Chapter VI: Introduction: General Characters—anatomy of Amphioxus—embryology and (1)

LIFE-HISTORY—CLASSIFICATION OF CEPHALOCHORDATA—SPECIES AND DISTRIBUTION

The CEPHALOCHORDATA comprise only a small group of little fish-like forms, the Lancelets, usually known as "Amphioxus," and referable to about a dozen species arranged in several closely allied genera under the single family Branchiostomatidae. The best known form is _Branchiostoma lanceolatum_ (Pallas), the common Amphioxus or Lancelet, which has been found in British seas, and even as far north as the coast of Norway, but is much more common in warmer waters, such as the Mediterranean, and is also found in the Indian Ocean. It is abundant in the Bay of Naples, and lives and breeds in great numbers in a salt lagoon, the "Pantano," near Messina, and from these localities most of the specimens have been obtained for the numerous recent researches upon its structure and development.

Amphioxus was first discovered and described (1778) by Pallas, who regarded it as a Mollusc, and named it _Limax lanceolatus_. It was first correctly diagnosed as a low Vertebrate, and named _Branchiostoma_, by Costa, in 1834. The term _Amphioxus_, under which it has become so well known, was applied to it a couple of years later by Yarrell.

The anatomy was for the first time fully investigated by Johannes Müller in 1841, and this important memoir has been supplemented in regard to special systems and histological details by numerous papers by many leading zoologists, such as those by Huxley in 1874, Langerhans in 1876, Lankester in {113}1875 and in 1889, Retzius in 1890, and Boveri and Hatschek, both in 1892. Important papers on special points have also been written by Rolph, Rohde, Benham, Andrews, Goodrich, and others. The development was first elucidated by Kowalevsky in 1867, at about the same time when he studied the development of the Ascidians, and later again in 1877. Further papers on the development and metamorphosis we owe to Hatschek in 1881, Lankester and Willey in 1890 and 1891, Wilson in 1893, and quite recently to MacBride. Dr. Willey's book, _Amphioxus and the Ancestry of the Vertebrata_ (1894), contains a summary of investigations on structure and development, an interesting discussion of the relations of Amphioxus to the other Chordata, and a full bibliography.

In addition to such original researches, Amphioxus is studied in more or less detail every year by countless senior and junior students in zoological laboratories and marine stations throughout the civilised world. The value of this primitive form as an object of biological education depends upon the fact that it shows the essential Vertebrate characters, and their mode of formation, in a very simple and instructive condition. Although no doubt somewhat modified, and possibly degenerate in some details of structure, in its general morphology it presents us with a persistent type probably not far removed from the ancestral line of early Chordata. There are no sufficient grounds for the view that Amphioxus is a very degenerate representative of fish-like Vertebrata.

GENERAL CHARACTERS.—The Cephalochordata (or Acrania, in contradistinction to the Craniata or Vertebrata) are marine, non-colonial Chordata, in which the notochord extends the entire length of the body, running forward into the snout beyond the nervous system. There is no skull, and the notochord is not surrounded by any vertebral column. There are no limbs nor paired fins. There is no exoskeleton, and the ectoderm is a single layer of non-ciliated columnar cells. The mouth is ventral and anterior, the anus is ventral, posterior, and asymmetrically placed on the left side. The pharynx is a large branchial sac, having its sides perforated by many gill-slits, and is surrounded by an ectodermal enclosure, the atrium, which opens to the exterior by a median ventral atriopore. The stomach gives off a simple saccular pouch, the liver, which has {114}connected with it a simple hepatic portal blood system. There is a respiratory circulation, the contractile ventral vessel which represents the heart sending the colourless blood forward to the respiratory pharynx to be purified. The body-wall is segmented into over fifty myotomes. There are numerous separate nephridia which develop from the mesoderm and open into the atrium. The brain remains undeveloped, being scarcely distinct from the spinal cord. There are two pairs of cerebral nerves, and many spinal, in which the dorsal and ventral roots or nerves do not unite. The sense-organs are simple; there are no paired eyes and no auditory organs. The sexes are separate; the gonads are metamerically arranged on the body-wall, and have no ducts: they burst into the atrium. In the development the segmentation is complete, a gastrula is formed by invagination, the nervous system is formed from the dorsal epiblast, the notochord from the hypoblast, and the mesoderm arises from metameric coelomic pouches. The body-cavity is an enterocoele. The gill-slits are at first perforations of the body-wall opening from the pharynx to the exterior, which later become enclosed by the development of the atrium.

ANATOMY.

EXTERNAL CHARACTERS.—Amphioxus[112] is about 1½ to 2½ inches in length, slender, somewhat translucent, and pointed at both ends (Fig. 69). It lives in shallow water and burrows in the sand, head first, with great rapidity. It frequently remains with the anterior end protruding from the sand. When on the surface it lies on one side. It is said to swim freely at night. The head end is rather the thicker, and the anterior two-thirds of the ventral surface are flattened (Fig. 70, A), and may be slightly ridged longitudinally. The lateral edges of this flat area project as metapleural folds (Fig. 70, _mt.pl_), which begin anteriorly at the edges of the external mouth, and die away in the middle line posteriorly behind a median opening, the atriopore (Fig. 70, _atrp_). From this point a ventral median fin (_vent.f_) extends backwards around the pointed posterior end {115}(caudal fin, _cd.f_), and then forwards along the upper surface (dorsal fin, _dors.f_) to the anterior end of the body. These fins thus constitute a continuous median fold around a great part of the animal (Fig. 70, B, and Fig. 71).

The surface is soft all over, there being no exoskeleton. The epidermis or ectoderm is formed by a single layer of {116}epithelial cells (see Fig. 72, p. 118), some of which bear sensory processes, while others have a striated cuticular border. There is no general ciliation of the surface in the adult.

The true mouth is a small pore at the bottom of a large vestibule (the stomodaeum), placed at the anterior end of the ventral surface (Figs. 70 and 71), and formed by the "oral hood," which may be a prolongation forwards of the atrial or metapleural folds at each side. The edges of the oral hood bear 12 to 20 pairs of cirri (Fig. 70, _cir_) or ciliated tentacles (strengthened by skeletal rods), which form a sensory fringe around the opening. The anus (Figs. 70 and 71, _an_), is asymmetrical, being {117}placed on the left side of the ventral fin, some distance behind the atriopore, and not far from the posterior end of the body. The short region behind the anus and surrounded by the caudal fin may properly be called "tail." The current of water for respiratory and nutritive purposes, and which may carry the ova and spermatozoa to the exterior, usually passes in at the mouth and out at the atriopore, as in the Tunicata. On occasions, however, it is said to be reversed.

GENERAL STRUCTURE.—The general plan of organisation of the body (see Fig. 71) is that a longitudinal skeletal axis, the notochord (_nch_), separates a dorsal nervous system (_sp.cd_) from a ventral reduced coelom (_coel_), in which lie the alimentary canal (_int_), the gonads (_gon_), and other organs. Thus a transverse section of the body (see Fig. 72) shows the typical Chordate arrangement of parts, and is comparable with a transverse section of a tadpole, a young fish, or a larval Ascidian. A peribranchial (_atr_) or atrial cavity (which is morphologically a part of the external world shut in) lies external to the coelom and body-wall around the pharynx and the greater part of the alimentary canal, and opens to the exterior by the atriopore. As in the Tunicata, the perforations (gill-slits) in the wall of the pharynx (_br.cl_) open into the atrial cavity and so indirectly to the exterior.

MUSCULATURE.—The thick body-wall is largely formed by muscular tissue metamerically segmented into about 60 myotomes (Fig. 71, _myom_). These muscle-masses, which (as is usual in Vertebrata) are thickest dorsally at the sides of the notochord and spinal chord (Fig. 72, _m_), are so arranged as to present the appearance in a lateral view of the body of a series of shallow cones (<<) fitting into one another and with their apices directed forwards. The muscle fibres are striated, and run longitudinally along the body from the anterior to the posterior edge of each myotome, so as to be attached at their ends to the two septa of connective tissue which form the boundaries of the myotomes. These septa, the myocommas, are conspicuous features in the external appearance of the body (Fig. 70, B). They are not arranged so as to be opposite one another on the two sides, but the myotomes on the right and left sides alternate, as can be seen in a transverse section (Fig. 74, A, p. 121).

{118}

It is by means of these lateral muscle-bundles that the rapid vibration or alternate bending of the body from side to side in swimming or burrowing can be performed. There are usually, on each side, 35 myotomes in front of the atriopore, 14 between the atriopore and the anus, and 11 postanal, making 60 in all: some species have only about 50 myotomes, and some as many as 85. (See {119}Classification, p. 137, where a list of the species with the number of myotomes in each is given.)

There are also transverse muscles (Fig. 72, _mt_) extending across the ventral surface in the region of the body enclosed by the metapleural folds, and serving to compress the atrial cavity, and so aid in the expulsion of its contents.

Outside the muscular layer of the body-wall the thin integument is formed of a dermal layer of soft connective tissue, covered by the epidermis, a single layer of columnar cells, many of which, especially on the oral cirri, have sensory bristles.

SKELETON.—The endoskeleton consists of the notochord and some tracts of modified connective tissue which support various parts of the body.

The notochord of this animal is noteworthy amongst Chordata for extending practically the entire length of the body, including the head, from snout to tip of tail (Fig. 71). It lies in the median plane, but nearer the dorsal than the ventral surface (Fig. 72), and has the myotomes at its sides, the nervous system above and the alimentary canal below. It is elliptical in section, and tapers to the two ends. The nuclei of the original notochordal cells are displaced to the dorsal and ventral edges, and the greater parts of the cells, in the adult, are occupied by large vacuoles filled with a fluid secretion, so as to form by their distended condition a stiff elastic structure. This state of the cells, and the appearance it gives rise to (Fig. 73), seen best in young specimens, is very characteristic of notochordal tissue. Around the notochord lies a sheath of connective tissue which is continuous with the similar sheath around the nervous system and with the septa between the myotomes.

In addition to these skeletal layers of connective tissue there is a cartilage-like tract in the oral hood. This is jointed, or made up of separate rod-like pieces, one at the base of each cirrus, into which it sends a prolongation (Fig. 71, _sk_). The dorsal and ventral fins are supported by single and double rows {120}respectively of what have been called "fin-rays." They are short rods of gelatinous connective tissue, each enclosed in a lymph space. Finally, the bars constituting the walls of the pharynx between the gill-slits contain slender skeletal rods which run obliquely dorso-ventrally, and are of a stiff, gelatinous nature (see Fig. 75, p. 122). This skeletal connective tissue consists in all cases of a fibrous deposit or matrix produced by the layer of epithelium (ectodermal, endodermal, or mesodermal) which adjoins the tissue.

ALIMENTARY CANAL.—This has, as its most noteworthy feature, the Chordate characteristic that the pharynx gives rise to the respiratory organ (see Figs. 71 and 74, A); and in size and prominence, both in side view and in sections, the modified pharynx of Amphioxus is fairly comparable with the branchial sac (pharynx) of many Tunicata (see Fig. 23, p. 51), and might be called by the same name.

The small primitive mouth, at the bottom of the cavity bounded by the oral hood (stomodaeum), has a membranous border, the velum (Fig. 71, _vl_), the edges of which are prolonged into a circle of 10 or 12 (up to 16 in some species) simple oral tentacles turned inwards towards the pharynx (compare tentacles of Ascidians, p. 45).

The pharynx, by far the largest part of the alimentary canal, and extending nearly half-way along the body, is more important as a respiratory than as a nutritive organ. Its walls over nearly the whole extent are perforated by a large, and indefinite, number (100 or more on each side) of gill-slits which run on the whole dorso-ventrally, but in the contracted condition seen in preserved specimens have their lower ends directed obliquely backwards, so that a vertical transverse section may cut through a number of such slits and the intervening branchial bars (Fig. 74, A, _kb_). These bars, and therefore the slits between them, are of two orders, primary and secondary, the latter being developed later in larval life as downgrowths or "tongue-bars," one from the top of each primary gill-slit, so as to divide it into two secondaries. The primary and the secondary (or tongue-) bars can be distinguished from one another by their structure in the adult animal (Fig. 75, A and B).

{121}

It must be remembered that these branchial bars, or septa between the gill-slits, are not merely portions of the wall of the pharynx, but are in a sense portions of the body-wall as well, and correspond in nature, though not in number, to the visceral arches in a Vertebrate lying between the visceral clefts which open on the exterior. In the adult Amphioxus the clefts in the wall of the pharynx do not open directly to the exterior, but into the peribranchial cavity or atrium, which, however, is only formed at a late larval period as an invagination or enclosure of ectoderm. Previous to that the first formed gill-slits opened to the exterior in Amphioxus (see larva, Fig. 86, p. 134), just as they do in a fish or a young tadpole. The atrial cavity is therefore, from its origin, lined by ectoderm, and the outer surface of a branchial bar is virtually a part of the outer surface of the body. It is only natural then to find that each bar contains a small section of the coelom in its interior, communicating dorsally and ventrally with other parts of that cavity (see Figs. 75 and 76). There are also blood-vessels which run in the branchial bars and their junctions. The greater part of the epithelium covering a branchial bar is pharyngeal epithelium or endoderm {122}(Fig. 75, _br.ep_), but the external, wider, non-ciliated cells (Fig. 75, _at.ep_) are ectodermal cells lining the atrium. The gelatinous skeletal rods in the primary bars are forked ventrally, while those in the secondary bars are simple; and there are other points of detail in which the two kinds of bar differ. These bars are obviously more numerous in the adult than the myotomes, but in the young larva the first formed gill-clefts are metamerically arranged, and then later they increase greatly in number. It is the cilia covering the pharyngeal epithelium on the branchial bars, possibly aided by the ciliated tracts of the oral hood, which cause the current of water already alluded to.

Transverse branchial junctions (synapticula) run across the branchial bars, connecting them at frequent intervals, and these transverse connexions, like the branchial bars, are supported by skeletal rods. Along the ventral median line of the pharynx runs a groove, the endostyle or hypopharyngeal groove, comparable with the similar structure in the branchial sac of Tunicata. This longitudinal groove (Fig. 76, _gl_) is lined by ciliated epithelium containing four tracts of gland cells (compare endostyle in Ascidians, Fig. 20, p. 46). There is reason to believe that this organ is the homologue of the thyroid gland of Vertebrata. As in the case of Tunicata the endostyle secretes mucus, which is carried forwards by the cilia to constitute a train with entangled food particles which pass back dorsally to the stomach. At the anterior end the ciliated lips of the endostyle diverge to {123}the right and left to encircle the front of the pharynx as the peripharyngeal bands. These unite again dorsally to form the epipharyngeal (or hyperpharyngeal) groove which leads backwards, corresponding to the hypopharyngeal groove below (see Fig. 74, A), till the posterior end of the pharynx is reached.

The remainder of the simple alimentary canal is straight, and is scarcely differentiated into regions. A slight narrowing of the tube behind the pharynx has been called the oesophagus, and a slight enlargement which follows, the stomach. From this point the intestine tapers backwards to the anus (Fig. 71, p. 116). The ventral edge of the stomach gives off a blind pouch, the hepatic caecum or saccular liver, which runs forwards on the right-hand side of the pharynx (Fig. 74, A, _l_). This is a digestive gland, is lined with glandular epithelium, and apparently corresponds with the liver of Vertebrata. There are no other digestive glands in connexion with the alimentary canal of Amphioxus.

COELOM.—In the young larva there are at first (as in Balanoglossus) five coelomic spaces, a median anterior "head-cavity," a pair of antero-lateral "collar-cavities," and a pair of more posterior long lateral grooves from which arise, in the later larva, the segmented myotomes and ventrally a large coelomic space surrounding the alimentary canal and separating it from the body-wall. In the adult animal, however, the coelom has been so much displaced by the formation of the spacious atrium that in front of the atriopore it can only be recognised as a series of canals and crevices. The relations of coelom to atrium in the region of the intestine are {124}seen in Fig. 74, B, and in the region of the pharynx in Fig. 74, A. Fig. 72 shows the distribution of the spaces more in detail (see also Fig. 71). Beginning anteriorly, along the dorsal surface of the pharynx and beneath the notochord run a pair of dorsal coelomic canals, one at each side of the epipharyngeal groove; these give off ventral diverticula which pass down the primary branchial bars of the pharyngeal wall and unite ventrally in a median tube, the endostylar coelom (see Fig. 72, _ec_). At the posterior end of the pharynx these dorsal and ventral canals unite in a narrow coelomic space encircling the stomach, inside the wall of the atrium, and sending an extension forwards around the liver (Fig. 74, A, _l_). In the region of the intestine, behind the atriopore, the coelom is allowed to expand to its primitive condition on the left-hand side (Fig. 74, B), but is still reduced on the right side, where there is a prolongation of the atrial cavity reaching nearly to the anus. All these coelomic spaces are lined by a coelomic epithelium.

The BLOOD SYSTEM of Amphioxus, although as simple as that of a Chaetopod worm, is undoubtedly laid down on the Vertebrate plan—even though there is no distinct heart and the vessels are few and of simple structure. Capillary networks are formed in some places, but the colourless blood also extends into many lacunae or lymph spaces, such as those around the fin-rays and in the metapleura. As in a typical lower Vertebrate, there is a contractile ventral vessel (the ventral or branchial aorta, Fig. 77, _v.ao_) running forwards under the alimentary canal to the pharynx, and giving off on each side afferent branchial vessels, which pass up the primary branchial bars and give off branches joining the vessels in the secondary bars. These latter do not communicate directly with the ventral aorta, but the vessels in all the branchial bars open dorsally by efferent branchial vessels into the paired dorsal aortae (Fig. 77, _d.ao_), which run backwards along the top of the pharynx, one at each side of the epipharyngeal groove. In the vessels of the branchial bars and their connectives the blood is aerated by the current of water passing through the gill-slits, and so reaches the dorsal aortae in a purified condition. The right-hand dorsal aorta is continued forward further into the snout than its fellow of the other side, and is dilated at its extremity (Fig. 77). At the posterior end of the pharynx the paired dorsal aortae unite to form the median dorsal aorta {125}which runs backwards, lying between notochord and alimentary canal. This vessel gives off branches to the wall of the intestine, and these break up into capillary networks (Fig. 77, _cp_), from which the blood is collected by the median sub-intestinal vein. This then flows forwards to pass by the hepatic portal vein to the ventral edge of the saccular liver, in the wall of which it is distributed in a capillary network. The blood is collected on the dorsal edge of the liver by the hepatic vein, which runs posteriorly and then turns downwards and forwards to become continuous with the posterior end of the ventral aorta or "heart."

It is clear that this course of the circulation agrees with that of a typical lower Vertebrate in all essential points:—(1) in having the main artery a dorsal aorta in which the blood flows backwards; (2) in having a ventral vessel representing the heart, and sending impure blood forwards to the respiratory region of the alimentary canal to be aerated; and (3) in having a hepatic portal system consisting of the capillaries of the liver, through which the blood from the intestinal wall has to pass before reaching the ventral vessel (heart).

RENAL EXCRETORY functions have been attributed to various organs in Amphioxus, and it is quite possible that, in addition to the true nephridia which are now known, other tracts of tissue in the body may be able to eliminate nitrogenous waste matters. Such are certain clumps of columnar epithelial cells on the floor of the atrium, and the single pair of large brown atrio-coelomic funnels lying on the dorsal edge of the posterior end of the {126}pharynx (Fig. 71, _br.f_). There are, however, a large number (about 100 pairs) of minute nephridia, discovered (1890) by Weiss and by Boveri independently, lying at the sides of the dorsal coelomic canals above the pharynx, which must be regarded as the chief functional renal organs. These are bent tubules, partly glandular and partly ciliated, each giving off several caecal knobs (at first supposed to be open nephrostomes, one shown at each end of the tubule and three along its upper surface in Fig. 78), which project into the coelom, and opening by one nephridiopore (on the lower surface, and opposite a tongue bar of the pharynx) into the atrial cavity. The knobs, or closed nephrostomes, are surrounded by peculiar, slender, club-shaped tubular and flagellated cells—which Goodrich[113] has shown to correspond to the "solenocytes" in the nephridia of Polychaete worms (see Fig. 79).

{127}The CENTRAL NERVOUS SYSTEM is dorsal and tubular as in Vertebrates, and lies in a connective-tissue sheath immediately above the notochord (Figs. 71, etc., and 80, A). Posteriorly it tapers to a fine point a little in front of the end of the notochord, but anteriorly it ends abruptly some distance behind the anterior extremity of the notochord. The central canal is connected with the dorsal surface by a median longitudinal cleft (Fig. 80, C), and at the anterior end it dilates to form the cerebral vesicle (_c.v_) with which two simple sense-organs, an eye-spot (_e_) and an olfactory pit (_olf_), are connected. A patch of ciliated epithelium in the floor of the vesicle has been described as an "infundibular-organ." There is also a surface dilatation of the dorsal cleft behind the cerebral vesicle (_dil_). The nervous system as far back as this point may be regarded as the brain, though scarcely distinguishable externally (Figs. 71 and 80, A) from the spinal chord behind. From this "brain" arise two pairs of "cranial" nerves, the first (I.) from the anterior end, and the second (II.) from the dorsal surface of the cerebral vesicle; both are in front of the first myotomes of the body, and supply the pre-oral snout with nerves.

The spinal cord gives off a large number of spinal nerves segmentally arranged, but, like the myotomes, not opposite and symmetrical on the two sides, but placed alternately (Fig. 81). Moreover, the spinal nerves arise on each side at two levels, there being a more dorsal series each arising by a single root and {128}supplying the integument as well as the transverse muscles, so as to be sensory as well as motor, and a ventral series arising each by a number of roots (Fig. 81) and wholly motor in function, as they supply only the myotomes. These two series may be compared to the dorsal and ventral roots which in the Vertebrata join to form a mixed spinal nerve.

In addition to ordinary small nerve cells the central nervous system contains certain large nerve cells with very long processes, the "giant fibres," which extend through the greater part of the length of the spinal cord. No trace of a sympathetic nervous system has been found.

The SENSE-ORGANS connected with the nervous system are few and simple. There are sensory cells in the ectoderm, on the margin of the velum, on the velar tentacles, and especially in clumps on papillae of the cirri around the mouth, which are probably tactile. In the roof of the oral hood there is a sensory structure, the "groove of Hatschek," which is supposed to be an organ of taste. The olfactory pit alluded to above opens externally on the left-hand side of the snout. It is ciliated internally and leads to the so-called olfactory lobe, an {129}antero-dorsal hollow outgrowth from the brain. In the young animal the olfactory pit opens by the neuropore into the central canal (Fig. 80, A), but that passage is closed in the adult. Possibly the olfactory pit is homologous with the hypophysis or pituitary body of Vertebrates, the homologue of which in Tunicata has a ciliated funnel. Finally, the median cerebral eye (Figs. 80 and 81) is a mere pigment spot in the anterior wall of the cerebral vesicle, and a series of somewhat similar pigment spots occurs along the floor of the central canal in the spinal cord.[114] There is no known auditory organ. On the under surface of the oral hood patches of ciliated epithelium drawn out into rounded lobes were called by Johannes Müller the "Räder-organ." This is probably of use in drawing water inwards to the pharynx, but it may also be a sense-organ.

The GONADS are segmentally arranged along the sides of the body, projecting into the atrial cavity at the sides of the pharynx and intestine. In some species the gonads are paired, but in others belonging to the genus _Asymmetron_ (p. 137) only a single series, that of the right side, is present. In the common Amphioxus (_Branchiostoma lanceolatum_) there are about 26 pairs (Fig. 70, B), lying in somites 25 to 51; and ovaries and testes are found in separate individuals in all other respects. Each gonad is surrounded by a layer of coelomic epithelium. The gonad must therefore be regarded as having grown down from a myotome of the body-wall into a coelomic pouch, carrying before it the coelomic and then the atrial epithelium (Figs. 72, and 74, A, _g_). Eventually the gonads, when ripe, burst through the layers of epithelium, and the ova and sperms are shed into the atrium and escape to the exterior by the atriopore, or it may be in some cases by the mouth.

{130}EMBRYOLOGY AND LIFE-HISTORY.

Development takes place in the sea-water where the egg is fertilised—apparently always about sunset, the embryonic stages being passed through during the night, and the larva hatched in the early morning.

The egg is small (0.105 mm. in diameter when shed) and contains very little food-yolk. Segmentation is complete (Fig. 82, A), is nearly regular, and results in the formation of a hollow blastosphere (Fig. 82, E, F), the wall of which is one cell thick. The lower cells (Fig. 82, B, C, D) are slightly larger than the upper. Invagination of the lower cells then takes place (Fig. 83, A), resulting in the suppression of the blastocoele or segmentation cavity and the formation of an archenteron, at first shallow and opening widely to the exterior (Fig. 83, B), and then deeper and with the opening narrowed to a small posterior blastopore (Fig. 83, C). This "gastrula" stage differs from the blastosphere in having a mouth or blastopore, and in being two cell-layers thick—epiblast (ectoderm) on the outside and hypoblast (endoderm) within. It soon shows the future aspects of the body by its {131}elongation and shape (Fig. 83, C), as the dorsal surface becomes flat and the ventral convex, while the blastopore is at the posterior end of the dorsal surface. The blastopore soon closes, and the mouth and anus are formed independently later.

The epiblast cells become ciliated all over the surface, so that the embryo rotates within the thin covering which still surrounds it. And now all the chief systems of the body begin to be marked out. The tubular nervous system develops from a depression of the epiblast (the medullary plate) in the middle line of the flattened dorsal surface (Fig. 84, A, _mp_). The edges of the depressed area grow inwards and unite over the deeper layer of epiblast, which becomes the wall of the neural canal or embryonic nervous system (Fig. 84, D, _n_); and further back these edges of the medullary plate join one another behind the blastopore, so that the latter comes to open into the floor of the neural canal, thus forming the neurenteric canal (Fig. 85, A, _cn_). Anteriorly the neural canal (_n_) opens to the exterior for some time by the neuropore.

The hypoblastic walls of the archenteron give off a long median dorsal groove which becomes the notochord (Fig. 84, C and D, _ch_); and also an anterior pouch and certain lateral pairs {132}of diverticula which are the enterocoeles or coelomic pouches, and give rise to the mesoblastic somites (Fig. 84, B and C, _mk_). The notochord (Fig. 84, D, _ch_) is at first a longitudinal cellular ridge, which becomes segmented off from the hypoblast as a rod lying below the neural canal. It is seen in various stages of development in Figs. 84 and 86, leading to the vacuolated condition of the adult.

The coelomic pouches are five in number—(1) one median, anterior, which gives rise to the two head cavities, the left-hand one of which opens to the exterior by means of the pre-oral pit; (2) a pair of small lateral pouches, placed anteriorly and dorsally, which do not divide but give rise to the first pair of myotomes only and their outgrowths which extend back into the metapleural folds, where, however, they are later replaced by lymph spaces; and {133}(3) a second pair of diverticula, more posteriorly placed, which continue to grow back towards the blastopore, and have paired mesoblastic somites, the cavities in which are the beginnings of the coelom in the body, constricted off from them successively from before backwards (Fig. 85, A, _ush_) to form all the remaining myotomes.[115] This is the first sign of segmentation in the animal, and at this stage, when it has about five pairs of mesoblastic somites, it breaks out of its covering and becomes a free-swimming larva.

The mouth now appears, and soon grows to a large opening on the left side of the now pointed anterior end (Fig. 86, A, _m_), and the first gill-slit (_ks_) forms as a direct communication from the front of the mesenteron (pharynx) to the exterior. It is ventral at first, and then shifts over to the right side.

The anus forms posteriorly, and the neurenteric canal closes {134}up. A depression on the floor of the enteron close to the mouth gives rise to the "club-shaped gland" (Fig. 86, B, _k_), which is probably a gill-cleft in its nature.

The walls of the coelomic pouches, which have been extending both dorsally and ventrally (Fig. 84, D), become the {135}mesoderm, the outer the somatic and the inner the splanchnic layer; and the ventral parts of their cavities unite to form the coelom. The cells of the dorsal parts become muscle fibres, and constitute the myotomes internally and the connective tissue of the skin externally.

The larva (Fig. 87) is now long and narrow with many segments, pointed ends, and a caudal fin. The gill-slits all appear first in the mid-ventral line and then shift over to the right side (Fig. 87, 1-4): they are metamerically arranged. After fourteen have been so formed a series of eight appear dorsally to those on the right side, and then the first set, originally ventral, move over to the left side, and by the suppression of some they become equal in number and segmentally arranged on the two sides of the body. This is perhaps the stage at which Amphioxus shows the nearest approach to the typical embryo of a higher Vertebrate. The gill-slits are here seven to nine on each side, and the Vertebrate embryo has usually five to seven on each side. These first gill-slits in Amphioxus are later subdivided by the downgrowth of the tongue-bar from the dorsal edge.

The atrium is an ingrowth of the external space between the two ventral metapleural or atrial folds (Figs. 88 and 89), paired lateral ridges of the body-wall, and so is lined by ectoderm. This ingrowth is shut off from the exterior by the {136}growth towards each other of sub-atrial ridges on the inner sides of the metapleural folds (see Fig. 89, A, _sl_), and then becomes greatly enlarged by the increased relative growth of the ventro-lateral part of the body-wall (Fig. 89, B, C). The posterior opening between the metapleural folds remains as the atriopore (Fig. 88, C, _ap_); while the anterior end (Fig. 88) also remains open for some time, but eventually closes. As the metapleural folds lie outside the gill-slits (Fig. 88, A) when these folds close in (B and C), it comes about that the gill-slits which formerly opened freely to the exterior now open into the cavity of the atrium (compare Figs. 87 and 88).

The mouth now becomes median and ventral, and is reduced in size, the oral hood (stomodaeum) is formed in front of it, the gill-slits become more numerous and vertically elongated, the endostyle forms along the floor of the pharynx, and the gonads grow as paired pouches from the body-wall. This brings the animal to the young adult condition, reached at a period of probably about three months after the fertilisation of the egg.

The development as a whole shows a very marked resemblance {137}to that of the Tunicata (see p. 55), but lends no support to the view that Amphioxus has degenerated from a higher group of the Vertebrata.

CLASSIFICATION OF THE CEPHALOCHORDATA.

The known species of Amphioxus may be classified as follows[116]:—

FAMILY BRANCHIOSTOMATIDAE.

Genus 1. _Branchiostoma_ (Costa, 1834).

Having biserial gonads and symmetrical metapleura.

_B. lanceolatum_ (Pallas)—Myotomes 36 + 14 + 12, gonads 23-29 pairs:
Mediterranean, N.W. Europe, Ceylon, E. of United States.

[_B. belcheri_, Gray—Myotomes 38 + 17 + 9: Torres Straits, Singapore,
Borneo, Ceylon.

[_B. nakagawae_, Jord. and S.—Myotomes 37 + 16 + 11: Japan.

[_B. caribbaeum_, Sundevall—Myotomes 37 + 14 + 9: West Indies, Atlantic,
N. and S. America.

_B. capense_, Gilchrist—Myotomes 47 + 19 + 9: S. Africa.

_B. californiense_, J. G. Cooper—Myotomes 45 + 17 + 9: California.

_B_. (_Dolichorhynchus_) _indicum_ (Willey)—Myotomes 42 + 14 + 15: India
and Ceylon.

(?) _B. elongatum_, Sundevall—Myotomes 49 + 18 + 12: Peru.

(?) _B. pelagicum_, Günther—Myotomes 36 + 16 + 15: Honolulu, Gulf of
Manaar, South Indian Ocean.

Genus 2. _Asymmetron_ (Andrews, 1893).

With uniserial (right) gonads and asymmetrical metapleura.

_A. lucayanum_, Andrews—Myotomes 44 + 9 + 13: Bahamas, Maldives,
Zanzibar.

_A. caudatum_ (Willey)—Myotomes 40 + 9 + 11: Louisiade Archipelago.

_A_. (_Heteropleuron_) _bassanum_ (Günther)—Myotomes 45 + 16 + 14: Bass
Straits, Australia.

" _cingalense_ (Kirkaldy)—Myotomes 39 + 16 + 8: Ceylon.

" _cultellum_ (Peters)—Myotomes 32 + 10 + 10: Torres
Straits, Australia, Ceylon.

" _maldivense_ (F. Cooper)—Myotomes 45 + 16 + 12: Maldive
Archipelago, Zanzibar.

" _hectori_ (Benham)—Myotomes 53 + 19 + 12: New Zealand.

{138}Thus sixteen species have been described, of which the three under _Branchiostoma_ placed after square brackets, seem to be merely varieties of _B. lanceolatum_, and _B. nakagawae_ is probably identical with _B. belcheri_; while it is a question whether _Asymmetron caudatum_ is more than a variety of _A. lucayanum_, thus leaving eleven or twelve species that seem fairly well characterised. The exact positions of the two marked (?), viz. _B. elongatum_ and _B. pelagicum_, cannot be determined in the absence of fuller descriptions of these species.

The list above, and the map (Fig. 90), give some indication of the geographical distribution of the group, and show that, although the few species are widely distributed over the shallow waters of the globe, most of the records lie between 40° N. and 40° S. latitudes. In fact the group is mainly a tropical one, and is most abundant in the Indo-Pacific region. The crosses indicate records of species of _Branchiostoma_, and the circles those of _Asymmetron_ (including _Heteropleuron_); the latter are confined to the Indo-Pacific seas, with the exception of _A. lucayanum_ from the Bahamas—one of the numerous cases of interesting similarity between the marine faunas of the East and West Indies.

FISHES (EXCLUSIVE OF THE SYSTEMATIC ACCOUNT OF TELEOSTEI)

BY

T. W. BRIDGE, Sc.D., F.R.S.

Trinity College, Cambridge; Mason Professor of Zoology and Comparative Anatomy in the University of Birmingham

{141}CHAPTER V

THE SYSTEMATIC POSITION AND CLASSIFICATION OF FISHES

In the first chapter of this volume it was pointed out that the Craniata, of which the Fishes form a subordinate group, is the last of the four principal divisions into which the Chordata are divided. The animals included in the first three, viz. the Hemichordata, the Urochordata, and the Cephalochordata, have already been dealt with in the earlier chapters, and it now remains for us briefly to consider the diagnostic characters of the Craniata, and then, more in detail, the organisation of the Fishes.

The Craniata, often termed Vertebrata, form one of the best defined and most easily recognisable divisions of the animal kingdom. As the name implies, they are distinguished from the more primitive Chordata by the formation of a definite "head," as the result of the modification of the anterior portion of the central nervous system to form a complex brain, round which are concentrated the chief organs of special sense. This is combined with the evolution of a skull, which, in addition to providing a "cranium" for the enclosure and protection of the brain, and partial or complete capsules for the sense-organs, is connected behind with a system of bony or cartilaginous visceral arches, which loop round the pharynx between the gill-clefts. Besides supporting the breathing organs (gills) in the lower aquatic Craniata, or existing as embryonic vestiges in the higher lung-breathing forms, these arches usually form the basis of jaws for the mouth. The epidermal portion of the superficial skin is always composed of several layers of cells. The notochord, which is always present in the embryo, and in a few Craniates, both living and extinct, may even be retained in its entirety in the adult, fails to reach {142}the anterior end of the brain. In most Craniates, however, the notochord becomes more or less completely replaced in the adult by the development round it of a series of vertebrae, forming the backbone or vertebral column. Two pairs of limbs, and cartilaginous or bony limb-girdles for their support, are very generally present.

The segmentation, or serial repetition of certain organs of the body, which is so marked a feature in the Cephalochordata, is also characteristic of the Craniata. Examples of this may be seen in the division of the lateral longitudinal muscles of the body wall into muscle-segments or myotomes by a series of transverse fibrous septa; in the formation of the vertebral column by a series of successive joints or vertebrae; in a similar serial repetition of the cranial and spinal nerves, the gill-clefts and branchial arches, certain blood-vessels, and the renal tubules. There is sometimes, however, no precise regional or numerical correspondence between the different organs which are successively repeated in this way, and hence it is probable that, in at least some of the organs of the Craniate body, the segmentation has been independently evolved in each case.

The pharynx is relatively much shorter than in other Chordata. The gill-clefts are few in number, whether, as in the lower Craniata, they are retained as the functional breathing organs, or are present, as vestiges only, in the embryos of the higher members of the group. In no instance are they subdivided by the growth of "tongue-bars" or "synapticula," nor do they open externally into an atrial or peribranchial cavity. The liver is a massive compound tubular gland, never, in the adult at all events, a simple caecal sac; and usually there is a pancreas and a spleen.

A spacious epithelium-lined body cavity or coelom, which, as regards its origin, may be regarded as a "syncoelom,"[117] surrounds the alimentary canal and separates it from the body wall. From the epithelial walls of the coelom are derived the gonads (ovaries and testes), which in the adult are limited to a single pair; while paired and often segmentally-arranged lateral tubular outgrowths from it (renal tubuli) acquire a glandular character and form the basis of the excretory or kidney system. A special portion {143}of the coelom also surrounds the heart and forms a pericardial cavity, and in some Craniata the genital ducts may be formed from its lining membrane.

There is always a muscular heart, consisting of at least three chambers, a sinus venosus, an auricle and a ventricle, and formed by a modification of the initial portion of the ventral or cardiac aorta of the Cephalochordata. The disposition of the great blood-vessels is based on a common plan in all Craniata, and the blood which circulates in them is red in colour owing to the presence of red, haemoglobin-containing corpuscles in addition to the colourless leucocytes which alone are present in the Cephalochordata. Ductless blood-glands of various kinds (spleen, thyroid, thymus, inter- and ad-renal bodies) are very generally present, and modify in different ways the character of the blood as it circulates through them. Besides blood-vessels there is also a somewhat similar system of lymphatic vessels distributed throughout the organs and tissues of the body, which serves the purpose of re-collecting the fluid portion of the blood that has diffused from the blood-vessels for the nutrition of the tissues, and conveying it back to the blood vascular system. These lymphatics contain lymph, a fluid comparable to dilute blood plasma, in which leucocytes float. In addition to their continuity with the blood-vessels at certain points, the lymphatic vessels may also communicate with the coelom, and hence the Craniata must be included among those somewhat rare exceptions to the general rule that no connexion exists between the series of blood-containing channels and the coelom.

In the excretory system the renal tubuli in the adult Craniata rarely retain their primitive embryonic communication with the coelom, and in no instance have they separate and independent external apertures; on the contrary, by the union of their outer or distal extremities, common efferent ducts are formed, which either open into a "cloaca," or directly on to the exterior of the body near the anus.

In all Craniates the dorsally-placed and tubular central nervous system has its anterior portion enlarged and otherwise modified to form a "brain," while the remaining portion, retaining a simpler and more uniform structure, forms the spinal cord. In the embryo the brain always consists of three successive sac-like enlargements known as the fore-, mid-, and hind-brain, and from {144}these are developed the various parts of the complex adult brain, which in the disposition and mutual relations of its parts conforms to a common plan in all the members of the group. There are at least ten pairs of cranial nerves having their origin from the brain, and, in addition, a varying number of spinal nerves arising from the spinal cord, and as a rule formed in each case by the union of a mainly sensory, ganglionated, dorsal root with a mainly motor, non-ganglionated, ventral root.

The median and usually vestigial, parietal, or pineal eye may sometimes be retained as a functional organ, but there exist in all Craniates, in addition, paired eyes, the sensory portion of which, the retina, is derived as an outgrowth from the first of the primary embryonic brain-vesicles. To these organs of special sense are added a pair of auditory organs, and a pair of olfactory organs, besides, in the lower aquatic Craniates, the peculiar sensory organs of the "lateral line."

The gonads are reduced to a single pair in the adult, although it is possible that they may have a multiple origin in the embryo. Gonoducts for the discharge of the sex-cells are almost invariably present, and may owe their origin either to a change of function on the part of certain kidney-ducts, or to independent evolution from the lining membrane of the coelom. The ova are generally provided with a large amount of nutritive reserve in the shape of food-yolk, and hence the process of segmentation is frequently partial or "meroblastic," but in some groups, in which the ova have less food-yolk, it is complete or "holoblastic." The typical invaginate gastrula stage, which is so striking a feature in the embryonic history of the lower Chordata, occurs also in a few of the lower Craniates, but in most of them it is apt to become masked or modified in various ways by the presence of a superabundant amount of food-yolk.

Functional hermaphroditism is of very rare occurrence in Craniates, and, as in the Cephalochordata, reproduction by budding and the formation of colonies are unknown.

Thus distinguished from other Chordata, the Craniata are divided into six "classes," which may be variously grouped, as the following table shows:—

{ } {145}
{ I. CYCLOSTOMATA. } AGNATHOSTOMATA.
{ Lampreys and } Without biting
{ Hag-Fishes. } jaws.
ICHTHYOPSIDA. {
Breathing by gills at some { }
period of life. { }
{ II. PISCES. }
{ True Fishes. }
ANAMNIOTA { }
No embryonic covering { }
or amnion. { }
{ III. AMPHIBIA. }
{ Newts, Frogs, and }
{ Toads. }
ANALLANTOIDEA. { }
No embryonic respiratory { }
organ or allantois. { } GNATHOSTOMATA.
{ } With biting
} jaws.
{ IV. REPTILIA. }
{ Lizards, Snakes, }
{ Turtles, and }
{ Crocodiles. }
{ SAUROPSIDA. { }
AMNIOTA. { { }
Amnion present. { { V. AVES. }
{ { Birds. }
{ }
ALLANTOIDEA. { }
Allantois present.{ VI. MAMMALIA. }
{ Hairy Quadrupeds. }

Apart from the distinctive characters of the six "classes" into which the Craniata are divided, two or three of these classes may possess important structural features in common by which they are distinguished from others. Thus, Cyclostomata, Fishes and Amphibia agree with one another, and differ from all the remaining groups in breathing by gills and in possessing lateral line sensory organs during part, or the whole, of life. Their embryos have no investing amnion, neither does the sac-like outgrowth from the hind-gut, which is known as the allantois, if present at all, ever extend beyond the coelom to form an embryonic investment or to act as a primitive breathing organ. Hence, therefore, the terms Ichthyopsida, Anamniota, and Anallantoidea have been applied to these three classes. Similarly, the term Sauropsida, as applied to Reptiles and Birds, is a convenient means of giving expression to the fact that, underlying the most striking diversity of outward form and habits, there is a community of inward structure which justifies the conclusion that these animals are more closely related to one another than either group is to any other class of Craniates. And again, the application of the terms Agnathostomata and Gnathostomata brings into sharp relief the fundamental distinction between the Cyclostomata and all the remaining groups of Craniata which is {146}only partially illustrated by the presence or absence of biting jaws.

In a general and popular sense the Cyclostomata are usually regarded as "Fishes," but this usage rests on no better foundation than a certain agreement between the Cyclostomata and the true Fishes in outward form and habits, and in their method of respiration by gills. On the other hand, it has been maintained that the distinctive features of the Cyclostomata are of sufficient importance not merely to separate them from the true Fishes, but possibly even (as is to some extent expressed by the use of the terms Agnathostomata and Gnathostomata) to warrant their elevation to a group equal in taxonomic value to all the remaining living Craniata taken collectively. The organisms included in the Cyclostomata, the Lampreys, and especially the Hag-Fishes, exhibit in many respects an extremely low grade of Craniate structure; but how far the simplicity or archaic nature of some of their organs is primitive, or has been acquired through degeneration, it is difficult, and is sometimes impossible, to determine with any degree of satisfaction. In other respects, such as the presence of a rasping "tongue," it is obvious that the Cyclostomata have attained a high degree of specialisation. As one of several illustrations which might be given of difficulties of this kind, it may be mentioned that it is by no means certain that the Cyclostomata are not the degenerate descendants of primitive but now extinct Gnathostomata. At all events the presence of paired cartilages in the skull of the Lamprey, which, with some show of reason, may be regarded as representatives of the primitive upper and lower jaws of the latter group, would seem to suggest this conclusion. If this be correct, we must regard the formation of a suctorial buccal funnel, with its complex system of supporting cartilages—one of the most striking features in the structure of this animal—as a secondary and adaptive specialisation of a mouth originally provided with biting jaws. But in spite of such difficulties there can be no question that the Cyclostomata are the most primitive of all existing Craniates, and so far differ from the true Fishes and from all other classes of Craniate animals, that their inclusion in a class by themselves is the least that can be done to give graphic expression to their isolated position, even if we do not fully accept the dictum of {147}Haeckel that "they are further removed from Fishes than Fishes from Man."

Briefly stated, the Cyclostomata or Agnathostomata are distinguished from "Fishes" and all the remaining Craniata (Gnathostomata) by the following characters:—

The mouth is either nearly terminal, as in the Hag-Fishes (_Myxine_); or, as in the Lampreys (_Petromyzon_), it opens out of a spacious, pre-oral, suctorial, buccal funnel, which, in its relations to the hypophysis or pituitary body, recalls the pre-oral buccal cavity of the Cephalochordata. As in Amphioxus, the hypophysis[118] is displaced dorsally by the forward growth of the pre-oral portion of the head in the embryo, and consequently it only attains its normal relations to the infundibular downgrowth[119] from the ventral surface of the fore-brain by perforating the floor of the skull from above instead of from below as in all other Craniates. In one section of the group (e.g. _Myxine_) the hypophysis opens into the oral cavity, and serves as a tubular passage for the inspiratory water-current to the gill-sacs, a feature in which these Cyclostomes are unique. The apparently median olfactory organ is carried inwards with the hypophysial involution, and communicates with the latter throughout life. A primitive upper jaw (palato-quadrate cartilages or sub-ocular arches) is present, and in at least some Cyclostomes (_e.g._ the Lampreys), and possibly in all, there are structures which very probably represent a primitive lower jaw (Meckel's cartilages); but such structures are always non-biting, and merely form skeletal supports for other portions of the skull. In place of biting jaws the mouth is provided with a complex rasping lingual apparatus supported by special cartilages, the so-called tongue, which bears horny teeth and is capable of protrusion and retraction. Paired limbs are entirely wanting.

In the Gnathostomata, on the contrary, there is no buccal funnel, and the mouth, whether terminal or ventral in position, opens directly outwards. The hypophysis is usually carried inwards with the stomatodaeal invagination which in the embryo gives rise to the mouth, and is therefore from the first in relation with the ventral surface of the brain. Biting jaws (palato-quadrate and Meckelian cartilages), formed by the modification of an anterior and primitively gill-bearing visceral arch, are {148}invariably present. The olfactory organs are obviously paired, and they are distinct from the hypophysis. Paired limbs are present.

As previously stated, the true Fishes form the second of the six "classes" into which the Craniata are divided. As compared with the higher Craniata, their distinctive characters may be concisely stated as follows:—