gayella 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Priscomasaris 0 0 1 1 1 0 0 0 0 0 1 1 0 0 0
Paragia 0 0 1 1 1 0 0 0 0 0 2 2 0 0 0
Ceramius 0 1 0 1 1 1 1 1 1 1 3 2 1 0 0
Celonites 0 0 0 1 2 2 1 1 1 2 3 2 1 1 1
Masarina 0 0 0 1 1 1 1 1 1 2 3 2 1 0 2
Jugurtia 0 0 0 1 1 1 1 1 1 2 3 2 1 0 2
Quartinioides 0 0 0 1 2 2 1 2 2 0 3 2 1 0 3
Quartinia 0 0 0 1 2 2 1 1 1 1 3 2 1 0 3
Mesosoma Forewing Hindwing Biology
Pretegular
carina, 16
Propodeal
spiracle,
17
Male
foretro-
chanter,
18
Marginal
cell, 19
Submar-
ginal
cell
number,
20
CuA2
and
A, 21
First
discal
cell,
22
CuA,
23
Cu-a,
24
Longitu-
dinal
folding,
25
Free
apical
section
of A,
26
Jugal
lobe,
27
Larval
food,
28
Euparagia 0 0 0 0 0 0 1 0 0 0 0 0 0
Gayella 1 0 0 0 0 0 0 1 0 0 0 1 1
Priscomasaris 1 0 0 0 1 0 1 2 1 0 1 1 1
Paragia 0 1 1 1 1 1 1 2 1 0 1 1 1
Ceramius 0 0 1 0 1 0 1 2 1 0 1 1 1
Celonites 0 1 0 0 1 0 1 2 1 1 1 1 1
Masarina 0 0 0 0 1 0 1 0 1 0 1 1 1
Jugurtia 0 0 0 0 1 0 1 0 1 0 1 1 1
Quartinioides 0 0 0 0 1 0 1 0 1 1 1 1 1
Quartinia 0 0 0 0 1 0 1 0 1 1 1 1 1
H.W
.K
renn
eta
l./
Arth
rop
od
Stru
cture
&D
evelop
men
t3
1(2
00
2)
10
3–
12
01
14
of the closed food tube of the elongated glossa (character 11,
state 3) in Masarina. Furthermore, the lengthening of the
anterior lingual plate (character 13, state 1) seems to be
crucial for the development of novel mechanisms enabling
the extension of the glossa out of the glossal sac. Elongation
of the glossa in Masarina is also associated with shortening of
the paraglossa (character 6, states 1 and 2). The presence of a
moderate-sized protruding glossal sac (character 10, state 1)
is interpreted by the analysis as a synapomorphy of the
Masarina; however, it is absent in Quartinioides. A large
protruding sac (character 10, state 2) is regarded as
convergent in Celonites and the clade Jugurtia þ Masarina,
however, it could be a synapomorphy of the higher Masarina
with a reversion in Quartinia and a loss in Quartinioides.
4. Discussion
4.1. Morphological innovations in the suctorial proboscis of
pollen wasps
Flower visiting behavior in insects is connected with a
host of modifications in the mouthparts. Many of these are
adaptations for pollen collection and ingestion as well as
nectar consumption. Radical transformations of the mouth-
parts are evident in various forms of elongation that are
associated with nectar feeding from flowers with a deep
corolla (Schremmer, 1961; Jervis, 1998; Jervis and
Vilhelmsen, 2000). The evolution of an elongate suctorial
glossa from a short homologous condition is exemplified in
the pollen wasps. The basal taxa of the pollen wasps, i.e.
Gayella, Priscomasaris, Paragia possess a relatively short
glossa which has cuticular structures that allow uptake of
nectar and water, presumably, in large part by adhesion. The
functional morphology which enables a passive uptake of
liquids, at least until the vicinity of the preoral cavity where
pharyngeal suction takes over, is regarded as plesiomorphic
for the Masarinae since it appears to differ little from that of
other wasps in Euparagiinae (Bradley, 1922), Eumeninae
(Richards, 1962; Osten, 1982) or Vespinae (Kirmayer,
1909; Brocher, 1922; Duncan, 1939). The higher Masarina
possesses an elongate suctorial proboscis with morphologi-
cal innovations of the labium, i.e. the lamellar structures of
the glossa forming a food tube, the specialized apex and
basiglossal articulation, as well as the shape and muscles of
tion are often novel solutions to biomechanical problems,
such as formation of suction tubes, mechanisms of move-
ment and new resting positions for the long proboscis. Some
of these will be referred to below.
Suction. The elongate proboscis in Lepidoptera operates
like a drinking-soda straw, in that fluid is sucked along an
air-tight tube due to pressure created by the muscular
pharyngeal pump (Kingsolver and Daniel, 1995). The same
analogy applies to the glossa of higher pollen wasps, where
the lamellar cuticle structures of the glossa, which must be
homologous to the rows of hair structures on the glossa of
other Vespidae, form the long and air-tight median food
tube. Other mechanisms for ensuring the air-tightness of a
food canal include the coming together or the interlocking
of different parts, either temporarily, like in bees, or
permanently. Permanent linkage of the two halves of the
proboscis is achieved in Lepidoptera by a series of hooks
Fig. 20. Cladogram of Masarinae based on data in Table 2. Subtribes indicated on right margin. Character numbers are given above line and character states
below. The outgroup is represented by Euparagia. Morphological innovations associated with the production of a suctorial proboscis are formation of a food
canal, a looped glossa, and a closed food tube. Glossa retracted in several loops is an autapomorphy in Quartinioides.
H.W. Krenn et al. / Arthropod Structure & Development 31 (2002) 103–120 115
and overlapping cuticle plates (Hepburn, 1971; Krenn and
Modifications of the plesiomorphic condition have led to
development of short and long-tongued conditions which
are associated with nectar feeding. The short-tongued
proboscis as in many bees and wasps can extend somewhat
beyond the reach of the open mandibles since it has
undergone a general increase in size or length of its major
Table 3
Composition of food canal produced by elongation of apical mouthparts in various aculeate Hymenoptera. Type of mouthpart specializations (CNEA, see text)
follows Jervis (1998)
Glossa Paraglossa Galea Labial
palpi
Maxill.
palpi
Masarinae þ Metaparagia and subtribe Masarina
Eumeninae þ þ Raphiglossa (CNEA type 1)
Eumeninae þ þ þ ? Eumenes (Osten, 1982)
Scoliidae þ þ Scolia (Osten, 1982)
Chrysididae þ Parnopes (Linsenmaier, 1997)
Sphecinae þ þ Ammophila (Ulrich, 1924) (CNEA type 1)