Chapter VII: , is termed the endoskeleton. The latter consists (i.) of an (3)

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 {262}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 {263}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.

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 {264}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 {265}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]

In a hypothetical simple type of valve, easily derivable from the more primitive type of _Petromyzon_, it may be conceived that, while not exceeding in width the semi-diameter of the intestine, the valve becomes disposed in several complete and more or less closely approximated spiral turns, the free edge of the valve being on the same level as its attached margin, and leaving an open axial canal along the centre of the gut. The nearest approach to this hypothetical type, which has been compared, not inaptly, to _un escalier tournant sans noyau_, is perhaps to be found in the Thresher-Shark (_Alopecias vulpes_).

The structure of the more complicated spiral valves of other Elasmobranchs are well illustrated within the limits of the single genus _Raia_.

In one specimen of _Raia_ sp. (Fig. 159, A) the last four coils of the valve are similar to those of the hypothetical type, but the more anterior ones, owing to the greater width of the valve, which here exceeds the semi-diameter of the intestine, have their free margins deflected downwards, while that portion of the valve which forms the first half turn is coiled inwards upon itself, so as to form a hollow cone, open dorsally, and having its apex directed forwards. In other examples a further modification is introduced by the increasing width of the valve, which now, throughout its whole length, equals the semi-diameter of the intestine; and by the formation of an axial columella by the thickened free edge of the valve, which is traversed by a central band of unstriped muscle, as well as by the intra-intestinal artery and vein, and takes the place of the central canal of the preceding types. The valve is, however, still regular, and its free margin remains on the same level as the corresponding portion of the attached edge. In other specimens, again, additional complications are introduced by a still further increase in the width of the valve, which now exceeds, often considerably, the semi-diameter of the intestine, and the consequent deflection of the free edge of the valve either forwards or backwards (C and D). As shown in C the valve, in consequence of the backward deflection of its free margin, presents the appearance of a nest of {266}imperfect truncated cones with their apices directed backwards, the successive cones adhering so closely to one another that they combine to form a central conical chamber with a spirally disposed cavity winding round it. In D, on the contrary, the free edge of the valve is deflected forwards, so that, as in C, a nest of cones is formed, but the apices of the successive cones are directed forwards instead of backwards. Notwithstanding these variations in the structure of the valve as a whole, the first coil or half coil nearly always resembles that described in A.

It is obvious that the structure of the valve varies considerably within the limits of the genus, and it may be added that various intermediate types of structure occur between A and B, {267}A and C, and A and D. The individual variations are perhaps even more remarkable, and appear to be quite independent of age and sex. By way of example it may be mentioned that valves approximating to one or other of those represented by C and D occur in different individuals of _Raia maculata_ of the same sex and similar in size, even in young specimens not more than three inches in length.

As regards other Elasmobranchs, the common Dog-Fish (_Scyllium canicula_)[244] has a well-developed spiral valve disposed in twelve coils, which structurally represents a more highly developed example of the type D. The existence of considerable individual variation is nevertheless indicated by the fact that in one specimen examined the valve was intermediate between C and D, five of the eight cones projecting forwards and three backwards. In a specimen of _Notidanus_ sp.[245] there were as many as twenty coils, which in disposition were intermediate between B and C, approximating, however, more nearly to B. In a specimen of the Port Jackson Shark (_Heterodontus_)[246] the valve had eight coils, and in structure was also intermediate between B and C, but approached more nearly to C. Some of the Hammer-headed Sharks (e.g. _Sphyrna malleus_)[247] possess a type of spiral valve which differs considerably from any of those hitherto described, and is termed a "scroll" valve (Fig. 159, E). The attached edge of the valve pursues a straight longitudinal course, or at any rate only describes a half turn and back again in passing from the pyloric to the cloacal extremity of the gut. In the middle of its course the width of the valve is about equal to two-thirds of its length, but towards either extremity it gradually diminishes until the free and attached margins meet. The valve thus constituted is rolled upon itself from left to right, the successive coils being comparable to a series of cylinders placed one inside the other, and becoming gradually larger both in length and diameter from within outwards. A similar valve is present in some of the Carchariidae.

In the Holocephali (e.g. _Chimaera monstrosa_)[248] the valve describes only three and a half coils, and is further remarkable in that the attached margin, for a considerable portion of its {268}extent, does not form a regular spiral but describes only a slightly sinuous course. Posteriorly, the valve is more normal, and consists of about two cones with their apices directed forwards.

In the Dipnoi the spiral valve is well developed, and in _Neoceratodus_[249] describes nine coils, and in _Protopterus_[250] six or seven. The structure of the valve in the latter Dipnoid resembles that of _Scyllium canicula_, except for the smaller number of cones.

In the more generalised Teleostomi the valve is best developed in the Sturgeon (_Acipenser_) and in _Polypterus_. In the former[251] the valve is restricted to the posterior half of the total length of the intestine, often extending to within an inch of the anal aperture, and describing in its backward course about seven or eight coils. The width of the valve is about equal to the semi-diameter of the intestine, and the thickened free margin forms a well-marked axial columella, round which the cavity of the gut winds, as in the type B, except that the spiral is a more open one. In _Polypterus_ the valve begins close to the solitary pyloric caecum, and for some distance pursues a straight longitudinal course, but eventually forms a few spiral coils, ceasing, however, at a considerable distance from the anus. The evidence afforded by petrified faeces or "coprolites" proves that certain extinct Crossopterygii (e.g. _Macropoma_, _Megalichthys_), like their living representative, _Polypterus_, possessed a spiral valve.[252] In _Amia_ and _Lepidosteus_[253] the valve is almost vestigial, being restricted to the terminal portion of the intestine, and is somewhat variable as to the precise number of its coils. In _Amia_ there are nearly four coils, extending over 3 cm., that is less than a tenth of the total length of the intestine, but in some specimens the coils do not exceed two and a half or three in number. _Lepidosteus_[254] has a still shorter valve which, in specimens of 7-10 cm. in length, may not consist of more than three and a half coils, and in much larger specimens may be reduced to less than two coils, a variation which suggests that a reduction takes place in the number of coils as the fish increases in age and size. The structure of the valve in the three last-mentioned genera resembles that described in _Acipenser_, and in none of them does {269}the width of the valve so far exceed the semi-diameter of the intestine as, by forward or backward deflection, to give rise to the highly characteristic cones of Elasmobranchs and Dipnoi.

In the more specialised Teleostomi (Teleostei) the spiral valve is wholly wanting, except perhaps as a vestigial structure in certain Clupeoids, as, for example, _Chirocentrus_,[255] and possibly also in some Salmonidae.[256]

From what has been said as to the structure of the spiral valve in the different groups of Fishes, it may be concluded that the valve most nearly retains its primitive condition in the Cyclostomata; attains its maximum development in the Elasmobranchs, especially in the Notidanidae, and shows no indication of degeneration in the Dipnoi. In the Holocephali and the lower Teleostomi, on the other hand, the valve exhibits various stages of retrogressive modification, and in the Teleosts is either absent altogether or persists only as a vestigial structure in a very few species.

From a physiological point of view the object of the spiral valve is to increase the absorptive inner surface of the intestine,[257] but, from what has been said as to the structural variability of the valve, it is obvious that its efficacy from a functional standpoint must be equally variable. The value of the valve as an absorptive mechanism necessarily depends on the area of absorption-surface which it provides, as well as on the degree of resistance which it offers to the passage of food material along the cavity of the intestine. These factors will in turn depend on the number of coils, on the width of the valve, and on the extent to which its free margin is deflected in forming the series of cones, but these again are precisely the structural features which are most liable to variation. The total absorption area in the four types of valve characteristic of the genus _Raia_ has been calculated, and may be expressed in square centimetres as follows:—A, 136.64; B, 143.82; C, 254.3; and D, 276.7.[258] Hence as regards mere absorption area a spiral valve of the type D has twice the extent of a valve of the type A, and if, in addition, account be taken of the retardation of the food due to the increased obstruction offered by the columella and cones in D, it is clear that the {270}difference in physiological value between the two types must be far more considerable than is indicated by a comparison of their relative superficial areas alone.

The evolution of the spiral valve was probably due to the necessity of increasing the absorptive area of an almost straight unconvoluted intestine, a result which in other animals is often obtained by an increase in the length and concurrent convolution of the intestine itself. Any attempt to correlate the variations in the degree of perfection or imperfection of the valve considered as an absorptive mechanism with any special variations in the nature or quality of the food is, however, a very difficult problem, and a satisfactory explanation has yet to be found. The difficulty, moreover, is increased by the fact that the majority of Fishes with a spiral valve are mainly carnivorous; the Elasmobranchs, in which this structure is at the same time most highly developed and most variable, exclusively so. On the other hand, the term "carnivorous" covers a multiplicity of minor differences in the nature and relative digestibility of different forms of animal food, and it is quite possible that it is with differences of this kind that the specific or individual variations in the development of the spiral valve are associated. The absence of the valve in the variously nourished Teleosts, save perhaps as a vestige in one or two, is also difficult to account for, although it is not improbable that compensating structural modifications exist in this group. As a rule, the intestine is much more convoluted in these Fishes, but to an extent which varies greatly in different species, while the characteristic pyloric caeca and the spiral valve appear to a certain extent to be developed in inverse proportion to one another.

THE GLANDS.

The glands associated with the alimentary canal in different Fishes are (1) the gastric glands, (2) the liver, (3) the pancreas, (4) the pyloric appendages, and (5) the "rectal" gland.

Oral salivary glands are wanting in all Fishes, the only secretory structures in the mouth being numerous mucus-secreting goblet cells, which here, as elsewhere throughout the alimentary canal, are intermixed with the ordinary epithelial cells.

THE GASTRIC GLANDS.—The Cyclostomata and Dipnoi do not possess any specially differentiated gastric glands, and it is {271}probable that in these Fishes the secretion of the digestive fluids is effected by the ordinary lining epithelium of the stomach or intestine, or both. In the remaining groups gastric glands are generally present in the form of simple caecal structures embedded in the submucosa and opening on the surface of the mucous membrane into the cavity of the stomach. The glands differ in different Fishes in the character of their lining epithelium and in the extent to which their component cells are differentiated from the epithelium of the stomach. There does not appear, however, to be any distinction into "central" (pepsin-forming) and "parietal" (acid-secreting) cells, as is the case in the higher Vertebrata. Towards the pyloric end of the stomach the true gastric glands are often replaced by mucous glands. There are, nevertheless, not a few Teleosts in which special gastric glands are absent, as, for example, _Syngnathus acus_, and several species of Cyprinidae, Labridae, and Blenniidae, etc. In at least two genera (_Gastrosteus_ and _Cobitis_), belonging to widely different families, gastric glands are present in certain species but absent in others. As suggested by Edinger,[259] the absence of these glands may possibly be due to degeneration.

It may be remarked that the formation of such digestive ferments as pepsin and trypsin, which are associated with the stomach and pancreas respectively, in the higher Vertebrates, is not nearly so strictly localised in Cyclostomes and Fishes. So far from peptic digestion being limited to the stomach, it may take place in the pharynx, stomach, and intestine of Ammocoetes, and in some Elasmobranchs (e.g. _Scyllium_), and in such Teleosts as the Pike, Eel, and Carp, the peptic region extends from the stomach for some distance along the intestine, while trypsin has been obtained from the mucous membrane of the stomach, intestine and pyloric caeca, as well as from the pancreas.[260]

Intestinal glands analogous to the glands of Lieberkühn in the higher Vertebrates seem to be entirely wanting in Fishes, unless represented by the sac-like or tubular crypts which are so generally present in the Teleostomi.

THE LIVER.—Phylogenetically the oldest gland in connexion with the Vertebrate alimentary canal, and in size by far the {272}largest, the liver arises as a caecal outgrowth from the embryonic mesenteron, and in this primitive stage recapitulates a condition which is retained throughout life in Amphioxus. By the subsequent division and branching of this outgrowth the massive compound tubular gland of the adult Fish is eventually formed.

The liver of Fishes (Figs. 153, 154) is very variable in size, shape, colour, and degree of lobulation. Anteriorly, it is usually moulded to the posterior face of the transverse septum between the pericardial and abdominal portions of the coelom, and from thence extends backwards in the abdominal cavity to a varying distance, in some Sharks as far as the cloaca. Externally, the gland is invested by the peritoneum, which extends on to it from the pericardial septum and forms a suspensory fold, and also from the oesophagus and stomach. The shape of the liver usually bears some relation to that of the body, being, for example, longest in the Eels and broadest in the Rays. In the great majority of Fishes the liver is bilobed, consisting of two sub-equal lateral lobes, disposed longitudinally and confluent anteriorly for a portion of their extent. From this normal type there are a few minor variations.[261] In _Petromyzon_, _Lepidosteus_ (Fig. 155, B), and a few Teleosts (_e.g._ the Gymnodontes, Lophobranchii, and some Salmonidae) the liver is unilobed. In the Myxinoids and in the Dipnoi (e.g. _Protopterus_), the organ is bilobed, but the small anterior lobe lies immediately in front of the much larger posterior lobe, with the gall-bladder between the two (Fig. 155, A). In some Teleosts (e.g. _Scomber_), the liver is trilobed. A gall-bladder is invariably present in either the larval or adult Cyclostomata, in the Chrondrostei, Holostei, Crossopterygii and Dipnoi, and generally also in Elasmobranchs and Teleosts. In the Elasmobranchs it is rarely entirely wanting, as in _Sphyrna_ and _Pristis_, and in the Teleosts in some of the Gurnards (_Trigla_). The gall-bladder and bile-duct of _Petromyzon fluviatilis_ atrophy after the metamorphosis which follows the larval _Ammocoetes_ stage, but in _Petromyzon marinus_ the duct, although usually absent, is sometimes retained. In the Ammocoetes the epithelium lining the gall-bladder is ciliated. In some Fishes, as, for example, in many Elasmobranchs, the gall-bladder is more or less completely embedded in the substance of the liver; in others, as in most Teleostomi, the organ is quite distinct from the gland (Fig. 154).

{273}A simple arrangement of the ducts from the liver and gall-bladder is that found in the common Dog-Fish (_Scyllium canicula_). In this Elasmobranch a cystic duct leaves the gall-bladder, and, after receiving several hepatic ducts from the lobes of the liver, becomes the bile-duct and opens into the commencement of the intestine. In the Myxinoids and in the Dipnoi (e.g. _Protopterus_), there are but two hepatic ducts, one from each lobe of the liver; these unite and then meet the cystic duct to form the bile-duct (Fig. 155, A). The number of hepatic ducts may, however, be considerably increased, as, for example, in the Siluroid _Amiurus_,[262] where 8-10 separate ducts join the cystic duct. In a few instances one of the hepatic ducts opens directly into the intestine, independently of that which unites with the cystic duct in forming the bile-duct. In the Dipnoi (e.g. _Protopterus_),[263] and in some Teleostomi (e.g. _Lepidosteus_),[264] the bile-duct receives the duct from the pancreas before opening into the intestine.

THE PANCREAS.—In the Cyclostomes (e.g. _Petromyzon_, _Bdellostoma_, _Myxine_) a rudimentary pancreas is apparently present, but the evidence as to its identity is not wholly conclusive. A well-developed pancreas occurs in Elasmobranchs, in at least one of the Dipnoi, and probably in most Teleostomi.[265]

In Elasmobranchs the pancreas is a compact structure, uni- or bi-lobed, and entirely distinct from the liver. In _Scyllium canicula_ (Fig. 153), the bilobed gland lies in the angle between the distal limb of the stomach and the adjacent portion of the intestine, and from the smaller of its two lobes the duct issues to pass to its intestinal aperture near the commencement of the spiral valve. In most of the Teleostomi in which its existence has hitherto been recorded, the pancreas is a singularly diffuse gland; and usually a considerable portion, or even the whole of it, is embedded in the substance of the liver, its lobules accompanying the ramifications of the hepatic artery and duct, and the portal vein. The pancreatic duct usually opens into the intestine near the aperture of the bile duct (e.g. _Amiurus_); sometimes the two ducts open on the apex of a common papilla (e.g. _Acipenser_ and _Amia_), or by their union form a common {274}duct (e.g. _Lepidosteus_). Among the Dipnoi a well-developed pancreas is present in _Protopterus_,[266] embedded in the wall of the stomach and intestine, internal to the peritoneal investment of these organs, and extending even into the first fold of the spiral valve. The gland is traversed by fine ductules which unite together and open into the bile-duct just before the latter enters the intestine. In the remaining Dipnoi the existence of a pancreas has yet to be ascertained. Developmentally, the pancreas resembles the liver, and, histologically, is very similar to that of the higher Vertebrates, consisting of terminal glandular alveoli continuous with intermediary tubular portions, and eventually with the finer ductules, which, by their union, form the main efferent duct.

THE PYLORIC CAECA.—These structures are caecal outgrowths from the intestine, and are situated close to the pyloric extremity of the stomach and the intestinal apertures of the bile and pancreatic ducts. Wholly wanting in the Cyclostomata and Dipnoi, and, unless represented by a pair of caeca opening into the long, tubular, non-valvate anterior portion of the intestine in the Greenland Shark (_Laemargus borealis_),[267] in the Elasmobranchs also, they are very generally present in the Teleostomi, although extremely variable both in number and arrangement in different families. In _Amia_ there is no trace of pyloric caeca. _Polypterus_ has a single short caecum with a thick muscular wall. In _Acipenser_, _Polyodon_, and _Lepidosteus_, on the contrary, pyloric caeca are unusually well developed. In _Acipenser_ the caeca are not only numerous, but are so connected together by connective tissue and blood-vessels, and so invested externally by the peritoneum, as to form a large, compact, gland-like mass, communicating with the intestine by a single wide duct. In _Polyodon_ the organ is essentially similar, but is lobed externally. In _Lepidosteus_ (Fig. 155, B, _py.c_), the caeca are also very numerous, but relatively short, and, although united into a compact mass, open by four pit-like orifices into the intestinal cavity. In Teleosts the caeca are subject to extraordinary variations in number, size, and arrangement.[268] In some families, and even in groups of higher taxonomic value, they are entirely absent, as is the case with the {275}Siluridae, Esocidae, Cyprinodontidae, Labridae, Plectognathi, and Lophobranchii. The "Sand-eel" (_Ammodytes_) has but a single caecum; the Turbot (_Rhombus maximus_) two, and other Pleuronectidae three to five; and the Perch (_Perca_), three (Fig. 160, _py.c_).

In other Teleosts, on the contrary, these structures are much more numerous. In _Labrus labrax_ there are about 60, in the Whiting (_Gadus merlangus_) 120, while in the Mackerel (_Scomber scombrus_) there are no fewer than 191. If few in number the caeca open separately into the intestine, but when numerous, more or fewer of them may unite to form a smaller number of efferent ducts, as in the Whiting, where four such ducts are formed. In some instances, as in the Tunny (_Thunnus_), the union of the caeca by connective tissue leads to the formation of a compact mass. As regards their arrangement, the caeca may either be disposed in a whorl round the intestine, as in the Whiting, or in a linear series, as in the Salmon (_Salmo_) and in some of the Clupeidae.

The mucous membrane lining the anterior pyloric caeca is often developed into a network of ridges, limiting crypt-like or tubular depressions; and not infrequently the epithelium is ciliated.

The precise function of these organs, whether digestive or absorptive, is still uncertain.[269] That they may be digestive is suggested by the presence of certain amylolytic and proteolytic enzymes, but this obvious conclusion is to some extent vitiated by the close proximity of these organs to the stomach, and more especially to the intestinal orifice of the pancreatic duct. It is by no means improbable, however, that the caeca are both digestive and absorptive organs. An attempt has been made to show that the pyloric caeca and the spiral valve vary inversely as regards the extent of their development in different groups of {276}Fishes.[270] To some extent the reciprocal variation of these structures supports this view, but it is also evident that there are obvious objections to its unqualified acceptance. Thus, in some Teleostomi (e.g. _Acipenser_, _Polyodon_), exceptionally well-developed and numerous caeca and a spiral valve are both present. _Amia_ with an almost vestigial spiral valve has no trace of pyloric caeca, and in Teleosts the absence of a spiral valve is associated with the complete suppression of the caeca in many large and important groups.

THE RECTAL GLAND.—The "rectal" gland, or appendix digitiformis, is a small organ of unknown function with complex glandular walls, and a central duct opening dorsally into the terminal portion of the intestine.[271] The organ is generally present in Elasmobranchs (Fig. 153, _rct.gl_), in which group the intestinal orifice of its duct may either be close to the termination of the spiral valve, or, as in _Chlamydoselachus_,[272] near the cloacal outlet of the gut. An apparent representative of the gland, the "caecum cloacae," is also present in the Dipnoi,[273] but communicates directly with the cloaca (Fig. 155, A, _cl.c_). The "rectal" gland is perhaps homologous with the intestinal caecum which is to be found in some Teleosts (e.g. _Box vulgaris_), and possibly also with the "caecum" (caecum coli), and its vermiform appendix in the higher Vertebrata.[274] The caecum cloacae, on the contrary, is morphologically a urogenital sinus, formed as a dilatation of the fused hinder portions of the mesonephric ducts, and probably comparable with the sperm sacs of male Elasmobranchs, and also with the urinary bladder of Teleostomes.[275]

{277}CHAPTER X

THE RESPIRATORY ORGANS

The principal respiratory organs consist of a series of pairs of branchial clefts in the form of perforations in the side walls of the throat, which place the pharynx in free communication with the exterior. The first and most anterior of these clefts, the mandibulo-hyoid cleft or "spiracle," is situated between the mandibular and hyoid arches; the second, the hyo-branchial or hyoidean cleft, between the hyoid arch and the first branchial arch; and the remaining clefts between the succeeding branchial arches. On the anterior and posterior walls of more or fewer of the clefts highly vascular plate-like, or variously shaped filamentous outgrowths of their lining membrane are developed, which subserve the purpose of exposing the blood to the influence of the oxygen-containing water, and are termed branchial lamellae or "gills." In addition to their usual respiratory organs, the gills, a few Fishes utilise the air-bladder either as a functional lung or as an oxygen reservoir, and in others accessory breathing organs of various kinds are developed.

The arrangement of the branchial clefts and the gills may be conveniently studied first in the Elasmobranchs. Excluding the spiracles, there are usually in this group (Fig. 161, A), five pairs of branchial clefts, but in certain primitive members of the group the number may be larger. Thus, in _Notidanus griseus_ (_Hexanchus_) and in _Chlamydoselachus_ there are six, and in _Notidanus cinereus_ (_Heptanchus_), seven clefts. The pharyngeal apertures of the clefts are relatively wide, but their external openings, which are freely exposed on the lateral surface of the head between the eye and the pectoral fin, are usually narrow and slit-like.

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The successive clefts are separated from one another by a series of inter-branchial septa, each of which consists of the lining membrane of two contiguous clefts and a median fibrous sheet; it is further strengthened on its pharyngeal margin by a branchial arch, and more externally by the fringe of cartilaginous rods (branchial rays) with which the outer convex edge of each arch is provided. The anterior and posterior walls of each septum are produced into a number of outwardly-radiating vascular plates or folds (branchial lamellae or "gills"), which by their free edges project into the cavity of the cleft (Fig. 161, A). Although slightly free at their outer extremities, the lamellae do not extend so far as the external margin of the septum to which they are attached (Fig. 164, B). Each series of lamellae is termed a "hemibranch," and, from what has been said, it is obvious that each inter-branchial septum and its supporting branchial arch carry two hemibranchs, an anterior and a posterior, the two forming a complete biserial gill or "holobranch." The hyoid arch, however, has only a single hemibranch, viz. that pertaining to the anterior wall of the hyo-branchial cleft, and as the fifth or last cleft has a hemibranch only on its anterior wall, the fifth arch is {279}gill-less.[276] The spiracle is a vestigial cleft. At an early stage of embryonic growth it differs but little from its fellows, but subsequently degenerating it is represented in the adult by a tubular passage between the oral cavity and the exterior, which, however, is often complicated by the development of caecal outgrowths.[277] The anterior wall of the spiracle often retains a rudiment of a hemibranch in the shape of more or fewer vascular lamellae, which, as they are supplied with arterial blood, and not with venous blood like the ordinary gills, are said to form a mandibular or spiracular "pseudobranch." The spiracle varies greatly in size in different families, being largest in the Trygons and Torpedos, and very small, or even absent in the Lamnidae. Its pseudobranch is best developed in the Notidanidae, where it has the essential structure of a true hemibranch, and, as in other Elasmobranchs, but to a greater extent, probably aids in the additional aeration of the blood which is distributed to the eye and brain. The characteristic opercular covering of the external apertures of the gill-clefts in the Teleostomi and Dipnoi is wanting in Elasmobranchs. It is interesting to note, however, that in _Chlamydoselachus_[278] curious frilled cutaneous folds are developed as extensions of the outer edges of the inter-branchial septa, as well as of the hyoid region, and, like a series of incipient opercula, project backwards over the successive branchial clefts (Fig. 252).

While in many respects more primitive than in Elasmobranchs the branchial system of the Cyclostomata presents certain special and peculiar features. The branchial clefts assume the form of oval, antero-posteriorly flattened pouches or sacs, varying, however, in number, and in their mode of communicating with the exterior, in different genera. In the Lamprey (_Petromyzon_) there are seven pairs of obliquely-disposed gill-sacs opening externally by small rounded orifices, and by similar apertures, not directly into the pharynx, but into a branchial canal (Fig. 162, _r.t_), which underlies the oesophagus, and, while ending blindly behind the last pair of sacs, communicating in {280}front with the oral cavity.[279] The first of the series of gill-sacs corresponds to the hyo-branchial or hyoidean cleft of Elasmobranchs and other Fishes. Spiracles are absent in the adult, but in the embryo are represented by pouch-like outgrowths of the hypoblast of the oral cavity, which subsequently undergo singular changes.[280] Thus, the outgrowths become converted into the lateral halves of a complete ciliated circum-oral groove, which is retained even in the Ammocoetes stage, and recalls the ciliated peripharyngeal ring of Ascidians. Another archaic feature is also to be noted in the continuity of the groove with a ciliated mid-dorsal pharyngeal ridge, which has been compared to the "dorsal lamina" of Ascidians, and to the equally characteristic hyperbranchial groove of _Amphioxus_.[281] Ventrally also, the lateral halves of the groove unite to form a single groove, which, after receiving the median aperture of the thyroid rudiment,[282] is continued backwards in the mid-ventral line of the pharyngeal wall as far as the last branchial arch. No trace of these ciliated structures is, however, to be met with in the adult.

The branchial lamellae are represented by a series of vascular horizontal and parallel ridges radiating outwards along the roof, floor, and lateral walls of each gill-sac, and invested by an {281}epithelium which is partially ciliated. The inter-branchial septa are much thicker than in Elasmobranchs, and include not only the walls of adjacent sacs and the branchial muscles, but also contain cavernous peribranchial lymph-sinuses. The cartilaginous branchial skeleton is situated wholly external to the gill-sacs, the so-called branchial arches lying between the external apertures of the sacs, and directly beneath the superficial skin, or, in other words, on the outer margins of the inter-branchial septa, and not on the inner, as is invariably the case with the branchial arches of Fishes.

In the Hag-Fish (_Myxine_) (Fig. 163), there are usually six, very rarely seven, pairs of gill-sacs, all of which open directly into the pharynx, and not into a branchial canal as in the Lampreys. On the other hand, _Myxine_ is unique in having the outer extremities of its gill-sacs produced into a corresponding number of tubular canals which, after a longer or shorter course obliquely backwards and outwards, unite to form on each side a ventrally-situated external aperture (Fig. 163). In the same genus a short canal, or oesophageo-cutaneous duct, passes from the pharynx {282}behind the last gill-sac of the left side, and opens externally with the common external branchial aperture of that side.

In _Bdellostoma_ there are usually six or seven pairs of gill-sacs, but some species have ten or even fourteen pairs.[283] They agree with those of the Lamprey in having independent external apertures, but resemble the corresponding organs in _Myxine_ in opening directly into the pharynx. An oesophageo-cutaneous duct is also present.[284]

In the Holocephali there are but four branchial clefts, the fifth cleft being closed. Spiracles are absent in the adult, although present in the young of _Chimaera_. The branchial lamellae resemble those of Elasmobranchs, but the inter-branchial septa are somewhat shorter, so that the lamellae project slightly beyond their outer margins (Fig. 164, B). A hyoidean hemibranch is present. A noteworthy feature is the development of a cutaneous fold from the outer surface of the hyoid arch, which grows backwards over the gill-clefts, and, uniting above and below with the body-wall, terminates in a free posterior margin, just behind the last gill-cleft. By the growth of this opercular fold the gills become enclosed in a spacious branchial cavity, and the clefts communicate with the exterior through a slit-like opening between the free margin of the fold and the body-wall.

The reduction in the extent of the inter-branchial septa which is initiated in the Holocephali is carried to a still further extent in the Teleostomi. Commencing with the Chondrostei, and passing thence to the more specialised Teleostei, the septa become gradually reduced in length, and the branchial lamellae project freely beyond their outer margins to an increasing extent.

This modification, least marked in _Acipenser_ (Fig. 164, C) and _Polyodon_, attains its maximum in the Teleosts (Fig. 164, D and E), where the branchial lamellae take the form of a double series of free filaments disposed along the convex outer margin of each branchial arch, and attached by their bases only to the reduced and inconspicuous septa. As a general rule each of the first four arches supports two hemibranchs,[285] forming a {283}biserial gill or holobranch. In shape the branchial filaments are usually somewhat triangular, and consist of an axial supporting cartilage or bone, invested superficially by a highly vascular mucous membrane. As in most of the preceding groups the fifth branchial arch is gill-less. All Teleostomi possess a well-developed movable operculum, supported by a more or less complete series of opercular bones, with or without the addition of branchiostegal rays (Fig. 161, B). The size of the external branchial aperture varies considerably. Usually the hinder and lower margins of the operculum are free, and then the aperture is spacious. Not infrequently, however, the more or less extensive fusion of the ventral and hinder edges of the operculum with the body-wall reduces the aperture to a narrow slit, as in the Eels and some Siluridae, or to a small upwardly directed pore, as in the "Sea-Horse" (_Hippocampus_). In the Symbranchidae the branchial apertures close dorsally, but fuse ventrally, leaving a single median orifice on the under side of the throat.

Open spiracles are wanting in most adult Teleostomi, but are, nevertheless, retained in the Crossopterygii (_Polypterus_), and in the Chondrostei (_Acipenser_ and _Polyodon_). They have been observed, however, in the embryos of some Teleosts, as in the Salmon (_Salmo_),[286] and even in the adults of _Amia_,[287] _Lepidosteus_, {284}and a few Teleosts[288] are represented by pouch-like recesses of the oral cavity. A few vestigial branchial lamellae may be developed on the anterior wall of each spiracle in _Acipenser_ and _Polyodon_, but are wanting in _Polypterus_, and, as in Elasmobranchs, represent a mandibular or spiracular pseudobranch.

The structure usually regarded as a hyoidean hemibranch in the Teleostomi differs greatly in its development in different members of the group. In _Acipenser_ it is undoubtedly the hemibranch of the hyoid arch and is a true gill, receiving venous blood from the ventral aorta and returning arterial blood to the dorsal aorta, as in Elasmobranchs. In _Polyodon_ and in _Polypterus_ the hemibranch is suppressed. _Lepidosteus_,[289] on the other hand, has two series of lamellae on the inner surface of the operculum, a dorsal and a ventral series meeting at an angle (Fig. 197). The ventral lamellae are supplied with venous blood, the dorsal with arterial,[290] so that while the former retain their primitive character as a functional hyoidean hemibranch, the latter is a pseudobranch. It is interesting to note, however, that the development of this pseudobranch and its blood-vessels proves that it does not represent any portion of a true hyoidean hemibranch, but is really a spiracular pseudobranch.[291] In most other Teleostomi a degenerate hemibranch occupies a similar position. In _Amia_[292] it is very feebly developed, and is lodged in a canal communicating with the branchial cavity by a small aperture, and situated directly anterior to the dorsal end of the first branchial arch. Its blood supply is arterial, and the organ is therefore a pseudobranch. In Teleosts the hemibranch is invariably a pseudobranch; nevertheless, its primitive condition as a gill is indicated either by its structure or by its embryonic history. In some genera the pseudobranch consists of short free lamellae, as in some Pleuronectidae; or it is partly free and partly concealed, as in some of the Horse Mackerels (_Caranx_) and in _Salmo_; or it may be completely hidden beneath the oral epithelium, as in the Cod (_Gadus_), where the organ is very degenerate, and is little more than a "rete mirabile" of blood-vessels. The nature of the Teleostean pseudobranch is not in {285}all cases quite clear. In _Salmo_ it is said that there is no hyoidean hemibranch, and that the pseudobranch is really a persistent spiracular pseudobranch;[293] hence it is probable that a like significance must be attached to this singular structure in other Teleosts. The evidence of the cranial nerves on this point is conflicting. If the pseudobranch pertains to the spiracular cleft its nerve supply should be derived from the nerve of that cleft—viz. the seventh or facial nerve; but if it represents a hyoidean hemibranch, then one would expect it to be innervated by the ninth or glossopharyngeal nerve. As a matter of fact, however, the organ is said to be supplied by the seventh in some Teleosts, and in others by the ninth nerve.

In the Dipnoi the branchial system is best developed in _Neoceratodus_, the increasing importance of the lungs as respiratory organs in _Protopterus_ and _Lepidosiren_ being associated with a corresponding reduction in the structural and functional development of the gills. There is no trace of spiracles in the adult.

In _Neoceratodus_[294] there are five branchial clefts, including the hyobranchial. Each of the first four branchial arches carries a pair of hemibranchs, and, as in the Holocephali, the gill-lamellae are attached along nearly their whole length to a well-developed interbranchial septum (Fig. 165). A peculiarity of _Neoceratodus_, which has no counterpart in any other Fishes, is the extension of the branchial lamellae on to the dorsal and ventral walls of the branchial clefts, so that the hemibranchs on opposite sides of each cleft are continuous both dorsally and ventrally (Fig. 166). The fifth arch is gill-less. {286}In addition to the normal gills there is also a hyoidean pseudobranch. As in other Dipnoi, an operculum forms the outer wall of the branchial cavity, and leaves but a narrow, slit-like external branchial aperture.

In _Protopterus_[295] the number of branchial arches is increased to six, but, in consequence of the closure of the hyobranchial cleft, there are but five open clefts. The first, second, and third arches are wholly devoid of branchial filaments: the fourth and fifth support each a biserial gill, while the sixth arch retains only an anterior hemibranch, which, however, as the source of its blood supply seems to indicate, may consist of "emigrant" gill-filaments from the posterior hemibranch of the fifth arch.[296] Interbranchial septa are practically non-existent, the flattened, leaf-like gill-lamellae being free except at their attached bases, and thus repeating a characteristic Teleostean feature. A "hyoidean" hemibranch or pseudobranch, supplied from the ventral aorta, is present, but as the hyobranchial cleft is closed it projects into the branchial cavity immediately in front of the cleft between the first and second branchial arches. In _Lepidosiren_[297] the branchial arches are reduced to five and the clefts to four, the hyobranchial and fifth clefts being closed. There is a "hyoidean" hemibranch resembling that of _Protopterus_.

The facts furnished by the study of the numerical and structural variations in the gill-clefts, gills, and gill-arches of different groups of Fishes prove that atrophy of these structures takes place at opposite ends of the series. We have examples of this anteriorly in the suppression of the hyo-mandibular cleft and its hemibranch, and of the hyoidean hemibranch, as the result of {287}the conversion of the mandibular and hyoid arches into jaws, or into skeletal supports for the jaws; and posteriorly, in the reduction which is evident when the generality of Fishes are compared with such primitive Elasmobranchs as _Chlamydoselachus_ and _Notidanus_.

In most Fishes the concave pharyngeal margins of the branchial arches are fringed with a double series of either cartilaginous or bony tubercles or filaments, the "gill-rakers" (Figs. 161 and 164). The anterior row of gill-rakers on each arch usually interdigitate with those of the posterior row on the preceding arch, and in this way the two rows form a sieve-like mechanism to prevent any solid particles, which may enter the pharynx with the respiratory current of water, from passing into the gill clefts and clogging or otherwise injuring the branchial filaments.

In a few Fishes the gill-rakers are enormously developed, and subserve a function similar to that of the baleen plates of the Whalebone Whales in acting as a filter for straining from the water the small pelagic organisms on which the Fish feeds. This is notably the case in the great Basking Shark (_Selache maxima_)[298] in which the closely-set, flattened, tapering gill-rakers may be so long as four or five inches, and, while somewhat resembling "whalebone" in appearance, have the histological structure of vascular dentine. The nature of the food, which in the stomach of one specimen examined consisted solely of an immense quantity of plankton, including Copepods and the larvae of other Crustaceans,[299] affords clear evidence of the great value of such a filtering mechanism to this Shark, and, at the same time offers an explanation of the striking and significant reduction in the size of the teeth, which, relatively to the dimensions of the Fish, are so small as to be almost vestigial. A similar filter has been observed in an extinct _Selache_ (_S. aurata_)[300] from the Antwerp Crag, and also in an existing South African Shark (_Rhinodon typicus_);[301] and in the latter, as in the Basking Shark, is associated with a marked reduction in the importance of the dentition. The long slender gill-rakers of the Chondrostean {288}_Polyodon_ also constitute an efficient filter, and the same may be said of several plankton-eating Teleosts.

THE MECHANISM OF RESPIRATION.—The aeration of the blood is effected by the rhythmical suction of water into the oral cavity, and its subsequent expulsion through the gill-clefts, bathing the highly vascular gill-lamellae in its course. In any single act of inspiration the mouth is opened, and the oral cavity enlarged by the lateral expansion of its walls. When the oral cavity is filled with water, the mouth is closed and the expiratory process begins. By the lateral contraction of the oral walls the water is driven outwards through the gill-clefts, and over the gill-lamellae. During this process the branchial arches become widely separated by the contraction of their muscles, the operculum is elevated, and the oesophagus is closed by the contraction of its muscular wall. In many Fishes the course of the expiratory water-current is controlled by special valve-like folds of the oral mucous membrane, the maxillary and mandibular "breathing-valves."[302]

The rate of "breathing" varies considerably in different Fishes, even in allied species.[303] In the Blue Wrasse (_Labrus_), and the Rockling (_Motella_), the number of respirations per minute is 15, in the Minnow (_Leuciscus_), and Stickleback (_Gastrosteus_), as many as 150. A deficiency of oxygen in the water accelerates the respiratory movements, and the Fish appears to "pant" or breathe hurriedly. In the Lampreys, both inspiration and expiration may take place through the external gill-apertures by the alternate expansion and contraction of the gill-sacs, more especially when the suctorial buccal funnel is used for the attachment of the animal. On the other hand, the singular habits of the Myxinoids involve a further modification of the respiratory process. In these Cyclostomata the inspiratory current enters the external naso-pituitary aperture and reaches the pharynx through the naso-pituitary canal, and thence, as an expiratory stream, traverses the gill-sacs on its way outwards. The pharynx is closed behind the last pair of gill-sacs by a constrictor muscle, which prevents the entrance of the water into the oesophagus, and converts the pharynx into a respiratory tube for the time {289}being; but, when food is being swallowed, the pharyngeal constrictor is relaxed and the internal apertures of the gill-sacs are closed by the contraction of their own sphincter muscles.

In addition to the usual respiratory organs it is probable that in not a few Fishes the superficial skin may share with the gills the function of breathing. In this connexion may be mentioned the fact that in _Periophthalmus_ the tail is used for respiration. Hickson[304] observed that a species of this genus, frequenting the extensive sandy shores of the Island of Celebes, often rests with its tail in the water, the head and trunk being exposed. Under such circumstances the gills are probably of little use, and the tail is utilised as a breathing organ, principally, as Haddon[305] subsequently pointed out, through the agency of its extremely vascular caudal fin.

Some Fishes possess larval breathing organs; others, even when provided with gills, either utilise the air-bladder, or develop special accessory organs, for aquatic or, more usually, for aerial respiration.

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