the structure of the mouthparts of syrphid larvae (diptera) in relation to feeding habits

The Structure of the Mouthparts of Syrphid larvae (Diptera) in Relation to Feeding Habits Michael J. Roberts Department of Biology,

University of Salford, England (Received July 7, 1969)

Abstract The anatomy of the head is described for three species of syrphid larvae of differing feeding habits and the relation of the structure to the function is shown.

The degree of adaptation of both the musculature and the skeletal parts of the cephalopharynx to the type of food which the larva partakes is discussed. The mouthparts are discussed in detail and the probable course by which the complex mandibular lobes of aquatic, filter-feeding syrphid larvae were evolved, is pointed out.

Despite the economic importance of the Diptera, little work has been published on the functional anatomy of dipteran larvae in relation to feeding. A study has been made by the author to compare this aspect in brachyceran and cyclorrhaphan larvae and the present paper deals with the aschizan family, the Syrphidae.

Aschizan larvae, as a whole, are more neglected than other groups of cyclorrhaphan larvae and the little work which does relate to them is often taxonomic. The mouthparts of a variety of syrphid larvae are described by Kruger (1926) and Bhatia (1939), whilst Hartley (1963) desoribes the morphology of the cephalopharynx in some syrphids and its mode of functioning in the filter-feeder, Erist- a h . Hartley attempts to prove that the latter has a primitive cephalopharynx and to derive other types from it.

Observations on the structure of the cephalopharynx in the filter-feeder Mya- thropa do not accord with those of Hartley

(1963) on Eri~talis. Examination of other types, such as Eumerus, supports the view that Eristalis and Myathropa are, in fact, highly specialised and other types cannot be derived from them.

Materials and Methods For histological sections, Carnoy-Lebrun fixed material was embedded in paraffin wax, usually after double embedding in celloidin-methyl benzoate solution. Serial sections were cut between 6 and 24 p and stained with Ehrlich's haematoxylin and eosin or with Mallory Triple. The latter stain is particularly useful for a functional study as it distinguishes between flexible and inflexible cuticle.

Much of the morphology was studied by dissection, however, and dissected material was stained with methylene blue, then counterstained with acid fuchsin. Some dissections were carried out under glycerol, xylol or concentrated caustic potash.

Acta Zoologica 1970, 51, 43-65

44. Michael J . Roberts

Fig. 1. Lateral view of the larva of Eumerus strigatus Fall. AMSO, antenno-maxillary sense organ; AS, anterior spiracle; TT, respiratory tube.

Feeding was observed under a dissecting microscope at a magnification of X50 or x 100.

Observations

Larvae of the Lesser Bulb Fly, Eumerus strigatus Fallen, are found in bulbs such as Narcissus.

The mature larva (Fig. 1) has a length of approximately 11 mm and a breadth of 3 mm. It is somewhat flattened dorso- ventrally and tapers to rounded ends. The whitish cuticle is fairly thick and opaque. E. strigatus possesses a short respiratory tube (TT) formed from fused posterior spiracles, which is only about twice as long as it is wide. The eighth abdominal segment bears three pairs of small lappets.

The abdominal and thoracic segments bear no prolegs but there are prominent groups of spinules on small papillae along the length of the larva. The antenno- maxillary sense organs (AMSO) are short and the mandibular lobes external and obvious.

Cephalopharynx The head of E . strigatus is completely retracted into the thorax, is somewhat reduced and has a different appearance

to that of a primitive brachyceran larva such as Rhagio scolopaceus (L.) (Roberts 1969). The modified cranium and tentorium, together with invaginations of the foregut, form a structure known as the cephalopharynx, cephalopharyngeal apparatus or buccopharyngeal armature.

Mandibles and mandibular lobes (Figs. 2, 3 & 14)

In Eumerus the mouthparts consist of a pair of heavily sclerotised h o d s fused to sclerotised bases as they do in many saprophagous cyclorrhaphan larvae, including Calliphora (Roberts, in preparation). The hook (MDH) is stout and curves slightly downwards and outwards. Along its ventral edge five or six short, blunt teeth are arranged. This adaptation occurs in saprophagous and phytophagous larvae. The short mandibular base (MDB) curves up- wards from the shaft of the hook and is fused with the lbase of the other mandible along their dorsal edges and the hooks, therefore, work in unison. Each base has a lateral triangular depression which com- municates with the lumen of the hook, and a long sclerotised spur (MDS) which branches off from the posterior edge almost at right angles to the base. Besides collecting food, the mandibles also support the mandibular lobes.

The primitive type of cyclorrhaphan mandible would seem to be of the type

Mouthparts of Syrphid Larvae 45

4

M P-

N

APMD ' I AeMD

Fig. 2. Lateral view of the cephalopharynx of Eurnerus to show the musculature. - A, antenna; ABMD, abductor muscle of the mandible; ADMD, adductor muscle of the mandible; CDM, cibarial dilator muscle; CF, clypeal phragma; DHP, dorsal head protractor muscle; HR, head retractor muscle; LR, labrum; MDH, mandibular hook; MDS, mandibular spur; ML, mandibular lobe; MP, maxillary palp; PCM, pharyngeal constrictor muscle; PRM, pestle retractor muscle; SGL, salivary gland; T, tentorium; TA, anterior ' tentorial arm; TR, posterior tentorial rod; VHP, ventral head protractor muscle.

retained by Calliphora and is a hollow, curved mandibular hook fused to a large mandibular base, which can be fairly easily derived from the rhagionid maxillo- mandible descri~bbed by Roberts ( 1969).

In the saprophagous cyclorrhaphan larvae, which have this type of mandibular hook, the mandibular lobe is unattached

HR DWP CF I /

-PCM

'PRM

to the mandible. The mandibular lobe is here a cuticular development of the lateral borders of the prestomum which bears ridges similar to the spines which usually ornament each body segment.

In Eumerus, the mandibular lobes are better developed and are attached to the mandibular abase. They are strongly con- cave and have pronounced ridges which converge on the prestomum and terminate at the supporting spur of the mandible. Each of the ridges bears a fringe of long, sclerotised spines which are directed towards the mouth and help conduct the food into the atrium.

Both the mandibular abductor (ABMD) and adductor (ADMD) muscles originate on the posterior tentorial rods and are in-

46 Michael I . Roberts

MP

Fig. 3. Median sagittal view of the cephalopharynx of Eumerus to show the cibarial musculature. - ADM, atrial dilator muscle; AT, atrium; AV, atrial valve; CDM, cibarial dilator muscle; CR, cibarial ridge; FG, frontal ganglion; FN, frontal nerve; FR, fused plate of cibarial filter; LRSO, labral sense organ; M, pharyngeal mortar; MD, mandible; ML, mandibular lobe; PCM, pharyngeal constrictor muscle; PE, pharyngeal pestle; PPM, pestle protractor muscle; PRM, pestle retractor muscle; PSM, pharyngeal suspensory muscle; RN, recurrent nerve; SD, salivary duct; VC, ventral channel.

serted on the dorsal edge of the mandibular base and on its spur, respectively.

Basal sclerite (Fig. 2 ) The term basal sclerite, in Eumerus, refers to all the cephalopharyngea1 skeleton ex- cept the mouthparts.

Basically, the sclerite encloses and supports a cibariopharyngeal sucking pump and it is roughly conical in shape. The sclerite is composed mainly of unpigment- ed, lightly sclerotised cuticle but, in places, it is strengthened by areas of heavy sclerotisation. A narrow emargination from the posterior edge splits the dorsal surface of

VC

the sclerite into a pair of clypeal or clypeo- frontal phragmata (CF), whilst wide lateral emarginations of the sclerite form dorsal and ventral wings from side view. A pair of arms of the ventral wings, or cibarial phragmata, support the transverse pestle-retaining muscles (PCM) which are described below.

The tentorium and the labrum contrib- ute sclerotised elements to the basal sclerite, the labrum forming a bridge (LR) between the clypeal phragmata. The tentorium (T) comprises large lateral areas of the sclerite and a pair of posterior tentorid rods (TR) brace the sclerite against the contraction of the mandibular muscles as they do in Rhagio and Sargus bipunctatus Scopoli larvae (Roberts 1969). In Eumerus the tentorial rods are fused to the cibarial phragmata as they are in Sargus. A pair of anterior tentorial arms (TA) provide the point of articulation for the mandibles, and are joined ventrally by a sclerotised bar which is anterior to the opening of the salivary duct into the f oregut.

Mouthpart>of Syrphid Larvae 47

VC

Fig. 4. Diagram of a transverse section of the posterior half of the cibarium in Eumerus and Myathropa. - DC, dorsal chamber; RC, cibarial roof; VC, ventral channel.

The cephalopharynx is protracted by a pair of dorsal and a pair of ventral head protractor muscles which originate on the anterior walls of the prothorax. The dorsal protractor muscles (DHP) insert on the posterior edge of the clypeal phragmata, whilst the ventral muscles (VHP) insert on the tentorial rods posterior to the mandibular muscles. Several pairs of head retractor muscles (HR) insert on the anterior atrial regions of the cephalopharynx and originate on the posterior walls of the prothorax.

Foregut (Fig. 3) The part of the gut enclosed by the cephalopharynx comprises, anteriorly, the atrium followed by the cibarium and the pharynx.

The roof of the atrium (AT) is formed by the flat, lightly-sclerotised epipharyngeal plate, which also bears the labral sense organs (LRSO), whilst the floor is partly formed by the labium. The salivary duct (SD) opens into the atrial lumen and the cuticle of the posterior edge of the salivary duct opening is produced forward to form a valve-like flap which probably prevents the entry of food into the salivary duct. The atrium is dilated by four pairs of

atrial dilator muscles (ADM) which insert on the epipharyngeal plate and, as these originate on the labral part of the basal sclerite, they could also be termed labral compressor muscles.

The cibarium is considerably larger than the atrium and has a thick flexible roof which stains blue in Mallory Triple. The posterior half of the floor of the cibarium is invaginated to form nine longitudinal ridges (CR). Each of the centre ridges bears two rows of filaments arranged at approximately 45 O to the vertical (Fig. 4) , and touching the row of filaments of the neighbouring ridge, with the result that the ridges appear Y-shaped in cross-section. The two outer ridges have but a single row of filaments and, thus, eight longitudinal channels (VC) are enclosed by the ridges. Whilst increased fluid pressure in the ventral channels will cause the filaments to move apart, an increase in pressure in the dorsal chamber will press them together and, therefore, the filter withstands pressure from above. Anterioxly the ridges terminate and the filaments are fused to form a solid sheet of cuticle (FR) which, thus, encloses a single ventral channel. A thin flap of cuticle (AV) which hangs from the atrial roof and rests on the sheet forms an atrial valve to the cibarium. The cibarium is dilated by a series of fifteen pairs of cibarial dilator muscles (CDM) which insert m its roof and originate on the clypeal phragmata.

The pharynx is nearly at right angles to the cibarium and both the roof and the floor are heavily sclerotised. The floor is the larger of the two structures and forms a mortar (M) whilst the grooved roof forms the pestle (PE) of a grinding mill. The pestle is held firmly against the mortar by a pair of large transverse constrictor muscles (PCM), which originate on the arms of the cibarial phragmata, described

48 Michael J . Roberts

previously. The pestle is protracted by three pairs of large muscles (PPM) which insert at its base, near to its junction with the cibarium, and retracted by four pairs of large muscles (PRM) which insert on a wing of the pestle and originate anteriorly on the clypeal phragmata. Retraction is probably also assisted )by one or two pairs of slender pestle suspensory muscles (PSM) which insert at the top of the pestle.

Feeding The Eumerus larvae used in the present study were only found in decayed bulbs of, for example, Narcissus where they were frequently extremely numerous in all stages of development whilst the larvae were completely absent in adjacent healthy bulbs. Martin (1934) postulated and later Creager and Spruijt (1935) confirmed, that the larvae of E. tuberculatus Rondani must feed on the fungus of basal rot in order to develop normally. The larvae may initiate infection by carrying fungal spores on the cuticle or in the atrium but, whether or not this is the case, they are probably mycetophagous or saprophagous and not phytophagous. This is also the opinion of Stone et al. (1965) who state that “The species (of Eumerus) are probably all associated with decaying plant tissue, and their feeding on healthy plants is ques- tionable”. This view is supported by the presence of a pronounced cibarial filter in the larvae of E. strigatus and E. tuberculatus. Keilin (1915) found that cibarial ridges are invariably present in ‘saprophagous’ cyclorrhaphan larvae and are absent in biontophagous larvae, that is those feeding on living plant or animal tissue but not microorganisms such as bacteria.

The mandibular hooks collect the food whilst the cibarial sucking pump ingests it.

The mandibles are fused to each other and, therefore, act together. Contraction of the mandibular abductor and adductor muscles causes raking movements of the toothed mandibular hooks which loosens surrounding semi-liquid food and pushes it, during adduction, towards the mouth. The abducted mandibles are thrust into the food by contraction of the head protractor muscles whilst adduction of the mandibles is assisted by contraction of the head retractor muscles. The plant material has already been made semi-liquid by bacterial digestion but may also undergo further digestion by the larva before it enters the mouth. Since the mandibular lobes are attached to the mandibles, they move with the latter and the spines of their ridges assist in pushing food towards the mouth whilst the channels enable conduc- tion of fluid.

Contraction of the atrial dilator muscles raises the epipharyngeal plate and sucks food into the atrial cavity. This dilation probably also draws saliva from the salivary duct into the atrium where it mixes with the food.

Contraction of the atrial muscles i followed by contraction of the cibarial muscles and the flexible roof of the cibarium is elevated to form a large dorsal chamber into which the food and saliva is sucked, raising the backwardly-directed atrial valve. Some food is sucked into the ventral channels but this is small compared with that in the dorsal chamber because the ventral channels are not dilatable. The food has now to be concentrated and ex- cess water expelled. This is brought about by contraction of the large cibarial constrictor muscles (cf. Fig. 12) which pull the cibarial phragmata together and de- press the cibarial roof. The increased fluid pressure in the dorsal chamber causes the atrial valve to be held against the anterior


5mm

AMSO

ridge plate and prevents escape of material in this direction. Water is forced through the filaments of the cibarial filter into the ventral channels and is egested by way of the atrium.

A wave of peristalsis passes the particles retained on the filter back to the pharynx where they are ground between the pestle and mortar before passing into the oesophagus. Grinding movements are perform- ed by contraction of the protractor and retractor muscles of the pestle described above.

The larvae of Myathropa florea inhabit rot-holes of the beech tree Fagus syluestris, and their biology is briefly summarised by Hartley ( 196 1 ) . The shallow rot-holes

Fig.' 5. Lateral view of the larva of M y ~ t h ~ o p ~ florea (L). - AMSO, antenno-maxillary sense organs; AS, anterior spiracle; PD, pseudopod or proleg; TT, telescopic respiratory tube.

which they inhabit rarely contain more than eight inches of water and become partially filled with an accumulation of rotting leaves and compost.

The larva (Fig. 5 ) has a thin, unpig- mented cuticle, through which many of the internal organs are visible, and is roughly cylindrical with a truncated anterior end. When fully grown the body has a length of approximately 22 mm and a width of 5 mm. The water of the rot-hole is stagnant and virtually oxygen-free but the larvae obtain oxygen by the possession of a telescopic respiratory tube (TT) which extends to eleven inches long in exceptional specimens (Coe 1953). The

4-Acta 2001. 1970: 1-2


M R

Fig. 6 . Atrial view of left mandibular lobe of Myathropa. - ML, mandibular lobe; MR, ridges of lobe; MRP, prongs of ridges: P, prestomum.

eighth abdominal segment is produced to form an ‘eristaline’ tail which protects the respiratory tube.

The thorax and each of the first six abdominal segments bears a pair of well- developed prolegs (PD). Those of the abdominal segments bear two semicircular rows of long recurved spines or crochets, whilst the thoracic prolegs bear a single row, with several rows of accessory crochets.

The larva is morphologically amphip- neustic, as in Eumeruj, but the small an-

terior spiracles (AS) are probably only used fomr exhalation of air.

Cephalopharynx The cephalopharynx is retracted further than that of Eumerus with the result that the mandibles and mandibular lobes have been drawn into the thorax.

Mandibles and mandibular lobes (Figs. 6, 7 & 8) The mandibles of Myathropa are very reduced and are represented only by a pair of C-shaped sclerites which support the mandibular lobes. The lobes, however, no longer merely channel food towards the


mouth, as they do in Eumerus, but are also used as a coarse filter to prevent the entry of excessively large particles.

The mandibular lobes are a pair of obloid, hemispherical cuticular shells, each strengthened peripherally by the C-shaped mandibular sclerite. The lobes are con- tiguous along their dorsal edges but are separated by a fleshy median labial lobe (LL) along their sides. Each mandibular lobe is invaginated to form pronounced internal ridges (MR) which radiate posteriorly from the prestomum. At their posterior ends, the ridges break away from the shell, forming prongs which curve into the centre of the lobe (Figs. 6 & 7, MRP). The combined effect of all these prongs is of the spokes of a wheel radiating in from the rim. Since the two hemispherical lobes are not completely ap-

Fig. 7. Diagrammatic oral view of ridges of mandibular lobe in Myathropa. - MR, ridges of lobe; MRB, bristles on ridges.

posed there is a large gap between the prongs of one lobe and those of the other. This is filled by the labial lobe.

Each ridge bears a fringe of bristles along its edge which is arranged perpendic- ular to the plane of the ridge (Figs. 6 & 7, MRB). The bristles form a comb which touches the ridge below, and, since the comb is continued along the leading edge of each prong, it filters all liquid passing into the atrium. The bristles are approximately 4 ,u apart and form a much coarser filter than the cibarial apparatus.

Thus the lobes of Myathropa differ from those of Eumerus only in that they are involuted with further retraction of the head into the thorax, and that the ridges


MXN

\

I / l m m PD

" ' I \ A ~ M D

I ADMD SD

Fig. 8. Lateral view of the cephalopharynx of Myathropa to show the musculature with left hand side of nervous system removed. - A, antenna; ABMD, mandibular abductor muscle; ADMD, mandibular adductor muscle; AN, antennal nerve; CDM, cibarial dilator muscle; CF, clypeal phragma; CP, cibarial phragma; DHP, dorsal head protractor muscle; HR, head retractor muscle; LN, labial nerve; LR, labrum; ML, mandibular lobe; MLN, maxillo-labial nerve; MP, maxillary palp; MSO, maxillary sense organ; MXN, maxillary nerve; OD, optic depression; PD, proleg; SD, salivary duct; SGL, salivary gland; T, tentorium; TA, anterior tentorial arm; TP, tentorial phragma; TS, spur of tentorium; VHP, ventral head protractor muscle.

break away from the lobe at their posterior ends to form a 'lobster pot' filter.

Glbmac (1960) and Hartley (1961) have shown that the Narcissus Bulb Fly, Merodon equestris (Fabricius), is closely related to Eumerus and Hartley (1963) describes the mandibular base of Merodon as being more heavily sclerotised than that

of Eumerus, no spur being distinguishable, whilst he implies that the mandibular lobes are reduced. I t would seem that with increase in the use of the mandibular lobe, the mandible itself becomes of less importance and, in Myathropa, it is reduced to the role of supporting the mandibular lobes.

Both the mandibular abductor and adductor muscles consist of two pairs of small muscle blocks which originate on the posterior rod of the tentorium. The abductor muscle blocks insert dorsally on the mandibular sclerite whilst the adductor muscles insert postero-ventrally.

The mandibular lobes may be closed by increased haemocoelic blood pressure, as a slight pressure applied to the. abdomen of a fresh specimen is sufficient to close them. The outside ,lateral walls of each lobe flex downwards so that the inside surface of


lmrn

each of these walls blocks the prestomum and is almost flush with the labial lobes. I t is not clear whether the animal uses this method itself or whether the mandibular abductor and adductor muscles could play some part in closure. Otherwise the weak mandibular muscles exert only a slight directional influence on the mandibular lobes through the intermediary of the mandibular sclerite.

Basal sclerite (Fig. 8 ) The basal sclerite of Myathropa is similar to that of Eumerus but differs most notice- ably in the region of the cibarial phragmata. There is no grinding mill and, therefore, supporting structures are absent, but the cibarial phragmata are proportionately much larger and form a long boat-shaped trough. The areas of cranial origin are confined to the anterior one-third of the basal sclerite.

The clypeal phragmata (CF) itre small and each lateral wall of the sclerite is braced by the postero-ventrally directed mainstay of the tentorium which terminates in a short tentorial rod or bar.

Fig. 9. Median sagittal view of the cephalopharynx of MyathroPa to show the cibarial musculature. - ADM, atrial dilator muscle; AT, atrium; AV, atrial valve; C, cibarium; CCM, cibarial constrictor muscle; CDM, cibarial dilator muscle; CR, cibarial ridge; ES, epipharynge- a1 sclerite; FG, frontal ganglion; FN, frontal nerve; LIC, labial cushion; LN, labial nerve; LRN, labral nerve; LRSO, labral sense organ; LSO, labial chemoreceptor sense organ; LTS, labial tactile sense organ; MD, mandible; MR, mandibular ridge; MXN, maxillary nerve; 0, oesophagus; PCM, pharyngeal constrictor muscle; PDM, pharyngeal dilator muscle; PV, pharyngeal valve; RN, recurrent nerve; SD, salivary duct; VC, ventral channel.

There is a short anterior spur (TS) from the base of the tentorium which forms the ventral edge of the tentorial phragmata (TP) and the anterior tentorial arms (TA) which articulate with the mandibles are very thin and slender in Myathropa. This reflects the reduced movement which is Rquired of the mandibles.

Anteriorly, each tentorial phragma bears a sub-circular depression (OD) on its outer surface which forms a dark background for the photoreceptor organ.

In Myathropa, the head protractor and


retractor muscles are much less well developed than those of Eumerus. The retractor muscles (HR) consist of a pair of slender muscles which insert on the atrial wall and originate on the posterior dorsal wall of the prothorax whilst the dorsal head protractor muscles (DHP) are equally slender and insert on the posterior edge of the clypeal phragmata. These two sets of muscles are probably relegated to suspen- sion of the cephalopharynx. The two pairs of ventral protractor muscles (VHP) are larger and insert behind the point of origin of the mandibular muscles on the tentorial phragmata.

Foregut (Fig. 9) In addition to the elements of gut present in Eumerus, Myathropa has the mandibular lobe cavity caused by further retraction of the head into the thorax and this is the first part of the foregut.

Whilst the roof of the mandibular lobe cavity is formed by the lobes themselves, the floor is formed by the labial lobe. An- tero-dorsally the hollow labial lobe bears a pair of cushions (LIC), each a mass of fleshy, sausage-like protuberances which stain blue in Mallory Triple and are, therefore, soft and flexible. The labium bears two pairs of sense organs, one pair above and one pair below the labial cushions. The apparently undescribed pair below the cushions are finger-like tactile sense organs (LTS) which protrude into the mandibular lobes near to the prestomum, and terminate in a long hair. Above the cushions, a pair of chemoreceptor labial organs (LSO) are present in the floor of the atrium, just anterior to the opening of the salivary duct. As in Eumerus, the posterior edge of the salivary duct forms a valve-like flap to prevent the entry of food but this is less pronounced. As in Eumerus, the roof

of the atrium is formed by the epipharyngeal plate (ES) and the atrium is dilated by four pairs of atrial dilator muscles (ADM) which insert on the plate.

The cibarial floor forms a long boat- shaped trough and bears nine longitudinal ridges (CR), as in Eumerus, but these extend the 1,ength of the cibarium and do not appear to be fused anteriorly. The hanging valve (AV) is fringed by a brush of bristles which rest on the cibarial filter, when the valve is in closed position, and ensure that any gaps, which the Y-shaped of the cibarial ridges and their filaments would cause with an unfringed valve, are obliterated. The cibarium is dilated by the contraction of about twenty pairs of cibarial dilator muscles (CDM) which insert on thin, flexible cibarial roof. As the clypeal phragmata, on which the muscles originate, constitutes only a small anterior part of the cephalopharynx, the flat cibarial dilator blocks slope diagonally, almost horizontally, forward. They tend to produce a maximum dilation at the posterior end because a majority of the muscles insert on the posterior part of the cibarial roof and because the roof is flexible. The cibarium can be subjected to powerful constriction by the two layers of constrictor muscles (CCM) which originate on the large cibarial phragmata. Dorsally, a large median cibarial Fnstric- tor muscle (Fig. 10, DCM) is attached broadly to the cibarial phragmata (CP) . Below this a pair of constrictor muscles [VCM) each originate near the anterior end of the cibarial phragmata and run diagonally across the space between the phragmata to insert on a plication of the posterior end of the opposite cibarial phragma. These muscles have a fused junction where they cross. Contraction of the constrictor muscles brings the cibarial phragmata closer together and forces the


PCM VCM

0 , , . . . .

- PDM

0-5mm

cibarial roof down, thus constricting the cibarial lumen.

There is no grinding mill in Myathropa, and the pharynx is represented by a small region of sclerotised roof, which stains red in Mallory Triple, between the cibarium and the oesophagus. This functions as a pharyngeal valve which is opened by the contraction of a pair of pharyngeal dilator muscles (PDM) and closed by contraction of a pair of pharyngeal constrictor muscles (PCM) .

Nervous System of the Head

(Figs. 8 & 9)

The larva of Myathropa is much larger than of Eumerus and therefore more suit- able for the dissection of the nervous system.

The central nervous system of the Mya- thropa comprises a pair of spherical cephalic ganglia which surmount the oesophagus and are connected by a short supraoeso- phageal commissure, and an elongate ventral ganglion which is ventral to the oesophagus and is connected to the cephalic ganglia by the circumoesophageal com- missures. This contrasts with the primitive- ly spaced ganglia of the brachyceran,

I PE M

Fig. 10. Dorsal view of the cephalopharynx of Myathropa, pharyngeal dilator and constrictor muscles cut. - CDM, cibarial dilator muscles; CF, clypeal phragma; CP, cibarial phragma; DCM, dorsal cibarial constrictor muscle; 0, oesophagus; PCM, pharyngeal constrictor muscle; PDM, pharyngeal dilator muscle; VCM, ventral cibarial constrictor muscle.

Rhagio scolopaceus (Roberts, in press) , and the ventral ganglion of Myathropa repre- sents the fusion of the suboesophageal, thoracic and abdominal ganglia of more primitive insects.

Cephalic imaginal rudiments cover the anterior surface of the cephalic ganglia and are connected to the clypeal sclerites by the membrane which encloses them. The short optic stalks connect the imaginal eye discs to the cephalic ganglia.

The optic nerves enter each cephalic ganglion along the optic stalk and supply the globular photoreceptors which are situated in the optic depressions of the basal sclerite. The dark background neces- sary for directional reception of light is provided externally to the eye, by the heavily sclerotised optic repressions and this contrasts with the more primitive type of eye in Rhagio (Roberts, in press).

Below the optic nerves, the anten- nolabral nerves issue from the cephalic


ganglia. These each give off a branch to the frontal ganglion, the frontal con- nective, and then split up into the labral and antennal branches. The latter (AN) supplies the large bulb of the antennal sense organ (A), whilst the former enters the cephalopharynx at the anterior end of its lateral emargination to supply the labral sense organs lying on the epipharyngeal plate (Fig. 9, LRSO).

The most dorsal nerve of the ventral ganglion is the maxilldabial nerve (MLN) which bifurcates near its anterior end to give the maxillary palp sense organ (MP) below the antenna and gives off a branch to the maxillary sense organ (MSO) situated anterior to the mandibular lobe. The labial nerve (Fig. 9, LN) terminates in branches which supply the tactile labial sense organ (LTS) and the chemoreceptor labial sense organ (LSO) . The mandibular muscles appear to be in- nervated by a nerve which originates on the dorso-lateral wall of the ventral ganglion.

Below the maxillo-labial nerve, a pair of nerves issue from the ventral side of the ventral ganglion to each segment of the thorax and abdomen. There is also an accessory nerve for each abdominal segment from the dorsal surface of the ventral ganglion which bifurcates before reaching its segment.

Feeding

The rot-holes which the larva of Mya- thropa inhabits are filled with decaying leaves and the water contains abundant suspended organic matter and bacteria. The larva filters out the suspended particles but, in common with other filter- feeders, this feeding process necessitates both the effective concentration of food material and the ingestion and expulsion

of large quantitites of unwanted water. Whereas in aquatic stratiomyids, such as Stratiomys chamaeleon L. described by Schremmer (1951), the process of filtration is a one-way system with a special orifice for exhalent water, in Myathropa and other filter-feeding syrphids the water is exhaled, as it is ingested, through the mouth.

In Myathropa, the mandibles do not collect the food but support a strainer which prevents the entry of excessively large particles. Contraction of the atrial dilator muscles (Fig. l l a , ADM) draws water into the atrium and this has to pass between the posterior prongs of the mandibular combs in order to reach the atrium. Large particles are caught on the combs and since the bristles on each ridge are approximately 4 ,U apart, only particles less than 4 ,LA in size are allowed through. After initial straining, food material is concentrated by the cibarial filter in similar man- ner to that of Eumerus. Myathropa has to sift far larger quantities of fluid than Eumerus and, therefore, requires the apparatus to both ingest large quantities of liquid and to filter it.

The volume which the cibarium holds is a function of the amount of retraction of the cibarial roof and of its flexibility. The distance which the cibarial dilator muscles will contract, however, is, directly dependent on their length and is inde- pendent of their width or of the number of fibres in each muscle. Therefore, long muscles are required and the greatest length which can be achieved is when they are horizontal. Thus the small, sloping clypeal phragmata and the anterior point of origination of the dilator muscles are an adaptation which allows for a maximum length of muscle to the cibarial roof. The thin flexible cuticle of the roof allows it to ‘balloon’ up when the muscles contract


Fig. 11. Action of cephalopharynx during feed- dorsal chamber; ML, mandibular lobe; 0, ing of Myathro$a. - ADM, atrial dilator mus- oesophagus; PDM, pharyngeal dilator muscle; cles; AV, atrial valve; CCM, cibarial constrictor PV, pharyngeal valve; VC, ventral channel. muscles; CDM, cibarial dilator muscles; DC,


1

MO-

I VHP

Fig. 12. Lateral view of the cephalopharynx of Syrphus ribesii (L.) to show the musculature. - ABMD, mandibular abductor muscle; ADMD, mandibular adductor muscle; DHP, dorsal head protractor muscle; LIR, labial retractor muscle; LR, labrum; MD, mandible; SD, salivary duct; TA, anterior tentorial arm; TR, posterior tentorial rod; VHP, ventral head protractor muscle.

(Fig. llb, CDM) and create the largest possible volume in cibarial lumen.

For concentration of this volume, Myathropa needs large cibarial constrictor muscles. A large body of water has to be forced though a fine filter (Fig. l l c ) against the resistance of both the filter

itself and of the accumulating body of solid material on the filter. Therefore, it is unlikely that whilst the inhalent stroke requires the contraction of a large number of dilator muscles, the exhalent stroke should rely on the elasticity of the deform- able walls of the cibarium as Hartley (1963) has suggested for the larva of Eristalis tenax. He suggests that the powerful constrictor muscles merely alter the power of the stroke but this is not con- sistent with constriction being the work stroke of filtration or with the anatomy. Since the constrictor muscles are large,


the invaginations of the cibarium, or cibarial phragmata, are also large for the origination of these muscles. They extend further forward than in Eumerus and, therefore, the filter can extend further forward with the result that the area for filtration is increased.

The pharyngeal valve (PV) is kept closed by contraction of the pharyngeal constrictor muscles during filtration and filtration is probably repeated several times before the valve is opened, by contraction of the pharyngeal dilator muscles (Fig. l ld , PDM), and accumulated food particles are swept into the oesophagus by cibarial constriction.

This mechanism is supported by the observation that particles are only found on top of the filter in both transverse and longitudinal sections and in cleared whole mounts of the cephalopharynx.

Differing functions have been ascribed to the labial cushions by authors. Wilkin- son (1901) described them as ‘triturating organs’ and suggested that they ground food particles against the mandibular combs but, since the processes are soft and flexible, staining blue in Mallory, they could not have this function. Hartley (1963) states that the labial lobe dislodges particles caught on the combs and strains food particles. They are without muscles, however, in Myathropa, and could not reach the anterior part of the combs if they had muscles. Their soft structure seems to preclude the possibility of their being used as a filter.

Since Myathropa is a filter-feeder, it needs an ‘unclogging’ mechanism. When constriction of the cibarium (Fig. l l c ) forces water out from the dorsal chamber and forwards, the soft flexible mass of labial processes acts as a plug between the mandibular lobes and ensures that the exhalent stream of water passes through

the posterior spurs of the ridges. As a result, the particles collected by the combs will be dislodged and the filter ‘unclogged’. The flexibility and accomodating shape of the processes fills all the gaps when the labial lobe is pressed against the roofs of the mandibular lobes by increased haemocoelic fluid pressure.

The larva of Syrphus r ibei i is dorso-ventrally flattened, as in Eumerus, but tapers to a more pointed anterior end. When mature the larva is 14 mm long and 3 mm wide and the posterior spiracles are fused in the final instar to form a spiracular boss. The white or pinkish fat body is visible through the dorsal cuticle and forms a characteristic pattern depicted by Bhatia ( 1939). Unlike Myathropa or Eumerus, Syrphus is completely terrestrial and is normally found on mses, cabbages, fruit- bushes and other plants where colonies of aphids may be found.

Cephalopharynx

(Figs. 12 and 13)

The larvae are aphidophagous and the cephalopharynx has become completely adapted for piercing and sucking its prey.

The mandibles are reduced to a pair of thin stylets (MD) which lie lateral to the anterior end of the cephalopharynx and articulate about the anterior tentorium (TA) . The posterior part of the mandible is drawn out into a long apodeme on which the mandibular abductor muscles (ABMD) insert, whilst the adductor (ADMD) muscles insert near the anterior end of the mandibular stylet. Both the mandibular abductor and adductor muscles originate on the posterior tentorial rod (TR) and are small.

The basal sclerite tapers to a sharply


CPM

\ LRSO

C . I

Fig. 23. Median sagittal view of the cephalopharynx of Syrphus. - C, cibarium; CCM, cibarial constrictor muscle; CDM, cibarial dilator muscle; LIR, labial retractor muscle; LR, labrum; LRSO, labral sense organ; LS, labial sclerite; SD, salivary duct.

pointed anterior end. The prestomum is reinforced by V-shaped upper and lower sclerites formed from the labrum (LR) and labium (LS) respectively. These are the main piercing organs of the cephalopharynx and therefore the largest muscles of the latter are the head protractor muscles. The large dorsal (DHP) and ventral protractor muscles (VHP) insert on the clypeal and cibarial phragmata, respectively, and the sclerotisation of the posterior tentorial rods extends to the posterior edge of the cibarial phragmata. The labial sclerite articulates on the tentorium and is lowered by the labial retractor muscles (LIR) . These insert on apodemes midway along the length of the labial sclerite and originate on the posterior tentorial bars.

The foregut is straight and there is very little morphological differentiation between the atrium and the cibarium-

pharynx. The atrial dilator muscles are continuous with the cibarial dilator muscles and the muscles are so wide that each series virtually forms a solid sheet of muscle from the anterior end of the atrium to the posterior end of the cibarium. The dilator muscles (CDM) are followed by four cibarial constrictor muscles (CCM) which originate on the cibarial phragmata. The common salivary duct (SD) is very wide and opens into the posterior part of the atrium.

Feeding

Syrphus larvae adopt a trial and error method of finding their prey. They move at random over the leaves and branches, investigating anything that comes into con- tact with the head. If the object is an aphid, the prey is lifted into the air and sucked out before being discarded. The larva then searches the surrounding area intensively by striking out in all directions with the anterior end of the body. Thus the immediate vicinity becomes cleared of

Mouthparts of Syrphid Larvae 61,

aphids and the larva resorts to random movements over the leaf or branch again.

The aphid is usually struck on the dorsal surface of the abdomen, the mouthparts are pushed into the soft body of the prey and a copious flow of sticky saliva is poured over it. The prey is then lifted into the air and its struggling comes to no avail since the legs are held clear of the leaf. The cuticIe of the prey is retained by the lateral hooks, while vigorous protrac- tion and retraction of the cephalopharynx is used to remove all the soft parts of the prey’s body. The food is made liquid by extra-oral digestion and then sucked into the atrium and cibarium by contraction of the atrial and cibarial dilator muscles.

The sharply pointed mandibles have only a weak musculature, but probably have a scissor-like movement which may either slit the cuticle of the prey or assist disintegration of its flesh. Contraction of the labial retractor muscles probably keeps the prestomum open during ingestion of the food.

Discussion

The anatomy of the cephalopharynx in relation to it3 function

Each cephalopharynx is a complex of adaptations to the mode of feeding adopt- ed. Two examples which illustrate this degree of adaptation are the cibarial musculature and the shape of the tentorium.

The cibarial muscuIature has been discussed above. Where the food is diffuse and large volumes have to be ingested, as in Myathropa, the muscles have to be long and this is achieved by small anterior clypeal phragmata and, consequently, by nearly horizontal muscles. Where the food is concentrated and small volumes have to be ingested rapidly, as in Syrphus, the mus-

cles have to have a large cross-sectional area and need only a short length. Hence the clypeal phragmata are large and central in Syrphus and the muscles are roughly vertical. Eumerus shows an intermediate stage and its food is of intermediate nutri- tive value as it needs some filtering.

The sclerotised parts of the tentorium show a great variety of forms amongst the different genera and species of syrphid larvae but this variety is by no means either random or even a good guide to taxonomic relationships. These sclerotised areas serve as braces to counteract the pull of specific groups of muscles on the cephalopharynx. They are, therefore, dependent on the mode of feeding characteristic of the larva.

In Eumerus the main body of the tentorium is vertical, its ventral end inclined slightly in an anterior direction. This braces the cephalopharynx against the main body of muscles, the dilator muscles of the cibarium and atrium, and the pestle depressor muscles. These are all nearly vertical. The posterior tentorial bar is strong and originates midway along the tentorial body, inclining ventrally towards the posterior end. This counteracts de- formation due to the pull of the mandibular muscles, the ventral head protractor muscles, and the pestle elevator muscles. A strong anterior tentorial arm supports the articulation of the mandibular hooks which are used for collecting food.

In Myathropa, the cibarial muscles slope diagonally backwards and to counteract this the main body of the tentorium is situated much further back and is also diagonal. As in Eumerus, the tentorial rod, now continued as a spur anterior to the tentorial body, braces the tentorial phragmata against the mandibular and ventral head protractor muscles. The mandibles are no longer used for collecting food and

62 Michael J. Roberts

MD

Fig. 24. Comparison of mandibular lobes (a) ( c ) Myathropa florea. - MD, mandible; MDS, Calliphora uornitoria, (b) Eurnerus strigatus, spur of mandibular base; ML, mandibular lobe.


the anterior arm of the tentorium is very slender.

In Syrphus, the dilator muscles are very powerful and range from forwardly-sloping atrial dilator muscles to vertical cibarial dilator muscles so that it is not surprising that the tentorial body is very wide and strong and slopes forwards, ventrally. The head protractor muscles are also very large and, therefore, the posterior tentorial rod is wide and extends to the posterior end of the cibarial phragmata. As the labrum is the main piercing organ, a prominent feature of the tentorium is its strong fusion with the former whilst the anterior arm for articulation with the mandible is small.

Evolution of the mandibular lobes (Fig. 14) In nernatoceran, in brachyceran and also in cyclorrhaphan larvae, the primitive role of the mandibles is collecting food. In Myathropa they no longer have this function and only support the mandibular lobes, which are present to prevent the entry of large particles. Consequently they are very reduced and the mandibular hook, or collecting part of the mandible, is virtually absent, whilst the base is also very reduced.

The mandibles can only be easily derived from the primitive brachyceran mandibles of, for example, Rhagio (Roberts 1969) if they are hook-shaped and these are found in the phytophagous syrphids Cheilosia and Merodon described by Hart- ley (1963). The cephalopharynx of Chei- losia is comparatively simple and has neither a cibarial filter nor a grinding mill. Merodon has a grinding mill and is probably related to the mycetophage, Eumerus which has both a grinding mill and a cibarial filter. The mandible of the semiaquatic Eumerus shows an interesting intermediate condition between the prim-

itive well-developed hooks of, for example Calliphora (Fig. 14a) which is also semiaquatic, with unattached, exocuticular lobes, and the reduced mandibular sclerites of the aquatic Myathropa (Fig. 14c) which support complex mandibular lobe structures. The mandible of Eumerus (Fig. 14b) is used both for collecting food and for supporting the mandibular lobe. This suggests the most probable type through which the complex structures of Mya- thropa were evolved.

Hartley (1963) states that the mandibular lobes of the filter feeding larvae are the most primitive, and that “it is fairly easy to derive the other forms of cephalop- pharyngeal apparatus from the saphrop- hagous type but the reverse is not so”. He does not suggest how the ‘primitive’, but complex, mandibular lobes of Eristalis might have evolved, however, and his argument does not appear conclusive. Hartley (1961, 1963) also suggests that the long eristaline respiratory tail is primitive. I t would seem m a e likely that both the mandibular lobes and the tail were developed by degrees. Hull (1949) suggests that an ancestral syrphid larva was saprophagous in dung or compost and a short breathing tube aided survival in a moist habitat. This assisted subsequent radiation into aquatic and other habitats, and the development of the breathing tube followed. The mandibular lobes probably also evolved gradually as suggested above.

The carnivorous syrphine larvae, such as Syrphus, are likewise generally thought to have developed from phytophagous an- cestors (Hamrum 1966, Chandler 1968) and the mandibles of Syrphus are as modified at those of Myathropa, even if they are modified in a different fashion.

The aphidophagous larvae and to a lesser extent, the filter-feeding larvae are very diverse and are, therefore, particularly suc-


cessful adaptations of the primitive type. Therefore, not only in the Stratiomyidae (Roberts 1969), but also in the Syrphidae filter-feeding is a higly specialised offshoot.

Summary Eumerus strigatus larvae are found in rot- ten bulbs and are, therefore, semiaquatic. The toothed mandibles are used for collecting food but also support the mandibular lobes, and are slightly reduced. The cibarium has both a cibarial filter and a grinding mill, and the larva is mycetophagous and saprohagous but probably does not feed on living plant tissue.

Myathropa florea larvae inhabit beech rot-holes and are aquatic. The larvae are well adapted to filter-feeding. The mandibles are reduced to C-shaped sclerites which support complex mandibular lobes and these prevent the entry of particles which are too large. The cibarium has a well developed filter which traps bacteria and small particles of detritus.

Syrphus ribesii larvae are terrestrial and are found on roses, fruit-bushes and other plants. The larvae are aphidophagous and the cephalopharynx is adapted for piercing and sucking its prey. The labrum and labium form sharply-painted V-shaped sclerites, whilst the mandibles are stylet- like. The cibarium has no filter.

The musculature and skeletal parts of the cephalopharynx are shown to be highly adapted to the mode of feeding involved.

The complex and specialised mandibular lobes of aquatic filter-feeding larvae, such as Myathropa, are discussed and it is shown how they might have evolved from more primitive hook-shaped mandibles by way of an intermediate form such as that found in Eumerus. The specialised mandibles of Myathropa and Syrphus show widely different and successful paths that

evolution has taken from the primitive mandibular hook, in the Syrphidae.

Acknowledgements I am indebted to Professor W. E. Kershaw, V.R.D., M.D., D.Sc., for facilities provided in the Department of Biology, University of Salford, during the tenure of a research studentship. Dr. E. J. Popham and Mr. M. J. Parr have read the text and I am grateful for their helpful comments. I also wish to thank Messrs. G. Murdoch and H. G. Morgan of the National Agricultural Advisory Service for specimens of Eumerus larvae.

References Bhatia, M . L., 1939. Biology, morphology and

anatomy of aphidophagous syrphid larvae. Parasitology 31: 78-129.

Chandler,'A. E . F., 1968. Some host plant fac- tors affecting oviposition by aphidophagous Syrphidae (Diptera). Ann. appl. Biol. 61: 41 5-42 3.

Coe, R. L., 1953. Diptera, Syrphidae. Handbk Ident. Br. Insects 10( 1) .

Creager, D . B. and Spruijt, F . J., 1935. The relation of certain fungi to larval development of Eumerus tuberculatus Rond. (Syr- phidae, Diptera). Ann. ent. Soc. Am. 28:

Glumac, S., 1960. Phylogenetical system of the syrphid-flies (Syrphidae Diptera) based upon the male genitalia structure and the type of larvae with characteristics of the family and tribes. Glasn. Muz. Beogr. (B)

Hamrum, C . L., 1966. Food utilisation of the common Minnesota Syrphinae species. Ecol. aphidoph. Insects, Proc. Symp. Prague, 1965, pp. 71-73.

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Keilin, D., 1915. Recherches sur les larves de diptsres cyclorrhaphes. Bull. d e n t . Fr. Belg. 49: 15-198.

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- (in prep.). The structure of the mouthparts of calypterate dipteran larvae in relation to feeding habits.

Schremmer, F., 1951. Die Mundteile der Brachycerenlarven und der Kopfbau der Larve von Stratiomys chamaeleon L. Uster- reichische 2001. Zeitr. 3: 326-397.

Stone, A,, Sabrosky, C. W., Wirth, W . W., Foote, R. H. and Coulson, J. R., 1965. A catalogue of the Diptera of America north of Mexico. U.S. Dep. Agric., Agric. Handbk. 276.

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the structure of the mouthparts of syrphid larvae (diptera) in relation to feeding habits

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