Evolution of the suctorial proboscis in pollen wasps (Masarinae

Evolution of the suctorial proboscis in pollen wasps

(Masarinae, Vespidae)

Harald W. Krenna,*, Volker Maussb, John Planta

aInstitut fur Zoologie, Universitat Wien, Althanstraße 14, A-1090, Vienna, AustriabStaatliches Museum fur 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 Muller, 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: S1 46 7 -8 03 9 (0 2) 00 0 25 -7

Arthropod Structure & Development 31 (2002) 103–120

www.elsevier.com/locate/asd

* Corresponding author. Tel.: þ43-1-4277-54497; fax: þ43-1-4277-

9544.

E-mail addresses: [email protected] (H.W. Krenn), volker.

[email protected] (V. Mauss).

http://www.elsevier.com/locate/asd

the glossa or of the distal part thus defines two lineages, the

subtribe Masarina and Metaparagia (Paragiina) (Carpenter,

1996/1997). As a relatively small group of flower visiting

Hymenoptera, the Masarinae offer the possibility to

examine the pathways of mouthpart evolution in the context

of nectar feeding. We focus on a comparative functional

anatomy of the glossa in Masarini since in some genera it is

relatively short yet retractable while in others it is extremely

long. We delineate several morphological innovations

which are important for the formation and functioning of

a suctorial proboscis, in addition to discussing further

evolutionary aspects of the proboscis in Hymenoptera.

2. Material and methods

2.1. Field observation

Flower visiting behavior and water uptake were observed

in Ceramius fonscolombei Latreille, C. hispanicus Dusmet,

C. lusitanicus Klug in Spain (Aragon, Province Teruel:

Barranco de Zorita, 19–26 June 1998; north of Almohaja,

16–18 June 1998; east of Los Ibanez, 7–12 June 2000;

Rambla de Rio Seco, west of Valdecebro, 9–16 June 2000)

and in C. tuberculifer Saussure in France (Alpes-de-Haute-

Provence: Peyresq 19–28 July 1994; Montagne de Boules

26–29 July 1994) in part with the aid of close-up binoculars

and documented by macro-photography (scale 1:1).

2.2. Morphology

The mouthparts of females were examined using light

microscopy in Priscomasaris namibiensis Gess (Priscoma-

sarina), Paragia decipiens Shuckard (Paragiina), Ceramius

hispanicus and C. fonscolombei which are considered to be

basal representatives of Masarina, and several higher

Masarina, i.e. Masarina familiaris Richards, Jugurtia

braunsi Schulthess, Celonites peliostomi Gess and Quarti-

nioides sp. (classification after Carpenter (2001), who

regards Quartinioides as a subgenus of Quartinia ).

Fresh specimens were fixed in 70% ethanol or Duboscq-

Brasil solution (Romeis, 1989). Whole mount preparations

of the mouthparts were made from dissected heads. They

were soaked in diluted lactic acid at 40–50 8C for 1–2 days,

washed in distilled water, and embedded in polyvinyl

lactophenol without dehydration on glass slides. The

preparations were covered with glass slips and dried at

50 8C.

Serial semithin-section technique was used to examine

mouthpart anatomy with light microscopy and to recon-

struct the possible functional mechanisms of glossal move-

ments. The isolated heads were dehydrated with acidified

DMP (2,2-dimethoxypropane) and acetone, then embedded

in ERL-4206 epoxy resin under vacuum impregnation.

Semithin sections were cut using diamond knives. They

were stained with a mixture of 1% azure II and 1%

methylene blue in an aqueous 1% borax solution for

approximately 1 min at 80 8C. Series of sagittal semithin

sections were prepared for all the above listed species of

Masarinae. Preparations were made of P. decipiens and C.

hispanicus individuals with retracted and extended probos-

cides. The mechanism of glossal movements was studied in

thawed specimens of freeze-killed C. hispanicus and in

freshly collected C. lusitanicus, C. hispanicus and C.

fonscolombei.

For viewing in the scanning electron microscope (SEM),

fixed samples of P. decipiens, C. hispanicus, C. peliostomi

and Quartinioides sp. were dehydrated in ethanol and

submerged in hexamethyldisilazane prior to air drying

(Bock, 1987). A graphite adhesive tape was used to mount

them on SEM viewing stubs. The samples were sputter-

coated with gold and viewed in a Jeol JSM-35 CF SEM.

3. Results

3.1. Flower visiting behavior

The behavioral pattern exhibited by Ceramius on flowers

differed according to the shape of the flower and whether

pollen or nectar was collected. On flowers with exposed

anthers [Helianthemum spec. (Cistaceae) (C. lusitanicus and

C. hispanicus ); Reseda spec. (Resedaceae) (C. fonscolom-

bei )] females primarily harvested pollen directly (Fig. 2),

their mandibles clasped and nibbled the anthers; their

maxillae were visibly active during ingestion of the

loosened pollen. The proboscis was never extended. Pollen

uptake at zygomorphic flowers with hidden anthers (Lotus

corniculatus L. (Fabaceae) (C. hispanicus ); Dorycnium

hirsutum (L.) Ser. (Fabaceae) (C. lusitanicus ); Teucrium

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.


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

(mia) and m. craniolabialis posterior (mcp). Occipital foramen (of); cardo (c); stipes (st); maxillary palpus (mxp); mandible (md); prementum (pr); paraglossa

(pgl); glossa (gl), labial palpus (lp).


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).



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


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.


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

arrangement: Euparagiinaeþ (Masarinae þ (Eumeninae þ

(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).


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

Head

1. Clypeal dorsal margin: (0) straight; (1) bisinuate

2.Wing-shaped clypeus: (0) absent; (1) present

3. Eye emargination: (0) present; (1) absent

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


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

the prementum.

Morphological innovations enabling mouthpart elonga-

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.


and overlapping cuticle plates (Hepburn, 1971; Krenn and

Kristensen, 2000).

Intake region. Closed suctorial proboscides require

specialized regions at the apex of the food canal for fluid

uptake. In pollen wasps, this takes place through the slit-like

openings in the food canal of the glossal lobes. In other

insects the apical regions of the food canal are outfitted with

specialized sensilla, for example in Lepidoptera (Krenn,

1998; Krenn and Kristensen, 2000; Krenn et al., 2001) and

Diptera (Szucsich and Krenn, 2000, 2002). However, in

pollen wasps, the acroglossal button and its sensillae are not

strongly modified even in the most derived species.

The long tongue of bees has different requirements. The

glossa is enclosed inside the food tube and independently

performs licking movements extending beyond the

ensheathing tube (Snodgrass, 1956; Harder, 1982; Plant,

personal observation). The apical food tube must first be

loaded with nectar by means of the glossal movements and

capillary action, before it is drawn through the food tube to

the mouth by suction action (Kingsolver and Daniel, 1995).

A presuction nectar-loading stage is not necessary in

butterflies and the higher pollen wasps, since suction begins

with immersion of the apical uptake region in the nectar.

Mechanisms of protraction and retraction. The labio-

maxillary complex of aculeate Hymenoptera permits a

slight extension and retraction. The mechanisms for this

have been described for Vespula (Duncan, 1939), sphecids

(Ulrich, 1924), scoliids (Osten, 1982, 1988), and the short-

tongued bee Andrena (Harder, 1983). It involves at least

three major steps, the movement of the cardines which

swing the proboscis in or out of the proboscidial fossa, the

z-shaped fold between prementum and glossa, and the

folding or unfolding of the galea. When a significant

elongation of apical parts of the proboscis takes place, new

steps of extension and retraction are added onto the

preexisting ones.

Storage of glossa. The length of the proboscis is

contingent on its required storage space as well as the

retraction method; in the pollen wasps, e.g. Ceramius, the

space available inside the prementum is a limiting factor for

the length of the glossa. One solution taken by the higher

Masarina is to store the glossa outside the prementum by

creating an ‘opening’ in the cuticular membrane between

the cardines through which the glossa invaginates into a

large sac. The basic mechanism, however, remains the same

as in Ceramius, in that the glossa is retracted into one loop

even if it is so large as to protrude out of the prementum.

Quartinioides has taken another direction, its glossa lies

entirely within the prementum but in several irregular criss-

crossing loops. The mechanism of extension in Quarti-

nioides, however, remains puzzling. It may be significant

that its glossa, although very long, is also extremely thin, at

least in the species examined. Richards (1962) suggested

that hemolymph pressure was important for extension. It is

likewise not known how the glossa of Celonites and

Jugurtia is projected out from its fully retracted position

protruding beyond the basal part of the prementum.

Compressing the sides of the prementum together is

probably not sufficient to eject the looped glossa. It is

astonishing that the labial musculature in the examined

species of the subtribe Masarina, e.g. Ceramius, is only

slightly modified from the plesiomorphic condition in

pollen wasps; all muscles can be readily homologized

with those in other Vespinae and in general with other

Hymenoptera (Duncan, 1939; Matsuda, 1965). Compared to

the short-tongued Masarinae, e.g. Paragia, only one muscle

has modified its course. Due to the elongation of attachment

sites on the anterior lingual plate and the particularly arched

prementum, one part of this muscle is positioned up to 908

differently from the plesiomorphic condition. In the derived

condition the contraction of this muscle compresses the

glossal pouch inward and seems to be the major force in

initiating extension of the glossa, at least in Ceramius. In the

plesiomorphic condition, the same muscle functions for

extension as well, thus no new neural motor pattern is

necessary for the control of the glossa movements.

4.2. Comparative remarks on proboscis evolution in

Hymenoptera

Convergent evolution of an elongated proboscis associ-

ated with flower visiting behavior is apparent in many

groups of Hymenoptera. Even within the Masarinae a

second clade, the Australian Metaparagia independently

evolved an elongated glossa for probing flowers with deep

corollas (especially Goodeniaceae; Gess et al., 1995; Gess,

1996). However, in this taxon the proximal section of the

glossa is greatly elongated and the paraglossae reach to the

bifurcated section of the glossa; in addition the proboscis is

also retractable into the prementum (Carpenter, 1996/1997)

but the associated morphological changes and the mechan-

ism of retraction are undetermined.

Examples of long or moderately long mouthparts are

numerous in other aculeate Hymenoptera, i.e. Eumeninae

(Vespidae), e.g. species of Eumenes, Pterocheilus, Raphi-

glossa, Labochilus (Schremmer, 1961; Richards, 1962;

Bohart and Stange, 1965; Giordani Soika, 1974; Haeseler,

1975; Osten, 1982; Mauss, personal observation), many

Sphecinae including Ammophila, Sphex, some Bembicinae

(Ulrich, 1924; Bohart and Menke, 1976; Osten, 1982),

certain Tiphiidae, Sapygidae, and Scoliinae (Osten, 1982,

1991) and some Chrysididae and Pompilidae (Jervis, 1998).

Most of these derived elongate mouthparts differ from that

in Masarinae in that the food canal is not formed exclusively

by the glossa but includes other parts of the labium and

maxillae. For example, in the long-tongued bees (Apidae

and Megachilidae) the elongate and flattened labial palpi

together with the galea form a stationary sheath-like tube

within which the glossa operates (Snodgrass, 1956).

Retraction of the glossa into the prementum as in the

Masarina is not unique in Hymenoptera. It has been

described for Scolia (Scoliidae) (Konigsmann, 1976;


Micha, 1927; Osten, 1982, 1988) and Epomidiopteron

(Tiphiidae) (Osten, 1991). However, the proboscis at least in

Scolia is not a thin suctorial tube as both the glossa and

paraglossae are enlarged and fold back into the prementum

(Osten, 1982). In long-tongued bees, the elongated apical

parts of the proboscis fold back beneath the prementum.

Depending on the total glossal length the folded proboscis

may exceed the thorax and abdomen.

Some short-tongued bees have independently evolved an

elongate proboscis of very similar construction to that in

Apidae and Megachilidae, for example, especially in

Rophitinae (Halictidae) and Panurginae (Andrenidae)

(Michener, 1944, 2000), and also in one species of Andrena

(Andreninae) (LaBerge, 1978). Individual species of short-

tongued bees have also achieved other forms of elongation,

presumably with formation of a food canal, by production of

the maxillary palpi, or the labial palpi, or both together.

Elongation of the glossa alone is also occasionally found in

short-tongued bees, however, it is not apparent how or if a

special food tube is formed. The structures which constitute

the elongated section of the apical food canal are listed for

various bees and other aculeate Hymenoptera in Table 3.

It is reasonable to assume that the structures of the

maxillae and the labium underlie different selection

pressures and evolutionary constraints arising from their

role in foreleg cleaning, nectar feeding, pollen ingestion,

nest and brood cell construction and other functions of the

proboscis. A change in one of these behaviors may free

structures for evolutionary recruitment. In some cases it

may be possible to indicate which structures are preoccu-

pied, for example, in pollen wasps the galea is connected

with pollen eating and therefore presumably not available

for elongation. However, in general it is difficult to

determine why one particular structure or one set of

structures undergoes modification and not another.

To summarize, at least three morphological–functional

groups of mouthparts can be distinguished which may be

related to feeding habits of adult Hymenoptera. (1) The

unspecialized small labiomaxillary complex. (2) Apo-

morphic ‘short-tongued’ and (3) Apomorphic elongate or

‘long-tongued’.

The first group is presumably plesiomorphic for

Hymenoptera (Jervis, 1998). The main body of the

mouthparts usually does not extend beyond the reach of

the open mandibles. The labial and maxillary palpi,

however, are very long and active in performing tactile

sensory movements. The mouthparts are used to lick and

suck nectar, honeydew or prey body-fluid, examples are

Syspasis (Ichneumonidae) (Richards, 1977), Ampulex

(Ulrich, 1924) and Psenulus (Sphecidae).

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)

Sphecinae þ þ þ Bembix

Long-tongued

bees

þ þ þ Megachilidae, Apidae (CNEA type 4)

Andrenidae þ þ þ Protomeliturgini, Melitturgini, Perditini (e.g. Perdita ), Calliopsini (e.g. Callonychium ),

Andrena (Callandrena ) micheneriana (LaBerge, 1978) (CNEA type 4)

Andrenidae þ þ Neffapis longilingua (Panurginae) (Rozen and Ruz, 1995) (CNEA type 6)

Halictidae þ þ þ þ Various Rophitinae

Halictidae þ Ariphanarthra palpalis (Eickwort, 1969) (CNEA type 5)

Colletidae þ þ Leioproctus (Filiglossa ) filamentosus (Michener 2000)

Colletidae þ Niltonia (Colletinae) (Laroca et al., 1989)

Colletidae þ Chilimelissaa, Xeromelissa (Xeromelissinae), species of Hylaeus (Pseudhylaeus ),

H. (Prosopisteroides ) (Hylaeinae), Euhesma, and Euryglossa tubulifera (Euryglossinae)

(Michener, 1965; Houston, 1983) (CNEA type 5)

Colletidae þ Palaeorhiza papuana (males only) (Michener, 1965)

Andrenidae þ Oxaeidae, Andrena (Iomelissa ) violae (Michener, 1944), A. (Charitandrena ) hattorfiana,

A. (Taenandrena ) lathyri

Melittidae þ Pseudophilanthus tsavoensis (Michener, 1981, as Agemmonia )

a Incorrectly given as labial palpi in Laroca et al. (1989).


parts. These parts of the labiomaxillary complex involve the

basal section (cardo, hypopharynx, labrum), the mid-section

(stipes, subgalea, laciniae, prementum) and not merely the

apical section (glossa, paraglossa, labial and maxillary

palpi, postpalpal galea). The short-tongued mouthparts are

thus well developed compared to the plesiomorphic small

proboscis. The principles of proboscis extension, retraction

and formation of the food canal are similar to those of the

plesiomorphic small proboscis, however, morphological

differentiation may occur in the postmental region (Plant

and Paulus, 1987), shape of the glossa, articulation of the

base of the glossa, and a reduction in the relative length and

function of the maxillary and labial palpi.

An elongate proboscis may be defined, as in the

Megachilidae and Apidae, when the glossa exceeds the

length of the prementum (Harder, 1983). An apical

elongation can occur by other structures as well. Essential

for the discussion here is when these lengthenings

necessitate the addition of new construction designs and

morphological innovations with respect to food canal

formation, storage of elongated parts, mechanisms of

extension and retraction, etc.

Jervis (1998) and Jervis and Vilhelmsen (2000) docu-

mented eight types of mouthpart elongations in Hymeno-

ptera for the uptake of nectar from flowers with long,

narrow, tubular corollas and referred to them as CNEA

(concealed nectar extraction apparatus). Briefly stated, these

are: (1) glossa and galea elongate, (2) glossa elongate and

galea only moderately elongate, (3) glossa, galea and

maxillary palpi elongate, (4) glossa, galea and labial palpi

elongate, (5) maxillary palpi elongate, (6) glossa and labial

palpi elongate, (7) maxillary and labial palpi elongate, (8)

prementum and stipes elongate. These types were intended

to account for the surprising variation found in various

groups of symphytans and parasitoid Apocrita.

We list in Table 3 those structures which partake in the

elongation of the apical food canal for various bees and

other aculeate Hymenoptera. Some of these examples

correspond to CNEA types of Jervis (1998) and are

indicated in the table, others would constitute new types

of CNEA, e.g. the mouthpart elongation of the higher

Masarinae, since it is achieved only by the glossa.

It can be seen that major aspects of the functional

morphology between the plesiomorphic small mouthparts

and the apomorphic short-tongued condition are similar. We

seek to underscore the functional–morphological differ-

ences between short-tongued and elongated proboscides and

to point out the morphological consequences of elongation,

rather than to emphasize the lengths of the different parts.

Thus we would not include in Jervis’ (1998) CNEA type 1

most of those flower visiting bees and wasps with

mouthparts that have undergone a slight or moderate or

short elongation. These forms correspond to our group 2,

apomorphic short. A short-tongued condition probably

represents the evolutionary starting point for further

modification by elongation.

Furthermore, the mouthpart condition found in typical

short-tongued bees such as Hylaeus, Colletes, Andrena and

Melitta, does not generally permit these insects to utilize

concealed nectar sources. The basal taxa of the Masarinae

with short mouthparts are likewise restricted to plant species

with easily accessible, actinomorphic flowers, e.g. Prisco-

masaris on Molluginaceae and Aizoaceae (Gess 2001),

Paragia on Myrtaceae, Proteaceae, Mimosaceae and

Bromeliaceae (Houston, 1984, 1986; Snelling, 1986; Gess,

1996). Our field observations on flower visiting behavior

confirm that species of Ceramius with elongate mouthparts

are able to utilize derived flower types with concealed

nectaries (e.g. Fabaceae, Lamiaceae, Pontederiaceae;

reviewed by Gess and Gess (1989), Gess (1996), Mauss

(1996), Mauss and Muller (2000) and Garcete-Barrett and

Carpenter (2000)) while the relatively short-tongued

Ceramius fonscolombei visits flowers with readily access-

ible nectar.

The morphology of the proboscis and its mechanisms of

extension in Ceramius permit a rapid exploitation of flowers

with very narrow corolla tubes. Pollen wasps can extend

their proboscis into a narrow corolla tube after landing on

the flower since the glossa is propelled forward from the

looped resting position. In contrast, the long proboscis of

bees requires more space to swivel out and unfold into the

feeding position. Many long-tongued bees must unfold their

proboscis before insertion into flowers and those with a

particularly long proboscis, such as euglossids and Antho-

phora, hover in front of blossoms and approach flowers with

an extended proboscis.

Based on the proposed phylogeny and biogeographic

pattern of the pollen wasps it is possible to roughly estimate

when the evolution from licking/sucking mouthparts to a

pure suctorial proboscis should have occurred (Fig. 20). The

basal subfamilies of the Vespidae, including the Masarinae,

appear to have become established in the early to middle

Cretaceous (Grimaldi, 1999). The basal-most group of

pollen wasps, Gayellini, is limited to the Neotropics. The

Masarini, however, represent a typical disjunct Gondwanan

distribution with the Paragiina endemic in the Australian

region and Masarina restricted to the remaining areas (Gess,

1992; Carpenter, 1993). In addition, most genera of

Masarinae are highly endemic to continental areas. The

diversification of pollen wasps probably thus took place

after the middle of the Cretaceous and coincided with the

diversification of angiosperms (Crane, 1993; Grimaldi,

1999). The independent evolution of an elongated proboscis

in the stem-groups of the subtribe Masarina and Meta-

paragia (Paragiina) must have occurred after separation of

the Australian land mass in the middle Cretaceous, about

100 million years ago (Fukarek, 1995).

Acknowledgements

We are especially grateful to J. Carpenter (New York)


and F. Gess and S. Gess (Grahamstown) who kindly

collected some of the investigated material for us and to

L. Castro (Teruel) for his extraordinary hospitality and

indispensable support of V. Mauss during the field studies.

M. Lopez (Diputacion General de Aragon) kindly issued

the required collection permits. We thank U. Hannappel,

C. Wirkner and A. Pernstich for technical assistance,

T. Osten for valuable comments on the manuscript, and

the Oberosterreichische Landesmuseum—Biologiezentrum

Linz for making available papers of the Fritz Schremmer

collection. Parts of the work were supported by the Austrian

Science Fund (Project 13944 Bio).

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Evolution of the suctorial proboscis in pollen wasps (Masarinae