1911 Encyclopædia Britannica/Trematodes
TREMATODES, or flukes (as they are called from their fish-like shape), one of the three classes that compose the phylum Platyelmia (q.v.). They are flattened organisms provided with two or more suckers, hence their name (τρηματώδης, pierced with holes), and are exclusively parasitic both in their earlier and mature stages of life. Their structure has undergone little degeneration in connexion with this habit, and may be compared organ for organ with that of the Planarians (q.v.). The chief peculiarities that distinguish Trematodes from their free-living allies, the Turbellaria, are the development of adhering organs for attachment to the tissues of the host; the replacement of the primitively ciliated epidermis by a thick cuticular layer and deeply sunk cells to ensure protection against the solvent action of the host; and (in one large order) a prolonged and peculiar life-history. The only organs that exhibit any sign of degeneration are those of sense, but in the ectoparasitic Trematodes simple eye-like structures are present and perhaps serve as organs of temperature. The class as a whole is linked to the Turbellaria not only by its similarity of structure, but by the intermediation of the singular class the Temnocephaloidea (see Planarians), which in habit and in organization form an almost ideal annectant group.
External Characters.—The body, which varies in length from a few millimetres to a couple of feet, is usually oval and flattened. In certain genera the margins are infolded either along their whole length (the male of Schistostomum haematobium; fig. 9, A) or anteriorly only (Holostomidae). The anterior third of the body is attenuated and sharply marked off from the bulbous trunk in Didymozoon. Trematodes never exhibit segmentation, though a superficial annulation may occur, e.g. in Udonella.
The ventral surface is characterized by one or more suckers and apertures. The mouth lies usually in the centre of the anterior and sub-terminal sucker or between two adoral suckers, but in Gasterostomum and its allies it is mid-ventral. A second sucker of variable size and shape lies behind the oral one. In the ectoparasitic Trematodes this post-oral sucker is a complex disk placed near the hinder end and provided with suckerlets, hooks and a musculature arising from a special skeleton. In the majority of endoparasitic forms it is merely a muscular disk just behind the mouth; but in the Aspidocotylea this sucker forms a muscular ribbed sole extending over the greater part of the ventral surface (fig. 7).
The anterior and posterior ends of the body are well defined. The former is specially modified in a few genera in a manner analogous to the “proboscis” of certain Rhabdocoel Turbellaria. Thus in the recently discovered arctic genus Prosorhynchus the muscular and glandular extremity is protrusible, but in the allied Gasterostomum this organ is represented by a sucker with fimbriated or tentacular margins. Another form, Rhopalophorus, has two cephalic tentacles that are retractile and covered with hooks. The chief genital pore is placed anteriorly between the oral sucker and the ventral one, and is posterior only in Holostomidae, Gasterostomidae and a few Distomidae. Usually this aperture is median, but occasionally asymmetrical. Both male and female gonoducts open through a common atrium to the exterior by this pore, but in three bisexual genera the male and female ducts are developed in separate individuals (Bilharzia, Didymozoon, Koellikeria) . A single or paired accessory gonopore is met with in many Trematodes just as in certain Turbellaria (e.g. Cylindrostomum, Trigonoporus) . This accessory pore is not of uniform significance. In ectoparasitic Trematodes it is paired and usually ventral (fig. 4 B, v), but the two apertures may run into one, and may also open dorsally (Hexacotyle) . In this group, the accessory gonopore is the opening of the “vagina,” in contradistinction to the median and atrial opening of the uterus which is a “birth-pore.” In most endoparasitic Trematodes the accessory gonopore is a median and dorsal structure. It is the opening of Laurer's canal and is homologous not with that of the “vagina” just mentioned, but with a totally distinct structure—the “yolk-receptacle”—which in ectoparasitic forms discharges into the gut instead of to the exterior (see fig. 3).
The excretory pore is terminal and posterior in endoparasitic forms: paired, anterior and dorsal in the ectoparasitic class.
Parasitic Habits.—The Trematodes with few exceptions select a vertebrate for their host. Speaking generally each species of parasite has a particular host, upon the blood of which it nourishes itself and matures its reproductive organs. This strange partiality is now to some extent intelligible. It has been shown in the mammals that blood-relationship, in the strict and literal sense, holds good. The blood of most species behaves differentially towards precipitants, and it is therefore conceivable that when blood is used as food and is elaborated into special compounds for the nutrition of the reproductive organs of a parasite, these specific or larger differences in the blood of animal hosts may prevent the ripening of the gonads of a widely diffused parasite and only one particular kind of blood prove suitable. It would seem that the Trematodes present various degrees of such adaptation, for whilst some—e.g. the common liver-fluke (Distomum hepaticum)—mature equally well in the bile-ducts of a man as in those of a sheep or rabbit, others and in fact the majority are restricted apparently to one host. It must, however, be borne in mind that a Trematode may develop in an “aberrant” manner in one host and “normally” in another; and unless we knew the initial stock, the two forms would be regarded as distinct species, each with its own host.
The position of the Trematode on its host is of far-reaching importance. If ectoparasitic and attached to the skin, apertures or gills, the Trematode adopts more elaborate adhesive organs and undergoes a less complex development than are required for the endoparasitic members of the class. The latter are almost invariably swallowed by their host in an immature state with its food, and front the stomach or intestine they work their way into the lungs, liver, body-cavity or blood vessels. These endoparasites have a peculiar larval development, the results of which are to increase their numbers and enhance the opportunity of their gaining the necessarily remote station in some fresh individual host. It is usual to consider the ectoparasitic habit as leading up to the endoparasitic one. From what we know of the Platyelmia, however, it is more probable that the two are quite independent and have been evolved separately.
The influence of Trematodes on their hosts is a varied one. Probably all of them secrete an active poison by the aid of their glands, but the effects of these substances are not readily perceptible. In addition to this, they constitute a drain upon the blood which may result in anaemia. If present in large numbers they may give rise to obstruction of the liver-ducts or to inflammation of other tissues. The most important of the Trematodes in its effect on man is Schistostomum (Bilharzia). This parasite is one of the plagues of Africa. In Egypt 30% of the natives are affected by haematuria which arises from congestion of the bladder consequent upon the attacks of this animal. The noxious influence of Trematodes is, moreover, not confined to their mature phase of life. The rapid multiplication that takes place in the larval stage of nearly all endoparasitic forms affects the tissues of the “intermediate” host in which they live. In most cases this is a mollusc, and the larvae bore their way into the most diverse organs, often accumulating to such an extent as to give a distinctly orange colour to an otherwise colourless tissue, and to cause the demolition of particular structures e.g. the liver and gonad. Perhaps the most remarkable of these effects is that produced by the larvae of Gasterostomum. These organisms live in cockles, oysters and other lamellibranchs and they so affect the gonads of these molluscs as to castrate and sterilize their host. A different but still more interesting result is produced by these Trematode larvae on certain lamellibranchs. The production of pearls by oysters and mussels is common knowledge, but it is only recently that the origin of pearls has been traced and admitted to be due to inflammation set up by a parasite. In the case of the pearl oyster this parasite is a cestode larva, but in the less valuable but no less genuine pearl produced by Mytilus, &c., the nucleus is a Trematode-larva (Jameson).
Structure.—The anatomical structure of the Trematodes is fairly uniform (Braun). The body is enveloped by a thick striated protective cuticle which is frequently raised into hooks or spines. In Dirtomum acanthocephalum the cuticle forms circlets of large and small hooks at the anterior end, somewhat as in Cestodes. The epidermis has lost its connected epithelial character and its cilia, and the isolated cells have become sunk inwards retaining their attachment to the innermost cuticular layer by slender processes. This layer also forms the attachment for the muscles, of which there are two enveloping coats, a circular and a longitudinal layer and also dorso-ventral fibres. The muscles are remarkable for two reasons. They occasionally exhibit striation and originate from large branched cells, the nucleus and unmodified part of which form conspicuous elements. The digestive system consists of a simple or bifurcated sac, opening through the mouth by means of a “pharynx bulbosus,” adapted to act primarily as a sucker, and secondarily, when drawing blood, as an aspirator. Between the blind gut and the cuticle is a reticular branched tissue which forms the chief substance of the body. This is the mesenchyma. As in other Platyelmia the elements of this tissue undergo the most varied differentiation. The main mass of it forms a spongy vacuolated matrix, but some of the cells become glandular and open by pores on the surface of the cuticle, others become “flame-cells” (fig. 2, D) and canaliculi of the excretory system as in Turbellaria, others again muscle-cells. Embedded in the matrix lies the complex genital apparatus composed usually of both male and female reproductive organs (fig. 2, B). The former consist of one pair or more of vesicular testes communicating by fine ducts with a vesicula seminalis. From this point a glandular tube runs to the genital atrium and during the last part of its course is converted into an reversible hooked “cirrus” or penis. The female organs consist of distinct ovaries and yolk-glands, the ducts of which unite in the neighbourhood of a “shell-gland” or “ootype.” Here the two elements, ovum and yolk-cells, are surrounded by a shell of operculate or of spindle-capped types. Coincidently, to allow of fertilization and the escape of excess of yolk, and of spermatozoa, other accessory ducts open at this point. Thus in ectoparasitic Trematodes, the paired vagina transmits spermatozoa to the egg: and a canal carries off yolk from this point of junction either to the gut for resorption or to the exterior for exudation. This duct (Laurer's canal) is sometimes rudimentary and ends blindly beneath the skin. The fertilized ova, provided with yolk and a shell, are next transferred to the “uterus” along which they travel to the exterior. In the endoparasitic trematodes the uterus is the only passage by which fertilization can be effected, and in cases of cross and self-impregnation this duct is physiologically a vagina. Lastly the nervous system is well developed and consists of a pair of well-marked and interconnected ganglia placed near the anterior end and dorsal to the oesophagus. From these ganglia, nerve-tracts provided with ganglion-cells are given off. Of these there are three on each side of the body; a large ventral tract, smaller lateral strands and dorsal ones. From these tracts a plexus of nerve-fibres is developed in connexion with the musculature and cuticle.
The Trematodes are divided into three orders, primarily distinguished by the character of their suckers, viz.: Heterocotylea, Aspidocotylea and Malacocotylea.
Order 1. Heterocotylea.—Ectoparasitic Trematodes, in which a large posterior adhesive apparatus is present and is usually accompanied by a pair of suckers placed anteriorly in relation to the mouth. The large posterior organ of attachment is usually wheel-shaped and provided with hooks; but the ridges may become separated into a number of independent suckers set on a disc or “cotylophore.” Eye-spots are general and the nervous system maintains a primitive diffused condition. The excretory system opens to the exterior by a pair of dorsal pores at the level of the pharynx. The eggs are comparatively few, and development is direct, the embryo after reaching its host remaining attached to it for life.
All the members of this order are parasitic on aquatic vertebrates and in rare cases derive their food from a vertebrate host indirectly by means of another invertebrate parasite (e.g. Udonella occurs on parasitic Crustacea). They are transparent leaf-like organisms and may often be found attached to the skin, mouth, nostrils or gills of fish; on the skin and bladder of Amphibia; and on those of certain Reptilia. Polystomum integerrimum (fig. 5) occurs commonly in the “bladder” of frogs and toads; Diplozoon on the skin of the minnow; Gyrodactylus (figs. 5, 6) on the gills of various fresh-water fish; and a large number of genera occur on the skin, cloaca and gills of Elasmobranchs and other marine fish. They ingest the mucus and, to some extent, the blood of their host by the aid of a sucking pharynx through which the food passes into the bifurcated alimentary sac and its branched caeca.
The life-history of this order offers many points of interest. The eggs are stalked and provided with chitinoid often operculate shell. Each shell contains a single ovum and a mass of yolk-cells. In most cases the eggs are attached to the host, but in Polystomum the eggs are laid in water. The egg of Gyrodactylus develops in the body of the parent.
The further history of the animal is only known in a few cases. Polystomum hatches out six weeks after ovi-position as a minute (.3 mm. long) larva capable of swimming freely for a short time by the aid of five girdles of ciliated cells. If in the course of the first twenty-four hours this larva meet with a tadpole it attaches itself at once and undergoes further development. If unsuccessful it dies. In the former case the larva creeps along the tadpole until it reaches the branchial opening into which it darts, fixes its sucker, and then throws off its cilia. Its further development takes place partly in the branchial chamber and partly in the bladder, which it reaches by travelling the whole length of the alimentary canal. In the former position the suckers are developed and growth proceeds for 8 to 10 weeks until the metamorphosis of its host. In the bladder it remains for three years before attaining maturity. Sometimes the Polystomum-larva attaches itself to a young tadpole, and in that case grows so rapidly as to become mature in five weeks. These Polystomum deposit their eggs in the branchial chamber and die at the metamorphosis of their host. They differ structurally from the normal form in being capable of self-fertilization only, and in the shape and details of their spermatozoa.
(After v. Nordmann. From Cambridge Natural History, vol. ii. “Worms, &c.,” by permission of Macmillan & Co., Ltd.)
Fig. 6.—Gyrodactylus elegans from the fins of the Stickleback; emb. embryo.
The life-history of Diplozoon (fig. 5) is remarkable in that two larvae (the so-called Diporpae) unite and fuse permanently into an X-shaped organism. Unless this occurs, the development of the larvae is soon arrested. The ciliated stage is only capable of free life for five or six hours, and if at the end of that time it has not encountered and attached itself to a minnow, it dies. If successful, the larva throws off its cilia and develops a dorsal papilla, a median ventral sucker and an additional pair of lateral suckers. Then the Diporpa stage is attained. This stage is capable of isolated existence for two or three months but remains immature. Should it, however, encounter another Diporpa, the mid-ventral sucker of either is applied to the dorsal papilla of the other, and complete fusion takes place across the junction. The compound organism now develops two sets of inter-connected genitalia and becomes a Diplozoon.
Gyrodactylus produces only one large egg at a time and this develops in situ into an embryo: but within this embryo another appears before the first leaves the parent. This anomalous phenomenon is still obscure, for we do not yet know whether the second embryo is developed sexually or asexually from the first. Von Linstow has indeed suggested that Gyrodactylus is a larval form capable of reproduction by an asexual method.
Order 2. Aspidocotylea.—Endoparasitic Trematodes provided with a large ventral sucker which is almost co-extensive with the lower surface of the body and is divided into rectangular compartments. The alimentary sac is simple and devoid of caeca. The development is direct.
These Trematodes occur in the alimentary canal and adjacent organs of Mollusca, the gall-bladder of Chimaera, and the intestine of Chelonia and of certain fish. Aspidogaster conchicola is a form not uncommon in Anodon, Unio and certain fresh-water Gastropods. When young it is found in the intestine, but becomes mature in “Keber's organ” and the pericardium. An allied form (A. margaritiferae) occurs in the pericardium of the Ceylon pearl-oyster (9).
(After Monticelli. From Lankester's Treatise on Zoology, part iv.)
Fig. 7.—Aspidogaster conchicola; ventral aspect; a mouth; b, marginal sense organs.
This order differs in several points from the preceding one. The excretory system is highly developed and opens at the posterior extremity by a paired muscular bladder. The testis is a single compact organ. From the oviduct a long duct full of yolk passes backwards almost to the hinder end of the body and ends blindly in a globular dilatation just below the skin. This structure is regarded as the homologue of a canal (Laurer's canal) which in the Heterocotylea opens into the intestine and so gets rid of the excess of yolk. The life-history of the order is almost unknown, but at the time of hatching the young Aspidocotylean has an oral sucker at the anterior extremity and an equally simple post-oral one at the other, thus resembling the members of the next order. Subsequently the body grows backwards and the ventral sucker comes to occupy a relatively more anterior position. Concomitantly its cavity is sub-divided by transverse ridges into a single row and later on into paired rows of compartments. A curious form (Stichocotyle) described in an immature condition by Cunningham from the lobster and Norway lobster probably belongs to this order.
Order 3. Malacocotylea (Distomae, Leuck: Digenea v. Ben.). Endoparasitic Trematodes with a variable adhesive apparatus. The oral sucker may alone be present (Monostomidae), more usually a second is developed on the under surface, but may be mid-ventral (Distomidae) or terminal. It is posterior (Amphistomidae), or anterior (Gasterostomidae). In addition to these suckers the sides of the anterior region may become infolded and give rise to an accessory adhesive organ (Holostomidae). In all these families spines and glandular papillae may be super-added. The intestinal sac has become bifid and is usually devoid of branches. The excretory system is highly developed; the larger collecting ducts are elaborately looped and open posteriorly by a single terminal aperture. A canal (Laurer's canal) leads from the oviduct or yolk-duct to the dorsal surface. The development is indirect. From the egg a larva arises. This enters a temporary host. Here it gives rise by a peculiar process to numerous individuals of a second larval form, and these usually produce a third form from which the minute immature Trematode is developed. In this manner a single egg may give rise to a large number of sexual individuals. The larvae usually live in Molluscs, the mature worm in vertebrates, and the immature but metamorphosed Trematode in either host and also in pelagic and littoral marine and fresh-water invertebrates.
The Malacocotylea occur in all classes of vertebrates. They are usually found in the alimentary canal or its appendages but occasionally work their way into the serous cavities, nervous system and blood vessels. Fourteen species belonging to five genera have been found in man, but only one [Schistostomum (Bilharzia) haematobium] is of serious medical importance, the others being rare and occasioned by want of cleanliness and close association with infected domestic animals. Domestic animals suffer periodically to a much greater extent. The liver-fluke (Distomum hepaticum) unlike most Trematodes flourishes in a wide range of hosts and infects man, horse, deer, oxen, sheep, pig, rabbit and kangaroo. Sheep, however, suffer most from this parasite and from the allied D. magnum. The former fluke is found in Europe, North Africa, Abyssinia, North Asia, South America, Australia and the Hawaiian Islands; the latter in the United States. Wet summers are followed by an acute outbreak of liver-rot amongst sheep and this, together with the effects of other diseases that accompany wet seasons, cause the death of vast numbers of sheep, the numbers from both sources being estimated in bad years at from 1½ to 3 millions in England alone. The anatomy of Distomum hepaticum is fully described in many accessible memoirs [Sommer (10), Marshall and Hurst, Braun (3)]. It has been shown that this parasite feeds upon the blood, not the bile of its host, though it occurs mainly in the bile ducts.
The life-histories of the Malacocotylea form the most interesting feature of the order. The majority of species are hermaphrodite and many are capable of self-impregnation. In these, the male organs ripen before the ova and spermatozoa may pass into the uterus before the external pore is formed (Looss). A few species, however, are bisexual, e.g. Schistostomum (Bilharzia) haematobium in which the male is larger than the female and encloses the latter in a ventral canal; Koellikeria filicolle Rud (Distomum okenii, Köll) which also occurs in pairs, a large female and a small male being found together encysted in the branchial chamber of Brama raji: and Didymozoon thynni (Monostomum bipartitum) which occurs in pairs fused for the greater part of their length and only free anteriorly; the larger individual is the female.
The egg consists of a fertilized ovum and a mass of yolk-cells. Segmentation takes place during its passage down the uterus. The result of this process is a minute ovoid embryo consisting of a solid mass of cells surrounded by a follicle of flattened yolk-cells. The central mass soon becomes differentiated into an outer epidermal and a dermal layer of flat-cells. Some of the central cells remain in clumps as “germ-balls,” others form a mesenchyma in which “flame-cells” arise; others again give rise to muscles; and at the thicker end of the body, rudiments of the brain and digestive system are observable. A pair of “eye-spots” develops immediately over the brain. If the egg with its contained embryo falls into water with the faeces of the host the larva hatches out and swims freely for a time. In dry localities or in the absence of the intermediate host (usually a mollusc) this larva soon dies. If, however, it encounters the host the larva bores its way in, and attacks the liver, mouth or gonad in which it comes to rest. In all Malacocotylea except the Holostomidae the ensuing change is a degenerative one. The cilia are lost, the eye-spots disappear, the digestive sac vanishes and the larva becomes a sac or “sporocyst” full of germ-cells. The origin of these cells is a moot point. According to some writers (Leuckart) they are derived from undifferentiated blastomeres, other authorities (Thomas, Biehringer, Heckert) trace them to the parietal cells of the larva. These cells aggregated in masses become the bodies of another generation of larvae within the sporocyst. By a series of changes similar to those by which the primary larva arose from a segmented egg, so do these secondary larvae or “rediae” arise from the germ-cells or germ-balls within the sporocyst. The structure of a redia, however, is an advance on that of its parent. Though not possessing eyes or cilia, it has a pharynx and short straight digestive sac; and its mesenchymatous cavities are filled with germ-balls in various stages of development. The movements and activity of the redia cause it to burst the wall of the sporocyst. It escapes into the adjacent tissue and there gives rise either to one or more generations of rediae or at once to a new type of organism—the cercaria. What determines the origin of the cercaria rather than a new generation of rediae is unknown. It originates from germ-balls by a differentiation similar in general to that already described, though profoundly different in detail. The cercaria is just visible to the naked eye and has an oval or discoidal body and usually a long tail of variable form. The tail may be a simple hollow muscular process or provided with stiff bristles set in transverse rows, or divided into two equally long processes, or finally it may form a large vesicular structure. The body contains in miniature all the organs of the adult fluke, including the gonads and in addition “eye-spots,” a stylet, rod-cells and cystogenous cells. The latter structures are only employed for an interval before the final host is entered.
The number of cercariae produced by the pullulating rediae in a single water-snail is immense, and as they are emitted at a given period or a few successive periods, the snail at these times appears enclosed in a cloud of whitish flocculent matter. The cercaria swims freely for a time and either encysts directly on grass or weeds or it enters a second host which may be another mollusc, an insect, crustacean or fish, and then encysts. In this process it is aided by the stylet with which it actively bores its way, throws off its tail and then, surrounding itself with the secretion of its cystogenous cells, comes to rest. The further development of the cercaria is dependent on the weed or animal in which it lies being eaten by the final host which is usually a predaceous fish or one of the higher vertebrates. When that occurs, the cyst is dissolved and the minute fluke works its way down the alimentary canal into some part of which it inserts its suckers and commences to feed on the blood of its host. Occasionally the fluke migrates into the blood vessels and may reach the lungs, kidneys, urethra and bladder. In the course of a few months it attains full size and maturity and probably in most cases dies in the course of a year after having given rise to another generation of larvae.
A few special cases of this general description of the life-history may be mentioned. The liver-fluke (Distomum hepaticum) passes through its larval stages in the water snail Limnaea truncatula in Europe; in L. oahuensis in the Hawaiian Islands; in L. viator in South America and in L. humilis in North America: and is eaten by sheep during its encysted stage attached to herbage. Distomum macrostomum, which occurs in various birds, produces a very curious sporocyst in the body of the snail Succinea putris. This sporocyst assumes a branched structure and penetrates into the tentacles of the snail (fig. 9, c, d). In this situation it becomes much swollen and banded with colours, and produces a large number of ecaudate cercariae. The attention of birds is speedily attracted to the snail by this appearance and by the peculiar movements which the worm executes, and the passage of the parasite into its final host is advantageously effected. In many cases it appears that only the brilliantly coloured tentacle is pecked off by the bird, and as the snail can easily regenerate a new one, this in turn becomes infected by a fresh branch of the sporocyst ramifying through the snail and thus a new supply of larvae is speedily provided (Heckert).
The life-history of Schistostomum haematobium is still unknown, but the difficulty in obtaining developmental stages in any of the numerous intermediate hosts that have been tried suggests that the ciliated larvae may develop directly in man and either gain access to him by the use of impure water for drinking or may perforate his skin when bathing. Experiments on monkeys have, however, given negative results.
The life-history of the Holostomidae differs from that of the Distomidae in an important regard. These Trematodes live chiefly in the intestine of aquatic birds or reptiles. The ciliated larva escapes from the egg into the water and enters an intermediate host (leech, mollusc, arthropod, batrachian or fish) where it undergoes a metamorphosis into a second stage in which most of the adult organs are present. In this condition they remain encysted as immature flukes until eaten by their final host.
The cycle of development taken by the Malacocotylea has been generally regarded as an alternation of one or more asexual generations with a sexual one. The question, however, is complicated by the uncertain nature of the germ-cells in the sporocysts and rediae. Some authors looking upon these as parthenogenetic ova regard the developmental cycle as one composed of an alternation of parthenogenetic and of sexual generations. Others again consider that the whole cycle is a metamorphosis which, beginning in the Heterocotylea as a direct development, has become complicated in the Holostomidae by a larval history, and finally in the Malacocotylea has acquired additional complexity by the intercalation of two larval forms, and is thus spread over several generations.
Literature.—R. Leuckart, Die Parasiten des Menschen (1889-1894), vol. ii.; M. Braun, “Trematodes,” Klassen u. Ordnungen des Tierreichs (1889-1893), vol. iv. (Monograph), and The Animal Parasites of Man (London, 1906); W. B. Benham in Lankester's Treatise on Zoology (1901), pt. iv.; A. Heckert, “Untersuchungen über die Entwicklung und Lebensgeschichte des Distomum macrostomum,” Bibliotheca zoologica, Heft 4 (Cassel, 1889); J. T. Cunningham, “On Stichocotyle nephropsis,” Trans. Roy. Soc. Edin. (1887), vol. xxxii.; A. Looss, “Die Distomen unserer Fische und Frosche,” Bibliotheca zoologica (1894), Heft 16; H. L. Jameson, “Pearl-formation,” Proc. Zool. Soc. p. 140 (London, 1902); A. E. Shipley and J. Hornell, “Parasites of the Pearl Oyster,” Report on the Pearl Oyster Fisheries of the Gulf of Manaar, The Royal Society (1904), pt. ii. pp. 90-98; F. Sommer, “Anatomy of Liver-fluke,” Zeit. f. wiss. Zoologie (1880), vol. xxxiv.; Thomas, “Development of Liver-fluke,” Quart. Journ. Mic. Sci. (1883), vol. xxiii.; Jägerskiold, Fauna arctica.