The Anatomy and Systematic Position of Temnocephala novae-zealandiae Haswell.
[Read before Otago Branch, July 14, 1942; received by the Editor, July 27, 1942; issued separately, December, 1942.]
The genus Temnocephala occurs mainly in the Southern Hemisphere, where it has a very wide distribution, being found in Australia, New Zealand, New Guinea, East Indies, and South America. In the Northern Hemisphere it is known only in Mexico. It was first recorded for New Zealand by Wood Mason (1875), but it was not till 1888 that Haswell (1888) listed Temnocephala novae-zealandiae as a new species. Later, Haswell (1893) published a further account with figures of the external and internal structure of Temnocephala novae-zealandiae, and more recently (1924) he revised the structure of the female reproductive organs. The most complete general accounts of the group are those given by Merton (1914, 1922) and by Bresslau and Reisinger (1933) in Kükenthal's Handbuch der Zoologie, but these writers as well as Haswell relied mainly on preserved material, especially for Temnocephala novae-zealandiae, with the result that the description of the New Zealand species is in part incomplete. In view of this and of the fact that Kükenthal and Merton's papers are not available in New Zealand, it was decided to publish a concise account of the New Zealand species based on the study of living as well as preserved material.
Material and Methods.
Temnocephala novae-zealandiae is found at all times of the year on the body and appendages of the freshwater crayfish, Paranephrops neozelanicus, the majority being attached to the great chele, where no doubt they received a certain amount of protection from the long setae. When removed from the host they are able to live for several weeks in fresh water without aeration, and for a much longer period in aerated water. The eggs are laid throughout the year and are attached by one end to all parts of the crayfish.
Fixing. Various methods were tried, the most satisfactory being that of Wilhelmi (Lee 1937, par. 1210). According to this method, the animals are covered with almost boiling Zenker's fluid and flattened under a glass weight. After about 30 minutes in the fixative the animals are removed to water for some hours and then passed into iodine alcohol.
Staining. For whole mounts, HCl-Carmine gave the best differentiation, and for sections Mallory's triple stain was most satisfactory for general work. Heidenhein's Iron Haematoxylin was useful for histology, while Biebrich Scarlet is an excellent plasma stain and made a good contrast with Celestin Blue.
Temnocephala novae-zealandiae has six tentacles instead of the usual five. The young, immature animal is whitish except for the conspicuous dark brown intestine lying across the body; but as the animal becomes sexually mature, its colour changes to greenish-grey or brown according to the amount of yolk present. The length of the animal varies according to its age and extension, the body of a large, fully extended specimen measuring six millimeters. At the posterior end of the ventral surface is the large, stalked, ventral sucker and in front of it is the common genital pore. The mouth is also ventral and lies just behind the base of the tentacles. Dorsally, there is a pair of eyes at the anterior end, and at the sides, just behind the level of the eyes, lie the two excretory pores.
(a) Body Wall and Glands.
The body wall is not characteristically turbellarian. It is not ciliated, although Haswell (1893, p. 99) has observed cilia in other species, and there are no glands in the epidermis. There is a striated cuticle outside the epidermis which is here a syncytium with widely-scattered nuclei. Haswell (1893) and Merton (1914) both describe elevations, sensory and otherwise, on the cuticle. I cannot find any in an extended animal, although when the animal is contracted, the cuticle is uniformly crinkled all over. The epidermis rests on a wide basement membrane under which lie circular, diagonal and longitudinal muscle-layers in that order, with the band of longitudinal muscles much broader ventrally than dorsally.
Although no glands lie in the epidermis itself, a number of gland cells are situated in the parenchyma and have long ducts opening on to the surface of the body. There are three regions on which these ducts open:—(1) Tentacular, (2) sucker, (3) genital pore.
(1) Tentacular Glands. (Pl. 21, t.g.)
In most species of Temnocephala these glands lie dorsally and are scattered along the sides of the body from the excretory vesicle to the anterior testis, but in Temnocephala novae-zealandiae the gland cells of each side are usually aggregated into two compact bodies lying one behind the other at the sides of the intestine. Each glandular body or gland is ovoid in shape and is enclosed in a thin muscular sac. The gland cells inside have large vesicular nuclei and are irregular in shape, their boundaries being more or less marked by dorso-ventral muscles.
The secretion consists of mucus containing short, shiny rods which are the rhabdites characteristic of Turbellarians. The rhabdites take a bright red stain with Mallory, so that the course of the ducts to the exterior can be easily traced. Strands of ducts (pl. 21, t.d.) go forward from the glands of both sides and meet at the base of the tentacles in front of the eyes. From here the ducts pass into the tentacles in regular fashion, two strands to each tentacle where the ducts separate out and open on the ventral surface mainly at the tips of the tentacles. The mucus is often squeezed out of the ducts in the form of coiled threads which appear to be quite firm and solid and must be useful in entangling prey; the function of the rhabdites in the mucus is more difficult to explain unless they strengthen the entangling mesh.
(2) Sucker Glands.
There is a pair of Sucker glands (pl. 21, s.g.) at the sides of the posterior end of the body They are not so compact as the Tentacular glands nor so deeply staining and the secretion is granular. There are no rhabdites. From the glands, ducts run in strands to the centre of the sucker, and passing through the stalk spread out and open all over its ventral surface. Both the Tentacular and Sucker glands are very important in locomotion, the animal moving very quickly with a looping action. When not travelling it remains attached by the Sucker gland, and stretching out to its full length swings round in a semicircle, reaching far forward with its waving tentacles. Both glands are useful, too, in attaching the animal firmly to its host, which darts about with sudden, quick movements.
(3) Genital Glands.
These will be described in connection with the reproductive organs.
(b) Nervous System.
The nervous system follows the general platyhelminth plan and is very similar to that of planarians. There is an outer and an inner nerve net surrounding the body, the outer net lying immediately under the epidermis, the inner and much thicker net lying immediately inside the inner longitudinal muscles. The two nerve-nets are connected by fibres all over the body. The inner nerve-net is thickened to form three pairs of longitudinal nerve-cords, a dorsal, a ventral, and a lateral pair. The longitudinal cords are connected by transverse cords, and diagonal cords connect the dorsal and ventral portions. The nerve-nets contain nerve-cells and processes as do the nerve-cords, which thus differ from nerves of higher animals which are composed of nerve fibres only. The cells in the nerve-cords are more differentiated than those of the nerve-net, many being bipolar so that an impulse can pass in one direction only.
The “brain” is a broad, thick, horizontal band of nervous tissue lying dorsally just in front of the pharynx. It is merely a concentration of the nerve cords and contains the bodies of nerve-cells and tracts of fibres. The “brain” sends nerve cords to the tentacles and receives sensory nerves from the two eyes (pl. 21, e.), which lie in front of, and slightly dorsal to the “brain.” Each eye consists of a double pigment-cup lying transversely to the body, with a concavity at each end. There is a single pigment-cell and one retinula in each cup. The retinula-cell completely fills the cavity of the cup, the nucleus lying just outside the brim, from which the cell tapers to form a nerve fibre going to the “brain.”
Sense cells occur over the whole body and are connected with the nerve-nets or nerve-cords.
(c) Alimentary Canal.
The so-called mouth appears as a transverse slit on the ventral surface of the body near the anterior end. It leads through a muscular pharynx and short oesophagus into a wide saccular intestine occupying the middle part of the body. According to Fernando (1934), the pharynx is ectodermal in origin but not stomodeal, and
the oesophagus and intestine are endodermal. Using Goodrich's (1935) nomenclature, the entrance to the pharynx is the true mouth (pl. 21, m.) and the entrance to the oesophagus is the enterostome (pl. 21, en.). In the retracted condition, the true mouth lies well below the surface of the body, and the skin above it is folded so as to allow the pharynx to be protruded, the amount of folding varying in different species. From this aspect von Graff (1908) has established three types of pharynx for Rhabdocoels—simplex, bulbosus and plicatus. Temnocephala novae-zealandiae has a pharynx bulbosus (pl. 21, ph.), over the anterior end of which the skin forms a pharyngeal sheath (pl. 21, ph.s.).
The epithelium lining the depression leading into the pharynx is a continuation of the body epithelium but contains gland cells in addition to the epithelial cells. At the outer margin of the pharyngeal sheath it changes abruptly to the very distinctive pharyngeal epithelium which covers the anterior end of the pharynx and lines its cavity. The pharyngeal epithelium is a wide, deeply-staining layer without apparent structure and without nuclei. It has been variously described as cuticle only, as a syncytium, or as a degenerate epithelium with only occasional degenerate nuclei or with no nuclei at all. The various pores and strings of granules described by both Haswell (1893) and Merton (1914) as appearing in the epithelium are not visible in any of my preparations and are possibly artefacts. Since this layer rests on a basement-membrane as is the case with epithelium generally, it would appear to be here not a cuticle but an epithelium which has become highly specialised for the work it has to do in holding and crushing prey.
The pharynx is enclosed in a connective-tissue capsule, and between that and the epithelium are several muscle layers. There is a narrow circular and a narrow longitudinal layer on the outside, and similar layers lie next to the epithelium. Between these outer and inner sets of muscles there is a wide band of radial muscles. Scattered among the radial muscle-fibres are large nuclei like those of the parenchyma-cells. These nuclei are all very similar, and I am unable to distinguish the three types of cell, myoblasts, gland-cells, and nerve-cells described by Merton (1914, p. 28) for Temnocephala novae-zealandiae. A small sphincter muscle surrounds the so-called “mouth,” and strong anterior and posterior sphincters control the openings of the pharynx.
The oesophagus is very short and inconspicuous. In transverse section the cavity appears to be very small, but the walls are deeply folded so as to allow for great extension. Beyond having a sphincter of circular muscles it is not marked off in any way from the surrounding parenchyma. Numerous unicellular salivary glands lie in the parenchyma between the pharynx and the intestine, and their ducts enter the oesophagus both on the ventral surface where the gland-cells lie free, and at the sides where the cells are grouped together into solid clumps.
The intestine (pl. 21, i.) is a wide sac in which may be distinguished a smaller median portion with a large pouch on each side. Each pouch is partially subdivided into about six smaller pouches by connective-tissue septa which project into the cavity from the
intestinal wall. There is a very thin layer of circular and longitudinal muscles on the outside of the intestine, but it is the lining epithelium which comprises the main thickness of the wall. It consists of elongated cells with nuclei at the outside, the size of the cells varying greatly in proportion to the amount of food which the animal has recently eaten. Among the epithelial cells are numerous digestive gland cells which empty their secretion into the cavity of the intestine.
(d) Excretory System.
The excretory system consists of flame cells, branched excretory canals, and a pair of oval excretory vesicles (pl. 21, ex.v.) which open to the exterior on the dorsal surface near the anterior end, in a similar position to that of the Graffillidae, a family of the Rhabdocoel sub-order Dalyellioida. The lumen of the excretory vesicle does not correspond to the outline, but is in the form of a wide s-shaped tube running along the length of the vesicle and receiving at the posterior end a short, more or less transverse, collecting canal. The wall of the vesicle consists of a firm layer of tissue on the outside and lining the cavity, with between the two a loosely fibrillated layer. Haswell (1893) describes the outer layer as being composed of circular muscles used for emptying the vesicle. In all my stained preparations this layer appears quite different from the ordinary muscle tissue, moreover the vesicle is emptied not by the separatc contraction of its wall, but by the contraction of the whole animal.
A series of extremely fine branching canals extend from the outer layer to the inner lining, through which they pass and open into the cavity of the vesicle. Haswell (1893) considers that these fine canals join and enter the main anterior excretory canal at a definite point on each side. I could find no such connection, and the function of these fine canals seems to be quite obscure.
At the posterior end of the vesicle are two large nuclei close together. These are the only nuclei found in the vesicle and from their position it has been presumed by Halswell (1893), Merton (1914) and others that one is the nucleus of the vesicle which is thus a single cell, and the other is the nucleus of the cell which forms the collecting canal. The whole excretory system is intracellular, and nuclei can be seen at intervals in the walls of the main canals.
The collecting canals divide into anterior and posterior longitudinal canals lying at the sides of the body. The two anterior canals join in front of the eyes and from this connective a branch runs up the axis of each tentacle. The posterior canals are connected behind the pharynx and intestine, and from all these main vessels branches are given off in all directions.
Flame-cells were observed at the ends of some of the terminal branches on the tentacles and in other parts of the body. These are the “wimperflammen” of Haswell (1893), who saw only the flame, but there is no reason to believe that they are not typical flame-cells. There are also a number of flame-cells (thirty or more) in the wall of the excretory vesicle. What their function here is I do not know, nor if they are connected with the fine canal system of the vesicle. Haswell gives no explanation and Merton, who had no living material,
was unable to see flame-cells at all. Bresslau and Reisinger (1933), in describing the excretory system of the group Temnocephala as a whole, state that the excretory vesicle is lined with cilia and that the terminal branches of the excretory vessels end in cells with “treib-wimperflammen”.
According to Haswell (1893), some of the terminal branches of the canals end in nephridial cells, of which he found four types. Merton (1914) found only one type of cell which he thought might be nephridial cells (there were about twenty of these cells), but which were unlike any of Haswell's types. Bresslau and Reisinger (1933) consider that the cells figured by Merton (1914) correspond to the paranephrocytes already seen in the Typhloplanioida, the Dalyellioida and the Kalyptorhynchia among the Rhabdocoels and from this assumes that similar cells may exist in another closely allied order, the Temnocephalida. I have seen cells in stained sections which resemble both Haswell's and Merton's drawings, but I can find no connection between these cells and the excretory canals as Haswell suggests. On the other hand, recent experimental work on the Turbellaria (Bresslau 1933) shows that in the groups so far investigated the nephridial cells or paranephrocytes are not connected with the excretory canals at all, but are wandering cells in the parenchyma, where they collect the excretory material and carry it to the intestine, whence it is emitted with the faeces. A small amount of excretion may take place through the walls of the excretory canals to be washed out by the excess water removed from the body by the flame cells.
The whole problem of the excretory system and its mode of action in Temnocephala is still unsolved, although the canals themselves and the flame-cells can be well seen in young animals. More experimental work requires to be done on other members of this group, particularly on the closely-related Didymorchids, and the results compared with those recorded for other Platyhelminths.
(e) Reproductive Organs.
The common genital pore (pl. 22, g.p.) is connected by a narrow passage in the muscular body-wall with the genital atrium (pl. 22, g.at.) which lies in the parenchyma about mid-way between the dorsal and ventral surfaces. Into the atrium open the two genital ducts, the male on the left, the female on the right. The male copulatory apparatus and the female organs, each surrounded by its own parenchyma, lie directly in front of the genital pore behind the narrow median part of the intestine.
(2) Male Orgems.
The male organs consist of a pair of testes on each side of the body with a vas deferens from each pair joining its fellow in the middle line to form a seminal duct. The seminal duct enters a seminal vesicle from which the sperms pass through a granular vesicle (vesicula granulorum of von Graff) into the ejaculatory duct opening through the penis into the genital atrium. Ducts from prostate glands enter the granular vesicle.
The oval testes (pl. 21, te.) lie in the parenchyma at the sides of the body, an anterior pair about halfway along the body, and just behind them a larger pair from which the vasa deferentia (pl. 22, v.d.) arise as wide, thin-walled tubes usually filled with spermatozoa. Each anterior testis is connected with the one behind by a narrow duct so that spermatozoa from the anterior testis must pass through the posterior one in order to reach the vas deferens. The two vasa deferentia join to form a median duct which runs forward beside the penis. Haswell (1893), Wacke (1903) and Merton (1914) call this median duct the seminal vesicle, but I prefer to reserve that term for another structure and to call this duct the seminal duct (pl. 22, d.s.), bringing it into line with similar ducts described by von Graff (1904–08), both for Planarians and Rhabdocoels. The proximal part of the seminal duct is wide and filled with spermatozoa, thus corresponding to the “false vesicula seminalis” of the Planarian Geoplana marginata and the Rhabdocoel Maerostomum tuba where the true seminal vesicle is a completely different structure. The distal part of the seminal duct is narrow and contains few spermatozoa. The walls of the vas deferens and seminal duct are similar in structure, with an outer layer of circular muscles and an inner epithelium with flattened nuclei.
The seminal duct enters the junction between two more or less spherical vesicles through a very small opening on the ventral surface. The anterior vesicle (pl. 22, v.s.) is the true seminal vesicle and, in sections, is seen to contain a very few spermatozoa. Its position corresponds exactly to that of the seminal vesicle described by von Graff (1904–08, p. 2274) for Rhabdocoels, and it has a specially muscular wall for forcing out the spermatozoa, such as is found in the seminal vesicle of Planarians where also as a result of the contraction of these muscles, spermatozoa are not found in preserved material. The muscles are arranged with an inner circular layer and a wider outer longitudinal layer from which radiating muscle bands converge to a point dorsal to the vesicle, these no doubt helping too in the discharge of spermatozoa. Haswell (1893) names this vesicle the ejaculatory sac on account of the fact that it usually contains a small number of spermatozoa. Wacke (1903) describes it as a second seminal vesicle, but Merton (1914), while denying that it is a seminal vesicle, is unable to account for its function. He says that its cavity is not connected with any duct and suggests some kind of valvular function for controlling the protrusion of the penis. I cannot agree with this, as such a function would, as far as I know, be unique for Rhabdocoels.
Posterior to the seminal vesicle is another vesicle (pl. 22, v.gr.) which is really the enlarged proximal end of the ejaculatory duct. Haswell (1893) calls it the caecal pouch, Merton (1914) and Bresslau and Reisinger (1933) do not describe it. It is filled with thin-walled ducts containing deeply staining granules and is the granular vesicle found in worms with prostate glands and described by von Graff (1904–08, p. 2274) for Rhabdocoels, resembling particularly that of the Dalyellid Jensenia angulata. The seminal vesicle, the granular vesicle and the L-shaped penis (pl. 21, p.) enclosing the ejaculatory
duct, all lie in a more or less straight line with a continuous sheath of circular and longitudinal muscles round all three, the whole being loosely bound to the parallel seminal duct.
An epithelial plasma lines the two vesicles and the penis and is continuous with the atrial epithelium. I could find no nuclei in the plasma, but as it rests on a quite conspicuous basement membrane, the plasma is comparable to the enucleate epithelium lining the pharynx. The plasma varies in thickness in the three different regions. In the seminal vesicle it is fairly wide, but in the granular vesicle and the penis it is extended to fill almost the whole cavity, and through it runs the ducts of the prostate gland (pl. 22, pr″d″). On the outside the plasma rests on the basement membrane, and on the inside it forms the lining of the narrow ejaculatory duct (pl. 22, d.ej.). In the penis the outer plasma contains a firm supporting layer of cutin (pl. 22, cu.) which at the distal end is flexible and is lined with long thin spines (pl. 22, cu.'). No part of the penis can be protruded into the genital atrium since the atrial epithelium is continuous with the epithelial plasma of the penis, but the flexible tip of the penis is able to be evaginated to form an extrovert which in this position has a wide band of spines right round the tip. These spines have the function of firmly attaching the end of the evaginated penis during copulation.
For almost the whole length of the long arm of the penis there extends outside the epithelial plasma a large protoplasmic cell (pl. 22, p.c.) with one large nucleus. Von Graff (1904–08, p. 2287) describes similar cells in Rhabdocoels which lie outside the penis and secrete the cutinous support. This large cell here produces a secretion which is found in lumps between the cell and the cutin, and which stains bright red in Mallory while the cutin stains light orange. The amount of secretion increases towards the distal end of the penis, where it forms a wide band round the outside of the cutin. It is difficult without further experimental work to say how the cutin is formed, but it is quite possible that it is formed by the large cell and that the red secretion is an intermediate stage in its formation.
The prostate glands (pl. 21, pr.) are a series of multicellular, more or less compact glands lying along the sides of the body between the excretory vesicles and the posterior testes. The glands are a uniform grey colour with Mallory, only the nuclei of the cells being deeply stained. The granular secretion, however, stains red and can be traced in strands of ducts running along beside the vasa deferentia. Where the two vasa deferentia join to form the seminal duct, the prostate ducts become more closely packed together and form a solid-looking mass (pl. 22, pr.d.) which ultimately surround the seminal duct as it enters the seminal vesicle (pl. 22, pr.d.). The prostate ducts enter the granular vesicle, and their passage through the epithelial plasma has already been described. Their secretion is discharged into the cavity of the ejaculatory duct, where it is mixed with the sperms and may serve to form sperm-packets as in other Rhabdocoels. In none of the previous papers on Temnocephala has the granular vesicle and its connection with the prostate gland been properly identified. Merton (1914) and Haswell (1893, p. 125)
both refer to prostate glands and their ducts, but neither seems to have traced out the ducts nor to have identified the granular vesicle as being connected with them, although it is such a regular feature of the Rhabdocoels.
(3) Female Organs.
The female organs have more distinctive features than any other part of the reproductive system and have been more recently described by Haswell (1924). They consist of a germarium with a germiduct, vitelline glands with their ducts, a vesicula resorbiens with its duct, three receptacula seminis and the ootype which connects them all with the genital atrium. With the exception of the vitelline glands (pl. 21, vit.g.) which are scattered over the whole dorsal surface, all the female organs are grouped together behind the narrow median part of the intestine and lie on the right side.
The germarium (pl. 21 and 22, gm.) is a compact oval body which can be easily recognised by the very large vacuolated nuclei of its ova (pl. 22, o.n.). The ova are wedge-shaped and are packed firmly together inside a connective tissue capsule. The short germiduct (pl. 22, g.d.) runs forward to enter the ootype, which here also receives the ducts of the three receptacula seminis (pl. 22, r.s.), and the two vitello-ducts (pl. 22, vit.d.). The vitelline glands consist of a series of follicles which are scattered throughout the dorsal parenchyma, particularly in the region of the intestine. The follicular ducts join to form a single vitelline duct on each side.
The vesicula resorbiens (pl. 22, v.r.) is the most anterior of the female organs and lies with its curved border pressed against the posterior wall of the intestine. It is a reservoir of superfluous reproductive material which can be absorbed at intervals into the gut. The contents are mainly yolk granules and secretion of the shell gland which are being produced all the time but are only needed periodically when an egg is being formed. This vesicle was originally called the receptaculum seminis, Weber (1889) and Haswell (1888), and was then thought to be a reservoir for spermatozoa. Haswell (1924) later revised his opinion as to the function of the vesicle in view of the fact that it contained yolk, not spermatozoa, and that Merton (1913) had found other spermatozoa-filled vesicles which were obviously the true receptacula seminis (pl. 22, r.s.), and to Haswell is due the name vesicula resorbiens. Among the Platy-helminths some such method for removing excess products from the female organs is not uncommon. The Laurer canal in the Malaco-cotylea and the genito-intestinal canal found in some Rhabdocoels, Triclads and Polyclads have the same function.
The anterior part of the ootype receives numerous pear-shaped unicellular shell-glands (pl. 22, sh.g.) with large nuclei. The posterior part is highly specialised to form a thick muscular bulb, the uterus (pl. 22, ut.) lined with hard, sharp teeth in which the egg is held until laid. This very conspicuous bulb is characteristic of Temnacephala novae-zealandiae and has no equivalent as far as is known in any other species. The egg is large and when ready to be
laid not only greatly distends the bulb with its hard shell, but displaces all the organs near it, reducing the cavity of the intestine to a slit. Round the atriopore are fine cement-glands (pl. 22, c.g.) for attaching the egg to the Crayfish.
According to Merton (1914) Temnocephala is protandrous, ripe spermatozoa having been found in the testes and seminal duct, while the female organs were still not developed. At the same time the receptacula seminis were also very full of spermatozoa which showed that either copulation or self-fertilization had already occurred.
Systematic Position of the Sub-Order Temnocephalida.
Great interest has always surrounded Temnocephala because of the problem of its systematic position. Superficially it appears to have at least some of the characteristic features of more than one class, which has in the past prevented it from remaining securely in any one position and led to the hope that it might prove to be a link between the Turbellaria and the Trematoda.
When first discovered by Gay (1849) it was set down as a Hirudinean, but later on it became a Trematode (Weber 1889 and Braun 1879–93). With a further study of related genera a better knowledge of the group was obtained, and Haswell (1893) and Benham (1901) created a separate class, Temnocephaloidea, of the Phylum Platyhelmia, between the two classes Turbellaria and Trematoda. This new class now contained other genera besides Temnocephala.
The Temnocephaloidea, nowadays called Temnocephalida, were first removed from their halfway position and placed in the Turbellaria in the second edition of Claus's Textbook of Zoology, edited by von Grobben (1909). Later Mexner (1925), Poche (1925) and Baer (1931) confirmed this, and there they remain at the present time.
Although the more obvious features of the Temnocephalida are ones that we associate with Trematodes—the shape, the sucker, the excretory vesicles and the fact that it lives on a host, these features have one by one been shown not to be exclusively Trematode, and therefore not diagnostic. Suckers are common among the Trematoda, but they may also be present in the Turbellaria. Thus a sucking-organ (according to Bohmig) is present in the acoelous Convoluta lenseni, also in the ectoparasitic Rhabdocoel, Genostoma. Among the Polyclads the Cotylea have a kind of primitive sucker, while among the marine Triclads the Bdellouridae are distinguished by having a sucker at the hind end. Since, therefore, the sucker is found in widely-varied groups of Turbellaria it can be regarded merely as an adaptation to specific circumstances and not as an exclusively Trematode feature, and the suckers of the Temnocephalida must not be used as an argument for classing them with the Trematoda.
The excretory system of the Temnocephalida with its two anterior excretory vesicles is very like that of the Monogenetic
Diagrammatic view of Temnocephala novae-zealandiae in a retractedcondition from the do [ unclear: ] sal surface to show the general arrangement of the organs. For details of the Genital Complex see Pl. 22.
Explanation of Lettering.
C.g., cement gland; cu., firm cutin; cu'., flexible cutin with spines which can be everted; d.ej., ejaculatory duct; d.s., seminal duct filled with spermatozoa; e., eye: en., enterostome leading into the oesophagus with salivary glands on both sides; ex. v., excretory vesicle; g.at, genital atrium; g d., germiduct; gm., germarium; g.p., genital pore; i, intestine; m., true mouth; o.n., nucleus of ovum; p., penis; p.c., formative cell; ph., pharynx with muscle layers and sphincters; ph.s., pharyngeal sheath; pr., prostate gland; pr.d., massed prostate ducts which at pr'd' surround the seminal duct, and at pr″d″ open into the ejaculatory duct; r.m., retractor muscle; r s., receptaculum seminis; sh.g., shell gland; s.g., sucker gland; t.d., ducts of tentacular gland; te., testis; t.g., tentacular gland; ut., uterus with muscle layers large sphincter and teeth; v.d., vas deferens; v.gr., granular vesicle; vit.d., vitello-duct; vit.g., vitelline gland; v.r., vesicula resorbiens; v.s., seminal vesicle.
Trematodes, but more recent work on the Rhabdocoels shows that in several families of that order similar paired excretory vesicles are present.
As for the Temnocephalida living on hosts, they are epizoic and not ecto-parasitic, indeed the fact that they lead, generally speaking, a non-parasitic mode of life is one reason for removing them from the Trematoda and placing them in the Turbellaria. The Temnocephalida are also separated fundamentally from the Trematoda by the structure of the epithelium, which is ciliated in some forms, and by the possession of rhabdite-forming glands—both Turbellarian characters.
The general anatomy and especially the reproductive organs of the Temnocephalida show a very close relationship to the Turbellarian order Rhabdocoela and it is now universally agreed that they are derived from a free-living Rhabdocoel, though it has not been decided so far which one is its ancestor. According to Bresslau and Reisinger (1933) the Turbellaria are polyphyletic in origin, the Rhabdocoels arising from three separate stems (text-fig.). Of these the Notandropora and the Opisthopora (both forms with ovaries, but differing from each other in the number of main excretory canals) arise on independent stems. The other main stem (forms with germarium and vitellarium) has two principal branches each with one offshoot—one branch the Typhloplanoida with an offshoot Kalyptorhynchia, and the other
branch the Dalyellioida with an offshoot the Temnocephalida. This branching stem shows many signs of higher organisation and gives rise to a great number and variety of families. Bresslau and Reisinger (1933) believe that the Temnocephalida are closely related to the Dalyellioida, being either directly connected to this sub-order or having evolved parallel to it. This theory has been further strengthened by their inclusion for the first time of Didymorchis in the Temnocephalida. This minute animal was discovered by Haswell (1900) in the gill-chamber of Paranephrops neozealanicus and was later placed by von Graff (1908) in the Dalyelliidae. However, in its structure and habit Didymorchis is typically Temnocephalid except for the absence of tentacles (not a diagnostic feature), and Bresslau and Reisinger consider it to be a Temnocephalid derived from a Dalyellid. This very close connection between Didymorchis and the Dalyellioida on the one hand, and between Didymorchis and the Temnocephalida on the other points to the fact that the Didymorchidae may be the ancestral group of Temnocephalida and that the three other Temnocephalid families—Scutariellidae, Temnocephalidae and Actinodactylellidae—may have each originated separately from a Didymorchid-like ancestor on the Dalyellid stem of the Rhabdocoela.
Thus the distinction between the Temnocephalida and the Daly-ellioida becomes much less marked and the line of separation between the two groups much more difficult to define; indeed, the more one studies the Temnocephalida the more one realises that far from being a unique group separating two important classes it falls into its natural position very close to the Rhabdocoela.
The question now remains whether to include the Temnocephalida in the order Rhabdocoela or to still retain a separate order for them. In the general classification of Vermes at the beginning of Kükenthal, only four orders of Turbellaria are given, the Temnocephalida being included, presumably, in the Rhabdocoela. Bresslau and Reisinger (1933), however, in discussing the phylogeny of the group, consider that the structure and evolution of the Temnocephalida make it still necessary to place them in a separate order of the Turbellaria and not in a sub-order of the Rhabdocoela.
My study of Temnocephala novae-zealandiae has further emphasised its close relationship to the Rhabdocoela, particularly to the Dalyellioida. This and the inclusion of the Dalyellid-like Didymorchis in the Temnocephalida so reduce the distinctive features of the latter group that there seem to be no characters left which are sufficiently distinct to warrant the formation of a separate order. I therefore have placed Temnocephala novae-zealandiae in a sub-order Temnocephalida of the order Rhabdocoela.
Further research on the phylogeny of the Dalyellioida and their relation to the other Rhabdocoel sub-orders may quite possibly show that the line of separation lies not between the Temnocephalida and the Rhabdocoela, but between the Dalyellioida (including the Temnocephalida) and the rest of the Rhabdocoela. This, however, can only be decided after careful study of all the Rhabdocoel sub-orders.
Classification of the Temnocephalida.
[From Bresslau and Reisinger (1933), who based their classification on Baer (1931).]
Amera (unsegmented worms).
Family 1: Didymorchidae. Temnocephalida without tentacles, and with one pair of testes.—Didymorchis Haswell (1900) with 3 species on New Zealand Crayfish.
Family 2: Scutariellidae. Temnocephalida with 2 tentacles and one pair of testes.—Three genera: Scutariella Mrázek (1907), 1 sucking-disc, gut divided into two, 1 species on the Southern Atyidae; Monodiscus Plate (1914), 1 sucking disc, gut simple, 1 species on the Indian Atyidae; Caridinicola Annandale (1912), 2 sucking pits, 1 species on the Indian Atyidae.
Family 3: Temnocephalidae. Temnocephalida with 5 to 12 anterior tentacles and 4–12 testes.—Four genera: Temnocephala Blanchard (1849), 5 tentacles, 4 testes, 21 species on South American, Central American, East Indian, Australian, and New Zealand Crabs, Crayfish, and Snails; Craniocephala Monticelli (1905), 5 tentacles, 6 testes, 1 species on the New Guinea Crab; Dactylocephala Monticelli (1899), 12 tentacles, 12 testes, 1 species on Madagascar Crayfish; Craspedella Haswell (1893), 5 tentacles, 10 papillae and 3 transverse lamellae at the posterior part of the body, 4 testes, 1 species on Australian Crayfish.
Family 4: Actinodactylellidae. Temnocephalida with 2 anterior tentacles and 10 at intervals along the body, 4 testes.—One genus: Actinodactylella Haswell (1893), with one species on Australian Crayfish.
The external and internal features of Temnocephala novae-zealandiae are described with reference to previous work on that species and to related forms.
The body-wall is not ciliated, although cilia have been found in other species. In the region of the tentacles, sucker and genital pore, open ducts of glands situated in the parenchyma often at a considerable distance from their exits. The tentacular secretion contains rhabdites.
The nervous system consists of an outer and an inner nerve net with three pairs of longitudinal nerve cords in the inner nerve net and a concentration of nerve cords in front to form the “brain.”
In the alimentary canal the true mouth is the opening into the pharynx which is of the pharynx-bulbosus type and may be protruded beyond the so-called mouth. The short oesophagus receives salivary ducts and gland cells are found in the intestinal epithelium. The opening into the oesophagus is the enterostome.
The excretory system is platyhelminth in type with a pair of excretory vesicles at the anterior end. In the walls of the vesicle are numerous flames and fine ducts, and branches of the excretory canals end in flame cells.
The male and female reproductive organs are described. In the male there is a granular vesicle for receiving the ducts of the prostate glands. This is commonly found in Rhabdocoels, but has not previously been described for Temnocephala. The female organs have more distinct features than any other part of the reproductive system. The muscular uterus lined with teeth is unique in Temnocephala.
The systematic position of the sub-order Temnocephalida is discussed, and it is shown that the characteristics originally supposed to be exclusively Trematode are also found in Turbellarians and therefore cannot be considered diagnostic features. The Temnocephalida are derived from a free-living Rhabdocoel and are most closely related to the Dalyellids, with which they are either directly connected or to which they have evolved parallel. Bresslau and Reisinger (1933) have enlarged the Temnocephoida so as to include the former Dalyellid Didymorchis although it has no tentacles. This further reduces the isolation of the Temnocephaloida and brings them more close to the Dalyellioida. The author places Temnocephala novae-zealandiae in the sub-order Temnocephalida of the order Rhabdocoela.
This work was done under the supervision of Professor B. J. Marples, to whom the writer gratefully records her thanks for valuable suggestions and criticism.
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