The submucosa (Fig. 157) lies between the muscular layer externally and the epithelial lining internally, and is characteristically developed in the stomach, and even more so in the intestine. Histologically, it consists of a framework of connective tissue, enclosing in its meshes masses of leucocytes (lymphoid tissue), some of which are amoeboid and migratory, and may even be found between the cells of the intestinal epithelium (including in some instances the cloacal epithelium), probably actively participating in the transmission of food material from the alimentary canal to the lymphatics and blood-vessels; while other and somewhat similar, but larger, leucocytes (phagocytes), are concerned with the elimination of waste substances or noxious micro-organisms. In addition to the diffused lymphoid tissue of the submucosa, special rounded or oval, and sometimes encapsuled, masses of this tissue (lymph follicles) are common in the intestinal wall (Fig. 157) of Acipenser, the Dipnoi and some Elasmobranchs, and are perhaps the only representatives in Fishes of the solitary follicles or "Peyer's patches" of the higher Vertebrates. A mass of lymphoid tissue exists in the axis of the spiral valve of Acipenser, which has been compared with a similarly situated structure in Lepidosiren.[[238]] In some Elasmobranchs a large lymphoid organ is imbedded in the submucosa of the oesophageal wall, while a local thickening of the tissue is met with in the pyloric sphincter. Protopterus is remarkable among Vertebrates for the extraordinary development of lymphoid tissue,[[239]] which, apart from its distribution in the submucosa, is abundantly present between the longitudinal and circular muscle layers, and the peritoneal and muscular coats of the intestine.
In addition to the lymphoid tissue the submucosa contains non-striated muscle cells and plexuses of capillary blood-vessels, which in certain Loaches (e.g. Misgurnus), where intestinal respiration occurs, extend between the cells of the intestinal epithelium. A network of lymphatic spaces or vessels surrounds the blood-vessels. In some Elasmobranchs the small arteries of the submucosa of the stomach are provided with singular sphincter muscles, which occasionally encircle both the artery and the corresponding vein.[[240]]
The lining epithelium differs considerably in character in different portions of the alimentary canal. The epithelium of the mouth, pharynx, and anterior section of the oesophagus is often squamous and is succeeded in the hinder part of the oesophagus, and in the stomach and intestine, by a columnar epithelium. As a rule the epithelium of the rectum is also columnar, but in Elasmobranchs it may become squamous. Goblet cells are of very frequent occurrence throughout the whole length of the alimentary canal, from the mouth to the rectum inclusive, interspersed between the superficial epithelial cells; in the same position in the intestine migratory leucocytes have been found. The primitive ciliation of the Vertebrate alimentary canal is retained to a greater or less extent in many Fishes, and is sometimes, but not always, associated with a feeble development of the musculature. In the larval form of Petromyzon (Ammocoetes), the whole canal is ciliated except the pharynx and rectum; but in the adult ciliation is retained only in places which gradually become fewer as the rectum is approached. In the Myxinoids, however, cilia are said to be absent.
In the Dipnoi (e.g. Protopterus) the epithelium of the stomach and intestine is largely ciliated, but in Elasmobranchs, ciliation is usually restricted to the posterior portion of the oesophagus and the edge of the spiral valve. Among the more generalised Teleostomi (e.g. Acipenser, Lepidosteus, Amia), the oesophagus, stomach, and intestine may be ciliated, but to an extent which varies in different genera. The pyloric appendages, when present, are also more or less extensively ciliated. In Teleosts, however, the recorded instances of ciliation are relatively rare. Nevertheless, ciliated epithelium has been found in the intestine of a few species (e.g. Rhombus aculeatus and Syngnathus acus), and also in the pyloric appendages; in the stomach (e.g. Perca and Esox), and even in the oesophagus (e.g. Perca).
The mucous membrane, including the submucosa, is frequently developed into variously arranged ingrowths projecting into the lumen of the alimentary canal; these are generally of the nature of longitudinal or transverse ridges, or a combination of the two, giving rise to retiform structures. The simple longitudinal folds, which are sometimes found in the oesophagus, stomach, and rectum, often disappear on distension, and probably merely provide for the enlargement of these cavities during the deglutition of relatively large prey, or for the accumulation of faeces. On the other hand, the permanent and often complicated folds of the intestinal mucous membrane are probably related to an increase in the secretive or absorptive area of this portion of the alimentary canal. In the stomach the mucous membrane is usually smooth, rarely, as in the "Electric Eel" (Gymnotus), reticulate. In the intestine the folds assume a highly characteristic and often complicated disposition.[[241]] In the Cyclostomata the folds are simple and longitudinally arranged. In Elasmobranchs (Fig. 158, A), obliquely transverse folds are present in addition, and, uniting with the longitudinal ridges, bound linear depressions.
Fig. 158.—The intestinal mucous membrane of different Fishes, to show the transition from simple longitudinal and transverse folds to crypts. A, Of an Elasmobranch; B, C, and D, of various Teleosts. (After Wiedersheim.)
In various Teleostomi (Fig. 158, B, C, D), the union of the two series of folds becomes more or less retiform, and the network of intersecting ridges bounds a series of deep tubular crypts which appear to penetrate to a considerable distance into the intestinal wall, and possibly foreshadow the characteristic Lieberkühn's glands of Mammalia. Crypts may also be found in the stomach, where they receive the apertures of the gastric glands, as in Amiurus, but more usually they are restricted to the intestine. In the Dipnoi (e.g. Protopterus) the mucous membrane of the stomach, and—excluding the Bursa Entiana where a number of oblique folds are present—of the intestine also, is, on the contrary, perfectly smooth.
In addition to transverse and longitudinal folds the mucous membrane of the various sections of the alimentary canal is often developed into outgrowths which are more or less linear.[[242]] In the oesophagus these may be papilliform, as in Box and Caesio; obtuse in Acipenser, hard and almost spine-like in species of Rhombus; or in the form of pyramidal retroverted processes with jagged or fringed edges, as in the Spiny Dog-Fish (Acanthias vulgaris). In the Basking Shark (Selache) similar processes are present, which, near the stomach, become unusually long and branched, so that the entrance to that cavity is surrounded by a series of backwardly-directed arborescent tufts. Peculiar papillose or tag-like processes of the mucous membrane are frequently present on the spiral valve of Elasmobranchs, in the intestine of such Teleosts as Balistes, Mugil and some Pleuronectidae, and also in the rectum of Rhombus maximus.
Of all the outgrowths from the mucous membrane of the alimentary canal the so-called "spiral valve" of the Cyclostomata, Elasmobranchs, Holocephali, Chondrostei, Crossopterygii, Amiidae, Lepidosteidae and Dipnoi is the most characteristic. The first appearance of this structure was probably in the form of a straight longitudinal fold or ridge projecting into the cavity of the intestine, similar, perhaps, to the typhlosole of many Invertebrata. This primitive condition is not retained in any existing Fishes, although it may be closely approached in the larval Cyclostome (Ammocoetes), and is perhaps also indicated in the straight anterior portion of the spiral valve of Polypterus. Absent altogether in the Myxinoids, the valve is represented in its simplest condition, as in certain other Cyclostomata (e.g. Petromyzon), by a ridge of mucous membrane which commences anteriorly on the dorsal side, and, after describing a partial spiral as it passes backwards, terminates posteriorly on the ventral side, the width of the valve not exceeding half the diameter of the intestine. This simple type of valve is repeated in embryo Elasmobranchs, but in the adults of these Fishes the valve becomes much more complicated, and exhibits a wide range of structural variation. The increased complexity of the valve seems to depend on several factors, the effect of which, in different Elasmobranchs, is best studied in a series of valves of progressively higher differentiation.[[243]]