The Anatomy of the Final Larval Instar of Diadromus (Thyraeella) collaris Grav. (Ichneumonidae), with Notes on Structural Changes Through the Prepupal and Pupal Stages.
Entomology Division, Plant Research Bureau, Nelson.
[Read before the Nclson Branch, July 17, 1944; received by the Editor, August 4, 1944; issued separately, December, 1944.]
Three larval instars are present in the life-cycle of Diadromus, and in appearance these stages are all similar in their maggot-like form. However, it is in the third instar and the prepupal stages that most of the transition from larval to adult organisation is noted, and consequently it is these stages which have been selected for special study. Although the pre-adult stages do not differ markedly from those of other ichneumons, there are certain features, such as the heart development, and the lack of complete histolysis, which are worthy of note. In the present account, only the more noteworthy features are dealt with.
The Third Instar Larva.
Immediately after ecdysis, the third instar measures approximately 2.5 mm. in length, but by the time feeding is complete, this dimension may reach as much as 4.5 mm. During this instar, considerable changes occur, and in the prepupal phases, adult structures can be clearly seen in an advanced stage of development. The spiracles are open throughout the instar, and the tracheal system functions normally. Abdominal chaetotaxy is lacking, and there is increased development of sensillae and sensitive apparatus generally in the oral region. Although the following anatomical description applies particularly to the active third instar, it also applies in its fundamentals to the earlier stages.
Head-capsule. (Figs. 1 and 2.)
The head-capsule in general outline from dorsal, lateral, or ventral aspects is approximately hemispherical in general form, although slightly flattened ventrally. The maxillary lobes (ma.) are rather less prominent, while the labium (lb.) is more prominent than in the earlier instars.
The labium is in the form of a hemispherical papilla which is constantly retracted and everted during feeding. The clypeal arch (cla.) bears on its ventral margin, a definite plate-like, lightly-chitinised flange (clp.), bearing several placoid sensillae. The labrum (lbr.) also has several sensillae with broad placoid bases, but each bears a minute central spine. From the inner side of each lateral arm of the clypeal arch, is an inwardly projecting chitinous process to which pharyngeal muscles are apparently attached. The pleurostomal
arches (pl.) and the mandibular struts (sms. and ims.) are much more strongly developed than in the earlier instars, but show no essential structural improvement. The mandibles (md.) are essentially the same as in earlier instars, but the articulation is better developed, and the mandibular apices are more tapering.
On the maxillary lobes and labium, definite palpal rudiments are seen in the form of complex chitinous discs containing sensory pits. Scattered basiconic and placoid sensillae occur on these organs and on the nearby cuticle. Above the clypeal arch are two lateral clusters of strong basiconic sensillae, but no definite antennary rudiments are to be seen.
Nervous System. (Figs. 3, 5, 6, 7.)
The nervous system is of a very primitive type, consisting of a comparatively unspecialised double chain of ganglia, connected by longitudinal and transverse commissures.
The largest ganglia are the supraoesophageals (sog.), which are ovoid, lying above the oesophagus just in front of the mid-gut. These ganglia give off definite trunks (mdnv.) to the anterior part of the head above the mouth. The paraoesophageal commissures run each side of the oesophagus to the suboesophageal ganglia (sug.), which give off trunks to the maxillae and labium (lb.nv.).
Behind this are the three pairs of thoracic ganglia fairly close together, and ten pairs of abdominal ganglia. No definite nerves are present behind the cephalic region.
Digestive System. (Figs. 3, 5, 6, 7.)
The digestive system is peculiarly degenerate in several ways due to the peculiar mode of life of the larva.
The oesophagus (oes.) is a short straight tube leading from the buccal cavity to the relatively enormous sacular mid-gut (mg.). The lining of the oesophagus consists of rather irregular cubical and columnar epithelium, underlain by a very poorly-developed muscular layer. The pharyngeal portion (ph.), which is separated from the oesophagus only by the presence of a thicker chitinous lining on its floor, has an arrangement of paired dorsal and ventral muscles extending outwards to the body-wall (dpm. and vpm.).
The mid-gut is lined with somewhat flattened cubical epithelium, and appears to be a storage organ for all material passing through the mouth. Here again, the muscular layers are very feebly developed. This storage organ occupies the greater part of the abdominal cavity, and leads behind to the blind hind-gut (hg.).
The malpighian tubules (mt.) are degenerate, being represented merely by paired, solid papillae. The hind-gut is not functional and consists of a more or less solid mass of cells. This hind-gut becomes functional only when the final prepupal ecdysis is about to take place. At this period, all the faecal matter accumulated and stored in the gut during the larval life is excreted.
Salivary Glands. (Figs. 3, 5, 6, 7.)
The salivary glands (sd.) are very well developed, and are one of the most conspicuous anatomical features of the larva. These glands open to the exterior on the dorsal surface of the labium, and the
opening is held in shape by a distinct chitinous collar. The duct bifurcates at the base of the labium, and the two branches run one on each side of the body to the base of the mid-gut at the posterior thoracic region, where each duct bifurcates again. About half way from the anterior to the posterior extremity, the third and final bifurcation occurs. Of the four branches now running along each side of the gut, the middle two are the longest, reaching to the beginning of the final abdominal segment.
These glands are straight and simple. They are glandular throughout their length, and are evidently very active. The cells are very large, with relatively huge nuclei. The cytoplasm appears granular-reticulate in section, and is very dense.
Respiratory System. (Fig. 4.)
In the third instar, the respiratory system is well developed and very complex. Spiracles (sp.) open to the exterior in the groove ventral to the pleural ridge on the first nine body segments. These spiracles are lagenate in shape, with necks leading to the main lateral tracheal trunks. The lateral trunks follow a sinuous course, forming ventral loops, particularly in the anterior five body segments. The first three thoracic loops are connected basally by stout sinuous commissural trunks.
Most of the subsidiary branches originate near the spiracular necks. From the first two thoracic spiracles, no ventral or dorsal commissures arise, but from the metathoracic and first two abdominal spiracles, originate complete ventral commissures. These commissures are incomplete in following segments, and their development progressively decreases posteriorly. From the main trunks, numerous finer tracheae arise which supply the tissues of the body.
In the early instars particularly, there is an extremely diffuse supply of hypodermal tracheae and tracheoles. Apparently this network serves a purpose in the absorption of oxygen from the surrounding body-fluids of the host.
Vascular System. (Fig. 7.)
Although the writer has been unable to locate any definite heart in the first instar, in the second instar it is present, and in the third well developed, and resembles the adult heart in structure. It is in the form of a dorso-ventrally flattened tube extending almost the entire length of the body of the larva. Dorsally it is suspended from the body-wall by cellular pillars (not illustrated), and ventro-lateral alary muscles are present. These alary muscles arise from groups of cells at the lateral edges of the heart, and extend outwards to the top of the pleural ridge. There are also irregularly-placed, very fine fibres inserted in the wall of the mid-gut.
In the fat-body, large, rounded oenocytes occur, and throughout the body various types of leucocytes are present.
Excretory System and Fat-body.
The malpighian tubules are not functional, and all excretory products are stored until the final prepupal ecdysis or later. Dorsally, there are metamerically arranged groups of relatively huge urate cells in the fat-body. These clusters can be seen in the living fully-fed
larva as white opalescent clusters beneath the dorsal body-wall. Whether or not any nitrogenous secretions are passed out with the gut-contents during the final prepupal ecdysis is not known, but these clusters of urate cells are still present during the pupal stage, and apparently their urate contents are not removed until the adult malpighian tubules are completely developed.
The fat-body cells are very large, and are almost identical with those of the adult. However, the peripheral layer of smaller cells is wanting in the larva.
The Prepupal Stages.
The stages in prepupation as described here are based on the work of K. Morris (1937).
When fully fed, the larva is more or less cylindrical in form, with the three thoracic segments, particularly that of the mesothorax, rather broader dorsally than the abdominal segments. This dorsal broadening gives the larva a rather hump-backed appearance, and forces the head downwards. Antero-posterior compression of these thoracic segments now begins, and this development marks the beginning of the prepupal stages. This slightly compressed form is known as the eonymph. The characteristic changes to produce the second stage or pronymph, consist of a marked dorsal enlargement of the abdominal segments, and the production of a slight “waist” between thorax and abdomen. At the same time the head becomes deeply sunken into the prothoracic segment, and the pleural ridge becomes less prominent. By this time, the imaginal eyes can be clearly seen, due to deposition of red pigment.
During the prepupal period, most of the elaboration of imaginal organs takes place. The imaginal discs for the antennae, wings, and legs, can be seen even in the first instar larva, but it is not until the prepupal stage that these structures begin conspicuous development. True histolysis is not apparent in Diadromus, and through the prepupal stages, a gradual absorption of larval structures, and the gradual building-up of adult organs takes place.
The larval gut degenerates rapidly, and becomes filled with a solid core of large, dense cells. By gradual arrangement and differentiation, the adult gut forms from this core of cells. During the prepupal period, all nervous elements are likewise gradually elaborated, and at no time is a central nervous system lacking in a recognisable form. The adult heart appears to develop by direct modification of the corresponding larval structure, and at this stage, both adult and larval muscles may be seen at the same time, one being built up from undifferentiated cell masses, the other being absorbed.
The genital structures probably become more or less differentiated at this stage, but the writer has been unable to detect them until fairly late in the pupal stage. One of the last of the larval structures to disappear are the salivary glands. The abdominal branches of these glands can still be seen in fairly late pupal stages, when the cephalic and thoracic organisation is almost completely imaginal.
The Pupal Stage.
After the comparatively long prepupal stages, the pupa libera emerges. By this time the adult organisation is well advanced, although the only pigmented portions of the insect are the compound eyes and ocelli, which are bright red. Very soon, the thorax becomes pigmented, but it is not until shortly before emergence that abdominal pigmentation occurs. Development is much more rapid in the cephalic and thoracic regions than in the abdominal region.
The protection of the pupa, it will be noted, is afforded entirely by the pupal skin and cocoon of the host. There is not the slightest indication of cocoon development or corresponding modification of the salivary glands in the parasite larva.
Morris, K. R. S., 1937. Bull. Ent. Res., 28, 4.
Morris, K. R. S. and Cameron, E., 1935. Bull. Ent. Res., 26, 3.
Wigglesworth, V. B., 1939. The Principles of Insect Physiology. Methuen and Co., Ltd., London.
Key to Lettering of Figures.
de.—developing imaginal eye.
dpm.—dorsal pharyngeal muscle.
ims.—inferior mandibular sturt.
lt.—lateral tentorial arm.
sld.—salivary duct and gland.
sms.—superior mandibular strut.
vpm.—ventral pharyngeal muscle.