Encyclopædia Britannica, Ninth Edition/Trematoda

by William Evans Hoyle

TREMATODA, popularly known as "flukes," form one of the three main divisions of the flatworms or Platyhelminthes. They have been defined thus (Jackson, 1):^[1]—

" Unisegmental Vermes, with a flattish, leaf-like, more or less cylindrical body provided with organs of adhesion in the shape of suckers and sometimes of chitinoid hooks. The cuticle, so called, appears to be a metamorphosed layer of cells. There is a well-developed nervous system, the ganglia of which are entirely supra-pharyngeal, i.e., dorsal. There is a mouth, and an alimentary canal which is usually forked, but no anus. The excretory system has the form of more or less branching tubes commencing with flame-cells, and either ending in a contractile vesicle or opening by two independent orifices. Hermaphrodite self-impregnation occurs, as well as reciprocal impregnation. The embryo either develops direct into the sexual form (monogenetic Trematoda} or gives origin to a series of intermediate non-sexual dimorphic forms (digenetic Trematoda). Parasitic."

Historical Sketch.—Some of the more salient points in the history of our knowledge of these animals have already been alluded to in the article Parasitism (q.v.) a few additional facts must, however, be mentioned here. The Trematoda were first formed into a group by Rudolphi (2), who included in it the following genera:—Monostoma, Amphistoma, Distoma, Tristoma, Pentastoma, and Polystoma; the name had reference to the suckers, which Rudolphi regarded as being for the most part openings into the body (Gr. τρῆμα, an aperture). Some of these forms were soon perceived to have but small connexion with the others; and Cuvier (3) reduced the whole to one genus, for which he adopted the name Fasciola, Linn. The Pentastomes have since been transferred to the Arachnida (q.v.).

Our scientific acquaintance with the group may be said to date from 1831, when Mehlis noticed that the eggs of certain Distomes hatched into a minute ciliated body with an eye-speck resembling an Infusorian, an observation which gave the key to the life-history of these forms. Von Siebold in 1835 (4) supplemented this discovery by the observation that the ciliated embryo of Monostomum mutabile contained, as a "necessary parasite," as it was termed, an organism identical with the "kingsyellow worm" (Redia), found by Bojanus in pond-snails, and Von Baer had previously shown (5) that these gave rise to free-swimming organisms not unlike tailed Trematodes. The materials were thus ready to hand for a co-ordination of the whole life-history, and Steenstrup recognized it as an instance of the so-called "alternation of generations" (6). These researches received important additions at the hands of Pagenstecher (7) and others, who showed experimentally that encysted Distomes grow mature directly after their transference from one host to another, and thus that a migration is necessary to the attainment of their maturity. Diesing's great work (8) appeared in 1850, and has formed the groundwork of all subsequent treatises on the systematic arrangement of parasitic worms, although it included forms which really belong to quite different groups. In 1861 Van Beneden gained a prize offered by the French Academy by his elaborate memoir on the intestinal worms (9), in which he not only described many new and interesting forms, but gave anatomical details regarding others previously known, and entered into detailed comparisons between the Cestodes and Trematodes, both in their adult and immature states. Of recent years the chief additions to our knowledge have been more in the direction of further details regarding the structure and life-history of special forms than the elaboration of new general principles.

Anatomy.—In endeavouring to give a very brief account of the more salient points in the anatomy of the Trematoda it has been thought expedient to select some well-known form as a type, and afterwards to indicate the characters in which other species differ from it; for this purpose the common liver-fluke, Fasciola (Distomum) hepatica has been chosen, as it is not unfrequently found in the bile-ducts of sheep and other domestic animals, and constitutes a scourge much dreaded by farmers. The account here given is in the main abstracted from Sommer (10).

External Appearance.—The animal has a flattened oval shape, with a sub-triangular process on the broader end, which represents the head. The total length varies from 20 to 35 mm., the breadth from 6 to 12 mm. On superficial examination two narrower lateral areas may generally be distinguished from a broader median one; the former are occasionally of a coarsely granular appearance and reddish-brown or orange in colour, and increase in breadth towards the posterior end of the body, where they commonly unite. The median area is commonly greyish-yellow in colour, sometimes spotted with black; its anterior portion corresponds to the uterus, the posterior to the testes. Two suckers (fig. 1, A, o, s) are in the middle line of the body; one is at the anterior extremity, and is directed forwards and somewhat downwards; it is known as the anterior or oral sucker, being perforated by the oesophagus. The posterior or ventral sucker is situated, as its name implies, on the inferior surface of the body, just behind the head-papilla.

FIG. 1. A, Fasciola hepatica, from the ventral surface (x 2); the alimentary and nervous systems only shown on the left side of the figure, the excretory only on the right, a, light main branch of the intestine; c, a diverticulum; g, lateral ganglion; n, lateral nerve; o, mouth; p, pharynx; *, ventral sucker; a, cirrus sac; d, left anterior dorsal excretory vessel; m, main vessel; v, left anterior ventral trunk; x, excretory pore. B, Anterior portion more highly magnified (from Marshall and Hurst, after Sommer). M, cirrus sac; d, ductus ejaculatorius; /, female aperture; o, ovary: od, oviduct; p, penis; 5, shellgland; I, anterior testis;, uterus; ra, rp, vasa deferentia; M, vesicula seminalis; y, yolk-gland; yd, its duct. C, Genital sinus and neighbouring parts (from Sommer). a, venlral sucker; 6, cirrus sac; c, genital pore; d, evaginatcd cirrus sac (? penis); e, end of vagina; /, vasa deferentia; g, vesicnla seminalis; h, ductus ejaculatoiius; t, accessory gland. D, A ciliated funnel from the ex cretory apparatus, highly magnified (from Fraipont.) o, orifice of the funnel. E, Egg of Fasciola hepatica; x 330 (from Thomas).

The suckers measure on an average about 1 mm. in diameter, the ventral being slightly the larger. The internal organs communicate with the outer world by four apertures: (1) the mouth (o), situated at the anterior pole of the body and perforating the oral sucker; (2) the excretory pore (x), placed at the opposite extremity, and giving exit to the effete products; (3) the poms genitalis (fig. 1, B, })), leading into a sinus into which the ducts of both sets of genital organs open, it is to be found on the under surface of the head-papilla at or near its centre; (4) the opening of the Laurer-Stieda canal, situated on the dorsal surface of the animal, near the junction of the two portions of the median area, it is excessively minute and difficult of detection, and leads by a narrow canal into the duct of the yolk-gland.

Internal Structure.—All Trematoda have been commonly regarded, like other flat-worms, as devoid of a body-cavity (cœlom), and as consisting of parenchymatous tissue, in which the various organs were embedded. Recent researches of Fraipont (15) appear to show, however, that the intercellular spaces in this tissue are to be regarded as the homologue of a cœlom. The body is enclosed by a complex sheath (cortex), which may be resolved into several layers, which will be discussed in order, proceeding from without inwards. (1) The cuticle, which encloses the whole body, is a thin, pellucid, structureless membrane; at the margin of the mouth it is reflected so as to form a lining for the oesophagus, and similarly at the opening of the genital sinus it passes inwards to form a lining to the vagina. The same phenomenon is observed at the excretory aperture. By the application of ammonia the cuticle may be separated from the subjacent tissues and its peculiarities demonstrated; although apparently smooth to the naked eye, it presents under the microscope numerous sharp backwardly directed pro cesses, each of which encloses a hard stylet-shaped body. These prominences are closely set over the whole body except immediately around the suckers, extending even into the interior of the sinus genitalis. The cuticle is furthermore perforated by innumerable fine pores, directed outwards and somewhat backwards. With regard to the homology of the cuticle of Trematodes the same uncertainty prevails as in the case of Cestodes (see Tape-worms); the general opinion is that it is not comparable with the chitinous cuticle of Arthropoda, but is either a specially developed basement-membrane (Kerbert, 11) or a layer of modified cells (Ziegler, 12, and Schwarze, 13). (2) The outer cellular layer is the matrix of the cuticle. (3) The muscular coat consists of three different layers: (i.) a thin layer of circular fibres; (ii.) the longitudinal muscles, which form a series of separate bundles; (iii.) the oblique muscles, confined to the anterior half or third of the body, and crossing so as to form a rhomboidal lattice-work,—they are especially strong on the anterior ventral aspect of the animal. (4) The inner cellular layer consists of elements which closely resemble those of the outer, but are somewhat larger; they have been mistaken by various observers for cuticular glands. The suckers may be considered as parts of the cortical layer; speaking generally, each has the form of the segment of a sphere, although the anterior one is shallower at the lower than at the upper margin, and is penetrated by the oesophagus. Each consists of three sets of muscles,—a thin outer equatorial layer, a second meridional, and a mass of radially disposed fibres forming the greater part of the substance. It would appear that the function of the first two of these groups is to flatten out the sucker, whilst the radial ones restore its cavity and thus produce a suctorial action. To the ventral sucker are attached a number of muscular fibres belonging to the dorso-ventral system, and in particular a strong bundle, which passes from behind down wards and forwards.

Digestive system.The digestive system (fig. 1, A), the presence of which furnishes one of the most characteristic differences between Trematodes and Cestodes, extends throughout the body on a plane between the peripheral nervous and reproductive systems. It has only one aperture, as above mentioned, in the centre of the anterior sucker. The anterior portion or pharynx, although very short, measuring not much more than 1 mm. in length, is again divisible into two sections. The hinder of these is the larger, and is sometimes spheroidal but more commonly fusiform in shape; it has strong muscular walls, which, in conjunction with protractor and retractor muscles, bring about a kind of pumping action whereby nutritive fluids are taken into the stomach, which name may be applied to the larger posterior section of the alimentary tract, since in it the digestive processes are carried on. The canal, which leads from the posterior end of the pharynx, divides almost immediately into two branches, which diverge at first rapidly and then run almost parallel, as far as the hinder end of the body. Each of these gives off from its outer aspect some 16 or 17 lateral branches (c), which divide and sub divide till their ramifications fill nearly the whole area of the body. The digestive tract is lined by a layer of simple cells, resembling a cylinder epithelium. These behave towards the blood corpuscles and other contents of the intestine exactly as would a number of Amcebae, putting out processes or pseudopodin, which ingest them,— so that, in common with many of the lower Invertebrates, the liver-fluke lives by "intracellular digestion" (see Metschnikoff, 14).

Excretory system.The canals of the excretory system (m) may be divided into three groups. (1) The collecting network consists of very fine tubules which anastomose freely with each other; they are situated on the boundary between the cortical and middle layers, and arc therefore visible from either side of the body. (2) Conducting vessels (v, d) receive the contents of this network. Each of these is formed by the union of a larger or smaller number of the delicate canals just described, and after a longer or shorter course opens into the median excretory canal (m). On the way, however, it communicates with the neighbouring vessels, so that a second network is formed, which is distinguished from that of the collecting tubules by the greater size of its meshes and by the fact that it is specially visible from the dorsal surface of the animal. In the head four of these con ducting vessels arise, which are disposed in two pairs, one situated dorsally and one ventrally. As they pass backwards they receive many branches, the dorsal unites with the ventral of its own side, and the two tubes thus formed unite to constitute the last division of the excretory system. (3) The median vessel (m) passes along the body for the posterior two-thirds of its length, immediately beneath the dorsal cortical layer. It is widest near the commencement, where it measures about 5 mm. in diameter, and finally opens at the posterior extremity of the body. The wall of the excretory apparatus is constituted everywhere by an exceedingly delicate elastic membrane, which exhibits neither a cellular lining nor cilia; furthermore, neither valves nor muscles have been demonstrated in connexion with it. It contains a thin colourless fluid, in which very small highly refractive drops are suspended.

The details of the termination of the excretory system seem to have been first clearly made out by Fraipont (15), who worked upon species in which they are more distinct than in the form now under consideration. The spaces between the round connective-tissue cells of the body are star-shaped in form, and into these the finest excretory tubules, above mentioned, open by funnels (fig. 1, D), into each of which projects a vibratile cilium, thus constituting the so-called "flame-cells." These researches have given rise to numerous differences of opinion, as regards questions both of fact (16) and of priority (17). Reproductive organs.The liver-fluke contains a complete set of male and female organs, which form the most conspicuous part of its anatomy, and both of which open into the genital sinus which has been described above. A. The Male Organs, (i.) The testes (fig. 1, B, t) are two in number, situated one behind the other in the hinder division of the median area. They rest upon the ventral cortical layer in the parenchyma of the body, and immediately above them are the ramifications of the digestive tract. Each consists of a large number of ramifying tubes, often with slightly dilated extremities. These unite into three or four, and eventually into two, main excretory ducts (va, vp), which terminate at the base of the cirrus-pouch. Within the testicular tubules may be found spermatozoa in all stages of development; the first stage appears to consist of small roundish membraneless cells with a single nucleus; the nucleus then divides and the cells become polygonal from mutual pressure. These large cells lie in the middle rather than at the sides of the tube, and among them are a number which, while they possess on one side a smooth evenly rounded contour, are on the other very irregularly and deeply serrated. These serrations elongate until they become the delicate filaments of spermatozoa, the small shining heads of which are still embedded in the protoplasm of the cell, (ii.) The vasa deferentia (va, vp) are a pair of slender elongated canals, which lie on the two sides of the middle line, and unite at the inner extremity of the cirrus-pouch, which they penetrate in common. Their walls consist of a very delicate homogeneous but resistant membrane, upon which contractile fibres are disposed, close together and parallel to the axis, (iii.) The cirrus-pouch (cs) is a muscular egg-shaped organ; the upper pole, which receives the united vasa deferentia, is situated above the ventral sucker and separated by only a very slight interval from the dorsal cortical layer, whilst the position of the lower pole is indicated by the porus genitalis (p). The muscles are disposed in two layers, of which the inner is thin and composed of circular fibres; the outer longitudinal layer is much thicker, and its fibres are disposed in bundles; furthermore its apex receives a large number of dorso-ventral fibres. Within the cirrus-pouch the two terminal sections of the male conducting apparatus are situated, (iv.) The first of these is the vesicula seminalis (fig. 1, B, vs; C, g), a large, spindle-shaped dilatation of the canal usually more or less curved upon itself. Its wall is somewhat more complex than that of the vasa deferentia, consisting of a layer of tissue with many nuclei but no distinct cell-boundaries, succeeded by a delicate layer of circular muscular fibres, which is again followed by a layer of longitudinal ones. (v.) The ductus ejaculatorius (fig. 1, C, k), which immediately succeeds the vesicula seminalis, is a long slender tube, disposed in coils, and usually projecting like a papilla into the base of the sinus genitalis. Its walls are furnished with a number of unicellular glands. B. The Female Organs. The female reproductive apparatus may be roughly divided into two portions, that which produces the eggs and that which conveys them to the outside of the body; in the former of these processes three organs take part one producing the germ, another the second ary or food-yolk, and a third the egg-shell, (i.) The germarium or ovary (fig. 1, B, o) is situated between the anterior testis and the ventral sucker, in about three cases out of four on the right hand side of the body. It has the form of a branching tubular gland, the ramification being dichotomous throughout; in most cases the branches are about as large as the stems which give rise to them. The oviduct passes towards the shell-gland, narrowing as it approaches this, and finally unites with the excretory duct of the yolk-glands, (ii.) The yolk-glands (y) of the liver-fluke are paired organs of considerable size; they extend over both lateral areas, to which they impart the opaque appearance and reddish colour above alluded to. They are composed of innumerable small acini, spheroidal in shape and situated in groups on minute ductules, which unite to form a longitudinal canal on either side of the body. These canals are on the whole parallel to the margins of the animal and distant from it about one-fifth of its greatest breadth. At the anterior margin of the testicular area each longitudinal canal gives off a transverse branch, which unites with its fellow of the opposite side in the middle line to form a pear-shaped reservoir, situated just behind the posterior margin of the shell-gland. From this reservoir the common yolk-duct passes forwards in the substance of the shell-gland and there unites with the oviduct. Previously to this, how ever, it gives off a minute canal, which after an upward course opens on the dorsal surface of the animal; it is known as the Laurer-Stieda canal, and its function has been the subject of much discussion. It has been supposed (1) "to serve for copulatory purposes," as has been seen by Zeller (18) in Polystomum, and as is supported by its structure in Axine and Microcotyle, and (2) "to act as a safety tube for the escape of over-abundant or altered vitelline products and spermatozoa," the main argument in support of which is that its calibre is too narrow to admit of copulation taking place by its means; compare Sommer (10), Kerbert (11), Poirier (19), Looss (20), and Lorenz (21). (iii.) The uterus or female conducting apparatus (u) originates at the union of the ducts of the germarium and yolk-gland. Its first portion, which lies within the shell-gland, is a delicate narrow canal, except when it is distended either by eggs or by semen. The median section of the organ is by far the largest both in length and breadth; it occupies almost the whole of the anterior part of the median area of the animal, between the ventral sucker and the shell-gland, and forms four or five large coils lying alternately right and left, which as a rule are filled with completely formed eggs. The third section of this organ includes the coils which lie above and anterior to the ventral sucker; it is some times called the vagina. When it contains eggs these are generally in a single file, and thus give it a moniliform appearance; it lies entirely on the left side of the body, gradually approaching the middle line as it passes forward, until it ends below the cirrus-pouch at the left and posterior aspect of the genital pore (fig. 1, C, e). (iv.) The shell-gland (fig. 1, B, s), which (as its name implies) furnishes the external coating of the eggs, has been already several times mentioned. In the Trematodes, as in the tape-worms, it forms a kind of central point of the female generative system; it is a spheroidal mass of unicellular glands, each of which opens by its own special duct into the commencement of the uterus. The secretion of the shell-gland is liberated in the form of small pellucid droplets, which unite to form drops; afterwards it becomes thick and viscid and of a mahogany brown colour. In this condition the drops are dispersed through the uterus mixed with the secretions of the other genital glands, and they apply themselves to the recently formed eggs, producing a delicate membrane around them. This process is carried on in those coils of the uterus which lie immediately out side the shell-gland, corresponding to the "ootype" described by Van Beneden in other Trematodes.

The eggs undergo a gradual development as they pass along the uterus. The ripe primitive ovum, on entering the female conducting apparatus, becomes coated with a larger or smaller number of spherules of secondary yolk, and then undergoes the process of segmentation which leads to the formation of a morula. At this point it receives the secretion of the shell-gland. The completely formed egg (fig. 1, E) has a length of 13 mm. and is ovoid in shape, with a small lid or operculum at the broader end; its contents consist of a number of roundly polygonal cells, with only a small quantity of secondary yolk remaining among them. All of these but one have a thick granular protoplasm, the exceptional cell having homogeneous and strongly refracting contents. It usually lies immediately under the operculum, and is partly embedded in the other cells. They are often present in the bile-ducts in such quantities as to form a stiff brownish mass resembling wet sand, and the number produced by a single fluke has been estimated at half a million.

The mode of fertilization of the liver-fluke has given rise to much discussion. According to Sommer, the organ which has usually been described as a cirrus or penis is merely the genital sinus evaginated by abnormal pressure (fig. 1, C, d); it is furthermore but ill-adapted to enter either of the canals which could possibly serve as a vagina. He is therefore of opinion that self-impregnation occurs, the external aperture being closed by the oblique muscles, and the semen passing directly from the vas deferens through the genital sinus into the uterus. The whole question of the fertilization of the Trematodes is a matter on which very varied opinions have been expressed, even by authors who have examined the same forms. The assertion of Von Siebold that a direct internal communication exists between the male and female organs has been denied by Stieda (22) and by many subsequent writers, but has been restated by Lorenz (21) and by Zeller in the case of Polystomum integerrimum (18); however this may be, there can be no doubt that self-impregnation does occur in certain cases. The structure of the organs renders it more than probable in some species (see Poirier, 19, p. 582); Zaddach has observed it actually taking place in Distomum cirrigerum encysted in Astacus (23), and a single Polystomum integerrimum has been found in a frog's bladder with sperm in the female passages. Reciprocal fertilization, in which two individuals act both as male and female simultaneously, has been recorded by Zeller in Polystomum integerrimum, by Looss (20) in Distomum clavigerum, and by Cobbold in Distomum campula.

Nervous system.The nervous system consists of a commissure passing round the oesophagus very obliquely, and swelling out into ganglia at three points. Tristomum molæ possesses eyes of an extremely simple type, the retina being merely a ganglion cell (Lang, 24).

Life-History and Development.—The life-history of Fasciola hepatica was worked out independently by Thomas (25) and Leuckart (26); regarding the question of priority see Jackson (27). The development of the embryo can only take place outside the body of the host and at a lower temperature, the most favourable being from 23° to 26°C., at which the process occupies two or three weeks. The free embryo (fig. 2, A) is conical in shape, with a rounded apex, its average length being 0·13 mm. At the broader anterior end is a retractile head-papilla, with the exception of which the body is ciliated all over. The interior of the body is composed of granular nucleated cells, and it contains a double eye-spot, composed of two crescentic masses of pigment. There are also two ciliated funnels forming the rudiments of the excretory system and a granular mass behind the head-papilla, probably representing the digestive tract. The embryo swims actively about, but if it does not succeed in meeting the appropriate host for its next stage of development (Limnxus truncatulus, a small pond snail) its period of vitality seems to be limited to about eight hours.

FIG. 2. Five stages in the life-history of Fasciola Jiepatiea; nil highly magnified. A, The free-swimming embryo. B, A sporocyst containing young redise. C, A young redia, the digestive tract shaded. D, An adult jedia, containing a daughter-redia, two almost mature cercaria?, and germs. E, A free cercaria. The letters have the same significance throughout, c. nearly ripe cercaria;; cc, cystogenous cells; dr, daughter-redia; dt, limbs of the digestive tract; /, head-papilla; h, eye-spots; h, same degenerating; f, germinal cell; /, cells of the anterior row; m, embryo in optical section, gastrula stage; n, pharynx of redia; o, digestive sac; oe, oesophagus;p, lips of redia; q, collar; r, processes serving as rudimentary feet; s, embryos; t, trabecnlse crossing body-cavity of redia;, glandular cells (?); v, birth-opening; tr, to, morals;; /, oral sucker; y, ventral sucker; z, pharynx. (All from Marshall and Hurst after Thomas.)

If it should meet with one of these snails it applies the head-papilla to some part of its surface and begins to bore, twisting round and round on its axis by means of its cilia, the head-papilla becoming pointed and elongated to four or five times its original length. Eventually the tissues of the snail are separated as if by a wedge, and a gap is formed through which the embryo forces an entrance into its body. Here it under goes a metamorphosis, losing its organs of locomotion and becoming what is termed a "sporocyst" (fig. 2, B). This is an elliptical sac, which commonly attains a length of 0·7 mm. Its wall consists of a structureless cuticle, beneath which are external, circular, and internal longitudinal muscle-fibres. These are succeeded by an epithelium, the elements of which vary greatly in size. These sporocysts may be produced by a process of transverse fission. Within the sporocyst rounded masses of cells are formed (morulre), which undergo a process of imagination, producing a gastrula, which again develops by the formation of a digestive tract into what is known as a "redia" (fig 2, C, D). This forces its way through the wall of the sporocyst, which heals up immediately, and then wanders through the tissue of the snail, most commonly finding its way to the liver. If many redife are present the snail usually perishes. The adult redia may attain a length of 1·6 mm. It has an elongated cylindrical form, and near its posterior extremity are two processes directed backwards, which probably serve as aids to locomotion. At the anterior extremity is the mouth, leading into a muscular pharynx, followed by a saccular digestive tract. A ring-shaped thickening is seen a little way behind the mouth, and immediately posterior to this a special aperture for the exit of the germs formed within the redia. About a score of these are usually to be found in all stages of development, the earliest being a rounded mass of cells (morula), which elongates, one end at the same time becoming more attenuated than the other, and gradually forming an elongated tail, while the body becomes oval and depressed (fig. 2, E). Two suckers and the rudiment of the future digestive tract make their appearance. As soon as the "cercaria," this being. the name given to the present organism, has attained this stage of development it emerges from the redia, and by the aid of its suckers and tail wriggles its way out of the host, swimming freely about in the water. Like other cercarire developed in rediae this one has no head-spine, but in mature examples the anterior of the body often exhibits a number of very minute spines. An interesting feature in the animal is the presence of the "cystogenous cells," two lobate masses arranged one on each side of the body. These cells contain small rod-like bodies, whence they have been termed "cellules a batonnets, " and similar bodies have been found in the protective cyst which they excrete; Sonsino (28) has suggested that they may assist in imparting stiffness to this structure, and has noticed that they are more abundant in those forms which encyst in the open air. When the cercaria has swum about for a short time it finds its way to the water-plants, and encysts itself on their stems and leaves. During this process the tail is swung vigorously about, until finally a more violent motion de taches it; at the same time the cells just mentioned throw out a gummy secretion, which rapidly hardens and encloses the cercaria in a kind of case. It is in this condition that the larvae are swallowed by the grazing sheep to form sexually mature flukes in their livers.

The life-history of a typical digenetic Trematode may be summed up as follows: (1) the egg, produced sexually; (2) the ciliated embryo; (3) the sporocyst; (4) the redia, produced asexually; (5) the cercaria, produced asexually; (6) the adult Trematode. Hence it would appear that the digenetic forms have at least one, usually many, asexual generations before the sexual one appears. Tho embryo may form either a sporocyst or a redia, these two forms being distinguished by the presence of a digestive tract and of a special birth-opening in the latter. Within these parent forms the germs may arise from two sources, the cells. which occupy the central region of the young sporocyst or redia, or the epithelium lining the body-walls. "The germs to which a sporocyst gives origin may develop in some instances into sporocysts, in others into redia? or into cercaria?. And it does not seem certain that there is any limit to the possible number of successive generations of redia?. Both cercaria? and redise may occur side by side in the same nurse. The last term in the series is, however, invariably a cercaria."

Fagenstechcr, Ercolani (29), and others have stated that the tail of a cercaria may become a sporocyst and produce germs, but this has not met with general acceptance, and the supposition is not supported by the structure of the tail, which consists of a " con tractile substnnce, occupying the axis and periphery, with large vesicular cells between" (Schwarze, 13). Ercolani (29) has also published striking statements to the effect that the structure of these entozna is so profoundly modified by their habitat that what have been hitherto described as distinct species may be only "local varieties"; thus he finds that Cercaria armata develops in Tropidonotus into Distomum signatum, whilst in Mus musculus and M. dccumamts it becomes a distinct dwarfed form, D. muris.

Pathological and Economic Relations.—Although the number of Trematodes which have been recorded from the human body is about equal to that of the Cestodes, the medical significance of the former is much less than that of the latter, because as a rule they occur in smaller numbers and are less apt to invade organs of vital importance. The Trematodes which have been found in man are—

Fasciola JiepatieJjiftomum lanreolattim, Mehlis, D. ophthalniobitim, Diesing, D. fieteropfiyes, Bilharz, D. crassvm, Busk = Z). buskii, Wedl, D. capense, Ilarley, .... D. tpatulatum, Leuckart, . . . D. endemiatm, Baelz, D. heptitis innacuum, Baelz, D. rathouisi, Poirier (42), Bilharzia hxmatobia, Cobbold, 3fonostomum lentis, Nordmann, Hexathyridivm pinguicola, Treutlcr, H. renarvm, Treutler, a, Linn in the liver. liver. lens of the eye. small intestine. intestine. eggs in the blood. liver. liver. liver. liver. veins of bladder, &c. lens of the eye. ovary. veins.

For the general principles which govern the pathological effects of Trematodes in common with other entozoa, reference may be made to the article Tape-Worms; only a few special cases need be alluded to here. The occurrence of most of the forms in the above list has only been recorded very few times, and in many cases the effects produced were very inadequately studied, so that we can hardly be said to possess a knowledge of their individual pathology. In a case of Distomum lanccolatum which occurred in Bohemia, the liver was enormously enlarged and the contracted gall-bladder contained eight calculi and forty-seven flukes; the symptoms during life were emaciation, pain over the liver, and distention of the abdomen.

The effects produced by Bilharzia hæmatobia are very well defined and exceedingly disastrous. The mature worms in couples inhabit the veins, especially those of the urinary bladder and mesentery; extravasations of blood and villous growths or ulcerations of the mucous membrane of the bladder present themselves, Mid thus the eggs of the parasite find their way into the urine, in which they are evacuated, and can be detected by microscopic examination. With the characteristic presence of the eggs are associated colic, anaemia, and great prostration of the vital powers, more particularly in the later stages; the disease when once fairly established is almost always fatal; see Cobbold (1).

From a practical point of view by far the most important Trematode is Fasciola (Distomum) hepatica, which gives rise to the disease known as "liver rot" in sheep. It is always more or less abundant in certain districts, and it is estimated that in the United Kingdom the annual loss of sheep due to it is not less than 1,000,000. The symptoms are said to be emaciation, tenderness in the loins, harshness and dryness of the wool, and a scaly condition of the skin. On post-mortem examination fluid is found in the peritoneal cavity and the viscera have a blanched appearance; the liver is dark chocolate or sometimes pale in colour, nodular, and uneven, the ducts are thickened and Distomes are found within them. Dead flukes have been known to furnish the nuclei of gall-stones in the gall-bladder. Briefly stated, the principal preventive measures seem to be as follows: (1) destruction of the eggs, and especially abstention from putting manure of rotten sheep on damp ground; (2) slaughter of sheep which are badly fluked; (3) adequate drainage of pastures; (4) an allowance of salt and a little dry food to the sheep; and (5) dressings of lime or salt on the ground to destroy the embryos (Thomas, 25). A series of wet seasons increases the prevalence of the malady, and animals which have been allowed to graze in low-lying ill-drained lands are specially liable to infection facts which are readily explicable on a consideration of the life-history given above.

Systematic Arrangement. The Trematoda, may be classified as follows:—

I. MONOGEXEA, Van Beneden; development direct, that is, without the mediation of nurse forms.

(i.) TRISTOMEJE, Leuckart; body roundish or elongate; posterior extremity never specially developed. Two adoral suckers often present: a large ventral sucker often armed with chitinoid structures. Sexual apertures on the left side or admedian. Laurer-Stieda canal single or double. Ova with a filament at one pole only.

1. Tristoniidaj, Van Beneden. 1. Tristomum, Cuvier; about a dozen genera of previous writers are here included; over 14 species are known, all parasitic on fishes; Taschenberg (30).

2. Monocotylida?, Taschenberg. 1. Calicotyle, Diesing; only species C. kroyeri (31). 2. Pseudocotyle, Taschenberg. 3. Honocotyle, Taschen berg; only one species, it. myliobatis, on the gills of the eagle-ray (Myliobatis aquila).

3. Udonellidse, Johnston. 1. Udonella, Jhnst.; five species, the type being U. caligorum, parasitic on a crustacean (Caligus), which in its turn in fests the holibut (flippoglossus rulgaris).

(ii.) POLYSTOME^E, Lcuckdrt; body elongate, pointed and narrow anteriorly; broad behind and generally provided with special organs of adhesion in the shape of suckers or chitinoid hooks, of suckers or claspers with chitinoid structures. Two adoral suckers in some instances. Sexual apertures median. Lanrer-Stieda canal single or double. Male sexual aperture often armed with chitinoid hooks. Ova frequently provided with two long appendages.

1. Oetobothriida?, Taschenberg. 1. Oetobothrittm, Nordmann; about a dozen genera of various authors arc here included by Taschenberg (30), containing fourteen species, parasitic on fishes, and almost invariably on the gills. 2. Anthocotyle, Hesse and Van Beneden; one species {A. merlucii), found in the hake. 3. Phyllocotyle, Hesse and Van Beneden; one species, from the gurnard. 4. Platycotyle, Hesse and Van Beneden; one species, from the gurnard. 5. Pleurocolyle, Gervais and Van Beneden (=Orubea cocMear, Dies.); one species, from the gills of the mackerel. 6. Diplozoon, Nordmann (see below). 7. Hexacotyle, Blainville; one specie*, from Thynnus brachypterus. 8. Plectanocotyle, Dies.; from the gills of Labrax mucronatus.

2. Polystomidse, Van Boneden. 1. Polystomum, Zeder; two species, best known P. inttgrirrimum (see below); Hexathyridium is probably a synonym. 2. Onchoeotyle, Dies.; five species, from the gills of sharks and rays. 3. Erpocotyle, Hesse and Van Beneden; one species, from the gills of Mustelus Ixvis. 4. Diplobothrium, F. S. Leuckart; one species, from the gills of a sturgeon.

3. Microcotylidae, Taschenberg. 1. Axine, Abildgaard; two species. 2. Microcotyle, Van Beneden; about half a dozen species, all parasitic on the gills of fishes (see below). 3. Gastrocotyle, Hesse and Van Beneden; one species, from the gills of Caranx trachurus. 4. AtpiJogaster, Von Baer (see below). 5. Cotylaxpis, Leidy; one species, occurring;in AnoJonta. 6. Afpidocotyle, Dies.

4. Gyrodactylidse, Van Beneden. 1. Gyrodattylus, Nordmann (see below). 2. Dactylogyrus, Dies.; about twenty species, all parasitic on fishes, mostly on the gills. 3. Tetraonchus, Dies.; three species, on the gills of freshwater fishes. 4. Diplectanum, Dies. 5. Calceostomum, Van Beneden; one species, on the gills of Scisena aqnila. 6. Sphyranura, Wright (34, 45); one species, from the mouth of Menobranchus lateralis.

IT. DIGENEA, Van Ben^icn; one or more non-sexual forms intervene between two successive sexual forms.

(i.) MouosTOMiDjE, Van Beneden; elongate, oval, or rounded in shape; one oral sucker. 1. Monostomum, Zeder; fifty to sixty species in mammals, birds, and fishes; type, J/. mutabite, Zeder, found in the body-cavity and eye of water-birds. 2. Notocotyle, Dies.; N. triseria e, Dies. ( = Monostomum rerrucosum).

(ii.) DISTOMIDJE, Van Beneden; body flattish. more or less leaf-like or elongate; an oral and a ventral sub-median or posterior sucker. 1. Distomum, Retzius (see below). 2. FascioJa, Linn.; three species are known; F. hepatica is described above; F.giganlea inhabits the liver of the giraffe. 3. Bilhania, Cobbold (=Gi/nxcophortis, Dies.); one species (see below). 4. Echinostomum, Dujardin; E. gadorum, Van Beneden, in the intestine of Gadus carbonarius (the coal-fish), an 1 twenty-five other species in the alimentary canal of mammals, birds, and fishes. 5. Amphistomum, Rudolphi; about twenty species in different Verte brates; A. subclavatum (Giize) in the rectum of the frog. 6. Gastrodiscus (?), Leuckart (see also 37). 7. Jlomalogaster, Poirier (38). 8. Gastrothylax, Poirier. 9. Eurycalium, Brock (44), has the excretory vessels dilated into wide chambers (? coelom).

(iii.) GASTEROSTOMID.S, Von Siebold; oral sucker sub-median and ventral; also an anterior sucker. 1. Gasterostomwn, Von Siebold; eight species, all in fishes; larval form Bucephalus (see below).

(iv.) HOLOSTOMID.K, Claus (48); body flattened, and divided into an anterior and posterior part, the former bearing an anterior and ventral sucker; two adoral lobes with glands in connexion, or a circumoral fold with lobes. 1. Holostomum, Nitzsche; twenty-three species, most in waterbirds; //. variabile, in various raptorial birds; larval forms Tetracotyle and Diploatomum. 2. Hemistomum, Dies.; three species, one in the wild-cat, two in birds. 3. Eustemma, Dies.

The true position of the following is doubtful: Nematnbothrium, Van Bene den (9); Didymnzoon, Von Linstow (30); Stichocotyle, Cunningham (39).

FIG. 3. A, biplozoon paraJoxum; two united specimens. B, Polystomum integerrimum; x about 100 (after Zellei ). C, Microcotyle mormyri; x 7. D, E, two views of the chitinous framework of a sucker of Axine belones; highly magnified (after Lorenz). F, Aspidogaster conchicola; x about 25 (after Aubert). G, Gyrodactylm elegans x about 80 (after Wagener).

Diplozoon paradoxum (18) infests the gill of the minnow in large numbers. The eggs hatch in the water, continuing to be attached to the gill by a filament at one extremity. The embryo is elongated oval in shape, and ciliated all over; on its back are two eyes, consisting of a cup-shaped mass of pigment, with a spheroidal lenticular body. It presents also the mouth with two peculiar suckers, the eesophagus and intestine, and the two claspers of the Diporpa. The embryo swims vigorously about until it finds its way to the gill of a minnow, failing which it dies in about six hours. Attached to its host it may live isolated for a considerable time, increasing in size; usually, however, it unites with another individual in a kind of reciprocal copulation (fig. 3, A). One individual by means of its ventral sucker seizes the dorsal papilla of another, and then the two twist across each other so that the sucker of the second seizes the papilla of the first. After this a complete fusion of the individuals takes place, the papilla? and suckers growing together so firmly as to be anatomically inseparable. Both individuals continue to grow and develop a second, third, and sometimes a fourth pair of claspers.

In Polystomum iniegerrimum (18), which inhabits the bladder of the frog, the eggs are developed during the winter and are laid in the spring, when the frogs resort to the water. It appears probable that the worm protrudes its body from the frog and thus deposits the egg directly in the water. The young worm, as it escapes from the egg, which takes place after a lapse of six or eight weeks, measures about 0-3 mm. in length, and swims vigorously about by the aid of a coating of cilia. At its posterior extremity is a rounded disk (fig. 3, B), round the margin of which sixteen delicate hooks are placed at equal intervals. Above the four hindmost of these are two others still smaller and more delicate. Upon the back are situated four eyes disposed in pairs. The mouth is wide and leads into a pharynx, and this into the intestine; two excretory vessels are present, but there is no trace of generative organs. The hindermost pair of suckers is the first to be developed, and they enclose those two hooks which lie at the outer side of the very delicate ones mentioned above, which eventually become the strong terminal hooks of the adult. The other two pairs of suckers are formed in a similar manner, the development of all three being usually completed during the month of July. The young Polystomum attacks not the full-grown frog but the tadpole, entering the gill-cavity and subsequently proceeding to the bladder. Like the frog it requires four or five years to attain sexnal maturity. In certain cases the Polystomum does not migrate; it then becomes prematurely sexual and dies when the tadpole undergoes metamorphosis; under these circumstances the sexual organs are simpler than usual: the testis is simple; the germarium is long and coiled; there is neither prostate nor Laurer-Stieda canal; and the oviduct has no dilated anterior portion.

Microcotyle mormyri, Lorenz (21) (fig. 3, C), has no penis, the semen issuing by an opening posterior to the spiked birth-opening; the vagina opens medially, not marginally. The posterior extremity is pointed. A xine belones, Abildg., resembles it, but is broad and obliquely truncated behind, this margin bearing a row of fifty to seventy peculiar attaching organs, which are of the form of a hand-satchel (fig. 3, D, EX the metal clasp being represented by a complicated chitinous framework. There are four groups of hooks and one ring of the same round the genital open ing. The mouth has a sucker at either side, and above it an ovul body which can be evaginated like the proboscis of a Dendrocele Plaiiarian.

Aspidogaster conchicola (32) is found in the perieardial cavity of the freshwater mussel; it is conical anteriorly with a terminal oral sucker; the ventral sucker Is very large and divided into rectangular areas; the excretory pore is at the pos terior extremity of the body, and the genital organs open on the left side of the fore-part of the animal (fig. 3, F).

Gyrodactylus elegans (33) is found on the fins and surface of the body of the pike, stickleback, and other freshwater fishes, and measures about 5 mm. in length; it is flattened in form and tapers towards either end (fig. 3, G). At the anterior extremity are two lappets, while the posterior is furnished with a subtriangular plate, which bears the organs of attachment in the_ shape of two large curved hooks in its centre and sixteen smaller ones on its circumference. The most interesting peculiarity, however, of this form is to be found in the fact that each embryo before it is extruded (the animal is viviparous) contains another embryo, and this in its turn another, so that three embryonic generations are present simultaneously.

The genus Distomum is by far the most extensive in the group, containing at the present time over 300 species, which occur almost exclusively in Vertebrates; the most important are perhaps D. lanceolatum, which inhabits the same situa tions as Fasciola hepatica, D. clavigerum, from the frog, and D. militare, Van Beneden, from the intestine of the duck. The name Fasciola (Linn.) has the priority over Distomum (Distoma) of Retzius, which, however, has obtained ex tensive currency. The name Fasciola may appropriately be used in a restricted sense for forms which have a branched digestive tract, F. hepatica above de scribed being taken as the type. This separation has not met with general recog nition, although supported by Blanchard and Cobbold (1). Weinland has proposed to substitute the term Dicrocaelium, used by Dujardin, for Distomum, retaining Fasciola for the type-species, but this proposal has not met with acceptance. The Distomes vary in size from forms almost microscopic to those which, like D. ingens, Moniez (35), measure 6 cm. long in alcohol, or even 12-5 cm. in the fresh condition (D. gigas, Nardo). Distomum halosauri, Bell (36), is parasitic upon a deep-sea fish taken in 1090 fathoms. Distomum macrostomum (fig. 4, B) of the woodpecker (Apternus tridactylus) has a remarkable larval form known as Leucochloridium paradoxum, which is parasitic on Succinea putris, and consists of a number of branching threads, from which are developed one or two contractile sacs (fig. 4, C, D). Their growth distends the tentacle until it bursts and the sac hangs outwards.

Fig. 4. A, Bitharzia hxmatobia, the thin female in the gynajcophoric canal of the stouter male; xlo (after Lcuckart). B, Distomum macrostomum, showing the digestive and the greater part of the genital apparatus with the cirrus pro truded; x 30. C, Snail (Succinea), the tentacles deformed by LeucochJoridium; natural size. D, Leucochloridium removed from the tentacle; natural size (after Zeller). E, Bucephalus polymorphus; highly magnified (after Ziegler). F, Portion of a sporocyst containing Bucephali in process of development; x about 50 (after Lacaze-Duthiers).

The threads within the Succinea contain only granular cells> whilst the contractile sac is occupied by an organism ovoid in form, with a thick clear border, the rudiments of two suckers, a digestive tract, and excretory system.

Bilharzia hxmatobia, Cobbold (1), is one of the most dangerous human parasites, and occurs in the blood of the portal vein and in the veins of the mesentery and bladder. The sexes are distinct, the female being from 16 to 20 mm. in length, and somewhat resembling a Nematodc on superficial examination. The male is only from 10 to 14 mm. in length, but much thicker. The surface of the female is covered with fine spines most distinct towards the tail; at the anterior pointed extremity is the oral sucker, from which a narrow opening leads into a wide pharynx, followed by the intestine, which at first forms two branches, these again uniting posteriorly to Ihe generative organs. The ventral sucker is placed only 0-2 mm. behind the oral one, and it is immediately succeeded by a long narrow groove, which extends down the ventral surface and corresponds to the cunalis gynsecpphorus of the male (see fig. 4, A).

The stages in the life-history of Gasterostomum are so remarkable that a short account of them must be given. From the egg there escapes (1) a club-shaped embryo, which in a manner hitherto unobserved enters the freshwater mussel, Anodonta or Unio, where it forms (2) the sporocyst (fig. 4, F); this is several centi metres long and provided with lateral branches; it oecurs chiefly in the liver and ovary, and it is best developed near the skin. The wall of the sporocyst consists of cells, muscles, and perhaps a cuticle; the extremities are pointed and filled with cells, and it is here that growth takes place. Within moniliform dilatations of these ramified tubes are formed balls of cells, each of which develops into (3) a " bucephalus." This organism (fig. 4, E) consists of a small oval body about 0-25 mm. in length with a double tail. At one extremity is a mass of glands with an imagination of the integument, which has been mistaken by many observers for the alimentary canal. This, however, opens about the middle of the body, and consists of a muscular pharynx, a forwardly directed oesophagus, and a simple saccular intestine. The excretory system terminates in an S-s iaped vesicle, which opens posteriorly in such a way that its contraction drives the fluid into the tail, whence it probably finds its exit by osmosis. Traces of genital organs are found in the form of an elongated plug of cells in the hinder fourth of the body, and two rounded masses of undifferentiated cells situated dorsally. The tail is double, and from about 5 to 2-5 mm. long according to its state of contraction. Each hulf consists of a spheroidal basal portion, and an elongated tapering filament. These caudal appendages contain many nucleated connectivetissue cells with fine protoplasmic processes. The larva: swim freely in the water, but sink and perish after about twelve hours, unless they enter the mouth of certain fishes (e.g., Leuciscus erythrophthalmus), when (4) they lose their tails and become encapsuled under the skin. The generative organs now become further developed; cuticular spines and the anterior sucker are formed. If the fish thus infected be swallowed by a pike or perch the cyst is dissolved, and the worms (5) become adult, continue to live in the intestine, and produce eggs. For further details, see Ziegler (12).

Phylogenetic Relations.—The detailed comparisons of Van Beneden (9) and the subsequent researches of others leave no doubt that the Trematoda are closely related to the Ccstoda. A consideration of their peculiarities leads moreover to the opinion that the former are more primitive than the latter; that is to say, the common ancestors of the two groups resembled Trematodes rather than Cestodes. The ancestry of the Trematoda is probably to be sought in types such as the Planarians rather than the Leeches; characters uniting them with the former are the possession of a commonly branched alimentary canal without an anus, bait with a powerful pharynx; the generative system is hermaphrodite, and similar arrangements obtain in the excretory vessels, nerves, and muscles, while histological agreements also are not wanting. Furthermore, certain forms are known which help to fill up the gap between the two groups: Monocelis caudatiis has a discoid posterior organ of attachment, und M. jjrotractilis a true sucker. Such forms as these could scarcely be distinguished from ectoparasitic Trematodes ex cept for their ciliated epithelium (Leuckart, 1). In this connexion, however, it is worth while to call attention to the researches of Fewkes (40) on a marine cercai ia, which had a tail distinctly annelid in character, with bundles of bristles disposed at intervals along it. Compare also Schauinsland (41).

Bibliography. (1) Jackson, in Rolleston's Forms of Animal Life, 2d ed., Oxford, 1887; other important text-books are Leuckart, Parasilen des Alenschen, Leipsic, 1863, new edition and English translation in preparation; Kuchenmeister und Ziirn, Parasiten des Afen&chen, Leipsic, 1881; Cobbold, Entozoa, London, 1864; Id., Parasites, 1879; (2) Rudolph!, Entozoorum Hist. Nat., Amsterdam, 1808-9, and Entozoorum Synopsis, Berlin, 1819; (3) Cuvier, Regne animal, Paris, 1829; (4) Von Siebold, Arcliivf. Naturgesch., i., 1835; (5) Von Baer, Nova Acta Acad. Cses. Leap., xiii., 1826; (6) Steenstrup, Alternation of Generations, Huy Society, 8vo, London, 1845; (7) Pagenstechcr, Trematodenlarven und Trematoden, Heidelberg, 1857; (8) Diesing, Systema Jlelminthum, Vienna, 1850; (9) Van Heneden, "Versintestinaux," Comptes Rendus, Paris, 1861; (10)Sommer. Ztschr. iciss. Zool., xxxiv., 1880; (11) Herbert, Archie f. mikr. Anat., xix., 1881; (12) Ziegler, Ztschr. wiss. Zoo!., xxxix., 1883; (13) Schwarze, Op. cit., xliii., 1886; (14) Metschnikoff, Quart. Jour. Micr Sci., xxiv., 1884; (15) Fraipont, Arch. d. Biol., i., 1880, ii.. 1881; (16) Pintner. Arb. Znol. Jmt. Vien, iii., 1880; (17) Van Beneden and Lankester, Zool. Anz., iv., 1881, v. 1882; (18) Zeller, Zlschr. wiss. Zool., xxii., 1872, xxvii., 1876; (19) Poirier, Arch. Zool. Exper., iii., 1885; (20) Looss, Ztschr. wins. Zool., xli., 1885; (21) Lorenz, Arb. Zool. lust. Wien, i., 1878; (22) Stieda, Reiehert, and Du Bois Reymond's Archiv, 1881; (23) Zaddach, Zool. Anz., iv., 1881; (24) Lang, Mitth. Zool. Stat. Neapel, ii., 1881; (25) Thomas, Quart. Jour. Micr. Sci., xxiii., 1883, also Jour. Roy. Agric. Soc., xix., 1883; (26) Leuckart Zool. Anz., v., 1882; (27) Jackson, Op. cit., vi., 1883: (28) Sonsino, Arch. Jtal. Biol., vi., 1885; (29) Ercolani, Mem. Acad. Sci. hut. Bologna, [4], ii., 1882, iii., 1883, also abstract, Arch. Jtal. Biol., i., 1882; (30) Taschenberg, Ztschr. gesammt. Naturw.,i., 1879; (31) Wierzcjski, Ztschr. wiss. Zool., xxix., 1877; (32) Huxley, Anat. Incert. Anim., London, 1877; (33) Wagener, Arch. f. Anat. v. Phys., 1860; (34) Wright, I roc. Canad. Jnst., i., 1884; (35) Moniez, Bull. Soc. Zool. France, xi., 188fi; (36) Bell, Ann. and Mag. Nat. Hist., [5], xix., 1887; (37) Lejtenyi, Abhandl. Senck. Gesellsch., xii., 1881; (38) Poirier, Bull. Soc. Philom. Paris, (7), vii., 1883; (39) Cunningham, Trans. Roy. Soc. Edin., xxxii., 1884; (40) Fewkes, Amer. Jour. Sci., (3), xxiii., 1882; (41) Schauinsland, Jena Z.-ilschr., xvi., 1883; (42) Poirier, Arch. Zoul. Exper., [2], v., 1887; (43) Von Linstow, Archiv f. Naturgesch., xliii., 1877; (44) brock, Gottinger Nachrichten, 1887; (45) Wright and Macallum, Amer. Jour. Morph., i., 1887. (W. E. HO.)

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1. These figures refer to the bibliography at the end of the article.