ARCHIANNELIDA, POLYCHAETA, AND MYZOSTOMARIA

BY

W. BLAXLAND BENHAM, D.Sc. (Lond.), Hon. M.A. (Oxon.)

CHAPTER IX

THE CHAETOPODOUS WORMS—THE ARCHIANNELIDA—ANATOMY OF NEREIS, AS TYPICAL OF THE POLYCHAETA

Those animals which possess lateral bundles of bristles (technically termed "chaetae") for use in locomotion constitute the group of "Bristle-worms," or Chaetopoda. The body of these animals is made up of a preoral lobe or prostomium, and a number of more or less distinct segments following one another in a line, and repeating one another in their internal and external structure. The Chaetopoda embrace the following smaller groups or Orders:—I. Archiannelida, II. Polychaeta, III. Myzostomaria, IV. Oligochaeta. The Archiannelida, although without the characteristic chaetae, are yet anatomically so similar to the true Chaetopoda that they must be included in the group, just as certain fishes are classed as "Vertebrata," although they do not possess vertebrae. The old term Annelida is sometimes used to include the above-mentioned groups, together with the Gephyrea^[292] and the Hirudinea or leeches.

Order I. Archiannelida.

The Archiannelida are very simple worms, but simplicity may be, and very frequently is, the result of degeneration; and it is not always possible to determine whether a simple animal is primitively, i.e. ancestrally simple, or whether it is secondarily simplified. Hence the term Haplodrili has been employed by Professor Lankester as the name of the group; a term which does not prejudge the question as to whether or not the worms are "primitive." It is quite possible, and even probable, that Dinophilus is ancestrally simple; whilst many features in Polygordius appear to be the result of simplification. For this reason it would be well to separate Dinophilus from the other two genera, on account of its much less elaborate and more generalised structure,—so generalised, in fact, that the worm is by some authorities placed amongst the Planarians; for the present, however, the group Archiannelida may be regarded as containing three genera: Dinophilus, Protodrilus, and Polygordius.^[293]

Dinophilus is represented on our coasts by at least two species: D. gigas Weldon^[294] and D. taeniatus Harmer.^[295] The latter is about one-twelfth of an inch in length, bright orange in colour, and more or less abundant, at springtime, in the rock pools around Plymouth, where it may be found amongst green algae, or on the mud at the bottom of the pools.

The animal consists of a broad prostomium, with a pair of eyes; and of a body, distinctly constricted in immature specimens into five or six segments, followed by a short conical tail. There are neither chaetae nor tentacles; locomotion is chiefly effected by means of the bands of cilia which encircle the body in a regular fashion, two bands round the head, and two round each segment in D. taeniatus; in some species there is only a single band on each segment. The whole of the ventral surface is covered with cilia, by the aid of which the animal probably "creeps" along the weeds.

The alimentary canal is straight, and divisible into the regions shown in Fig. 121; a muscular protrusible organ, which is a ventral outgrowth of the foregut, is employed as a "sucker." The coelom is more or less obliterated (or ill developed). The excretory system in the genus is varied: in some species, as in D. gigas, it is stated to be constructed on the Planarian plan; in others, as in D. taeniatus, the organs are definite nephridia. Of these tubes there are five pairs, the last pair in the male serving as a seminal vesicle. Each nephridium is a ciliated tube, the internal end of which lies in the body-cavity and appears to be blocked by a ciliated tongue-shaped appendage. The first pair corresponds to the "larval nephridia" of Trochosphere larvae.

The nervous system, which is in contact with the epidermis, consists of a brain in the prostomium, and, on each side of the body, a ventral cord with five ganglia, connected by transverse commissures in as many segments.

The sexes are separate, and are usually similar; the male of D. gyrociliatus is, however, much smaller than the female. The generative organs occupy the greater part of the body-cavity; in the male the testes communicate, by means of the pair of seminal vesicles, with a median eversible apparatus. In the female the paired ovaries communicate with a median sac which serves as a spermatheca.

The development is simple:^[296] the worm itself is more like a larval Polychaete than a full-grown worm. Dinophilus is an extremely interesting form, and it has been suggested that, while still possessing certain Planarian characteristics, it may be looked upon as closely resembling the ancestor from which the Chaetopoda have arisen.

Protodrilus and Polygordius are distinctly Annelidan in character. Protodrilus^[297] is found in the mud of the "Pantano," an inlet of the sea near Messina; whilst of Polygordius^[298] one species at least occurs on our shores, and several others in the Mediterranean and elsewhere. The worms are cylindrical, with many segments, but these segments are only indistinctly marked externally—by girdles of cilia in Protodrilus, or by faint grooves in Polygordius; but there are none of the characteristic Chaetopod bristles or chaetae. The small prostomium which overhangs the mouth is provided with a pair of ciliated pits, and carries a pair of tentacles, serving as sensory organs, which, in Protodrilus, are also respiratory. The anus is surrounded by glandular papillae in Polygordius, by means of which the animal can fix itself; these are represented in Protodrilus by a couple of processes.

The nervous system lies entirely in the epidermis. The body-cavity is regularly segmented by transverse septa passing from the body-wall to the intestinal wall. The foregut presents a slight eversible portion in Polygordius, whilst in Protodrilus it has a peculiar U-shaped muscular diverticulum on its ventral surface, corresponding with the similar apparatus in Dinophilus; it is capable of eversion, and aids the worm in burrowing, as well as in seizing and swallowing the mud. The vascular system is represented by a dorsal and a ventral vessel, neither of which, however, is contractile. In Protodrilus the dorsal vessel divides into two branches in the first segment, each of which passes to the tip of the tentacle, and returning, joins its fellow to form the ventral vessel. In some species of Polygordius there is a pair of vessels connecting the dorsal and ventral vessels in every segment, but no vessel to the tentacle. The blood is colourless in some species of Polygordius, but may be yellow (P. neapolitanus), red (P. lacteus), or green (P. erythrophthalmus). Paired nephridia, with distinct funnels, occur regularly throughout the body.

The sexes are separate in Polygordius, whilst Protodrilus is hermaphrodite, bearing ova in the first seven segments and testes in the remaining segments. The genital cells are produced from the body-wall in every segment; their mode of discharge is unknown in the male Polygordius, though probably the nephridia convey the spermatozoa to the exterior; but in the female the body-wall ruptures to allow the ova to escape, and then the animal dies. The development of Polygordius has been made the subject of very careful study; the larva has long been known, and is a typical "trochosphere" of rather a depressed form. This "trochosphere" larva is of considerable importance, as it makes its appearance in sundry groups of animals in some form or another. Here, in Polygordius, it has the appearance of a couple of wide but low cones united together by their bases, which form the equator of the larva. This equator carries a double girdle of cilia, dividing the animal into a preoral and postoral region; for the mouth is placed on one side of the animal between the two girdles, while the anus lies at the apex of the postoral cone, and is surrounded by another girdle of cilia. The alimentary canal is divisible into three regions; it is separated from the body-wall by an extensive space, which contains cells destined to give rise to muscles and nephridia. A nervous system (apical plate) is present at the apex of the preoral cone. This little larva swims freely on the surface of the sea, moving, balancing, and feeding by means of the girdle of cilia. It soon increases in length by the active growth of the apex of the postoral cone, which becomes cylindrical and then segmented externally and internally. The greater part of the original larva remains of the same shape as before, and forms the head (prostomium and peristomium): small tentacles grow out of the preoral lobe, and after a gradual reduction in the relative size of the "head" by the growth of the segmented "body," the animal becomes worm-like and develops into a Polygordius.^[299]

Order II. Polychaeta.

Anatomy of Nereis.—In order to obtain a general idea of a Polychaete worm, it is well to study a concrete example, and for this purpose the common Nereis serves excellently. Several species (see p. 315) occur more or less commonly on our coasts, and the general remarks will apply to one as well as to another.

Nereis pelagica Linnaeus reaches a length of 5 to 6 inches, and is about ¼ inch across. It is convex above, nearly flat below. Its colour is brown or bronze. The worm, which is to be found in shallow water, is made up of a considerable number of rings or segments, constituting the "trunk" or "body," terminated at each end by modified segments known as "head" and "tail" (Fig. 122). The segments composing the trunk are all alike, except for small proportional differences, and it will be convenient to describe a "typical segment" before referring to the head or tail.

A typical body segment carries on each side a muscular lobed outgrowth, bearing bundles of bristles or "chaetae," and filamentous sensory organs known as "cirri." To this lateral locomotor organ Huxley gave the name "parapodium" (Fig. 124). Each parapodium or foot consists of a basal portion, supporting a dorsal and a ventral process, the "notopodium" (ntp) and "neuropodium" (nrp) respectively, each of which is bilobed. The lobes are very vascular and glandular, and probably serve as respiratory organs or "gills."

The chaetae, or bristles, of each bundle project from the mouth of a great sac, the lips of which are particularly prominent in Nereis. Each chaeta arises from a single cell situated at the bottom of the sac. The chaetae of Nereis, as of many other Polychaetes, are of a kind usually termed compound or "jointed," each being composed of a long stalk and a small "appendix" articulated in a cup at its extremity (Fig. 123). The shape of the cup varies; it is in some cases of equal height all round, or it is higher on one side than on the other. Further, the appendix may be short and curved, or more elongate and spear-like; it is generally notched or finely toothed on one side.

In addition to these projecting locomotor chaetae, there is embedded in each of the two chaetigerous lobes a much stouter and dark-coloured, needle-shaped bristle known as an "aciculum," whose point only just projects beyond the surface. This aciculum extends into the interior of the body much farther than do the locomotor chaetae, and it is to it that the muscles serving to move the whole bundle of chaetae are attached. The acicula thus serve as an internal skeleton to the parapodium. The shape of the parapodium, the relative lengths of cirri and lobes, the shape and arrangement of the chaetae, are all employed as specific characters.

The head consists of a preoral portion above the mouth, the "prostomium," and a postoral region surrounding the mouth, the "peristomium" (Fig. 125). The prostomium varies in shape in different species of Nereis; but it always carries on its dorsal surface two pairs of eyes. From its narrower anterior end there arises a pair of short, somewhat conical, sensory processes known as the "prostomial tentacles." A second pair of processes springs from the under surface, and rather to the side of the prostomium; these are known as the "palps," and in Nereis are much more conspicuous than the tentacles; each is composed of two parts, a large basal piece and a smaller terminal joint, capable of being withdrawn into the former. The palps are highly muscular, and though they are sensory organs, act also as great lateral lips.

The peristomium is in many species of Nereis (as in N. pelagica) considerably larger than the trunk segments; it carries at its anterior edge four filiform cirri on each side, which are directed forwards and used as feelers. They are arranged in couples; a more anterior couple of dorsal and ventral cirri, and a more posterior couple of dorsal and ventral cirri.

The Tail.—As the most anterior segment is perforated by the mouth, and is modified as described above, so the last or anal segment, which carries the anus, differs from the rest. It is more or less elongated, cylindrical, and without parapodia or chaetae. It retains, however, its pair of ventral cirri, which are very long.

Internal Anatomy.—In correspondence with the external metamerism there is an internal repetition of parts. For, except in the anterior segments, where the powerful protrusible pharynx is situated, the body-cavity or "coelom" is divided into a series of chambers, by means of muscular septa inserted, on the one hand, into the body-wall at the level of the grooves between the external segments, and, on the other, into the wall of the alimentary canal. Each of these coelomic chambers contains a pair of nephridia, a portion of the intestine, of the vascular system, and of the nervous system, as will be seen in Fig. 124.

The epidermis, which forms the outer part of the body-wall, consists of a single layer of cells, covered externally by a thin, tough cuticle. The latter is usually stated to consist of the chemical substance known as chitin, but since the cuticle differs from true chitin by dissolving in caustic potash after a time, Eisig^[300] has suggested that its substance is merely a stage in the formation of chitin. The epidermis contains gland-cells, which are especially abundant on the lobes of the parapodia. Below the epidermis lies the circular coat of muscles by whose contraction the worm diminishes its diameter: it is interrupted on each side at the junction of the parapodium with the body. Deeper still lie the longitudinal muscles, which form four great bundles, two dorsal, separated by the insertion of a small mesentery and dorsal blood-vessel, and two ventral bundles separated in the middle line by the nerve-cords. These longitudinal muscles, by their contraction, bend the worm from side to side, and are continuous from segment to segment. A very characteristic muscle, present in all the Polychaeta, is an obliquely transverse sheet of fibres passing from the body-wall at the side of the nerve-cord to the parapodium, where it spreads out and serves to move the parapodium (Fig. 124). All these muscles consist of smooth fibres, as in the earthworm.

The alimentary canal may be divided into the following four regions:—(1) buccal or eversible region, (2) pharynx, carrying the great jaws, (3) oesophagus, (4) intestine.

The first two regions constitute an "introvert" (Lankester^[301]). When fully everted the whole of the buccal region is turned inside out, and the terminal aperture leads directly into the pharynx, which is not everted but merely protruded. Throughout the following chapters the word "buccal" region is used for that part—if any—which is thus everted (Figs. 125, 126).

Both the buccal and pharyngeal regions are wrapped round by several coats of muscle, to form apparently a single muscular organ (Fig. 127, sh), which occupies about eight segments in a condition of complete introversion. The septa are absent from the anterior part of the body.

The buccal region is lined with chitin, which is specially thickened at certain definite spots, forming small "denticles" or "paragnaths" (Fig. 125), which have a different arrangement in the various species.

The cavity of the pharynx is narrow and the walls thick and muscular; each side wall carries a large, dark, chitinous "jaw" (Fig. 127, J), which is hollow at the base, into which the muscles serving to move it are inserted, whilst the apex is solid, curved, and more or less notched. These two great jaws are used not only for tearing prey, but for seizing it; for when the pharynx is entirely protruded the two jaws are wide apart, and when retraction takes place they come together and grasp the prey.

Eversion of the apparatus is partly effected by protractor muscles (Fig. 126, A, p) and partly by the pressure of the coelomic fluid, compressed by the muscles of the body-wall; the eversion is stopped at a certain stage by a sheet of muscular tissue or "diaphragm" (Fig. 127, diaph) inserted round the buccal region and attached to the body-wall in the second segment. The introversion is effected partly by the contraction of this diaphragm and partly by the action of powerful retractor muscles (Fig. 126, r) inserted into the hinder end of the pharynx and passing to the body-wall (these are removed in Fig. 127). The movement of the jaws themselves and of the wall of the apparatus is due to other muscles.

The oesophagus is quite short; into it opens a pair of sacculated diverticula or glands. Then follows the intestine, which extends through the rest of the body as a thin-walled tube, slightly dilated at the insertion of the septa.

The vascular system consists of a contractile dorsal vessel and of a non-contractile ventral vessel extending along the whole length of the body, from each of which paired and segmentally-arranged vessels pass to the intestinal wall and to the body-wall, and here form extensive capillary networks (Fig. 124, p. 247). This type of vascular system is pretty generally adhered to throughout the Order, but in the Terebelliformia, Scoleciformia, and Cryptocephala the dorsal vessel and capillary plexus on the intestine are replaced by a continuous blood sinus, situated in the substance of the gut-wall. This "perienteric sinus" has the same relation to the segmental vessels as the dorsal vessel has in the Nereidiformia, and from it a tubular dorsal vessel arises anteriorly. In Arenicola the sinus is preceded in the young stage by a network the branches of which gradually enlarge, meet, and fuse to form the sinus.^[302] Whether it is in all cases secondary is a moot point.

This system of vessels in the majority of Chaetopoda contains a respiratory fluid coloured red^[303] by haemoglobin in solution; in it float a very few small oval nucleated non-amoeboid corpuscles. But the place of this red pigment is taken by a green one, named "chlorocruorin," in the Chlorhaemidae and many Sabelliformia;^[304] whilst in Magelona^[305] the blood is tinted madder-pink by a number of globules of "haemerythrin." The blood (or "haemal fluid") is driven forwards in the dorsal vessel, and passes backwards in the ventral vessel. Respiration in Nereis is carried on by the whole surface of the body, but naturally with greater activity in the surface of the parapodia, the lobes of which, with their extensive vascular plexus, may be termed "gills"; but it must be borne in mind that these organs have other functions as well.

The coelomic fluid, which fills the general body-cavity, is colourless, and contains amoeboid corpuscles or "leucocytes." It corresponds to the lymph of Vertebrates, being nutritive in function, in that it conveys absorbed material from the wall of the intestine to the organs of the body, and at the same time removes any waste substances from these organs; these waste substances contain nitrogen, and are ultimately removed by the nephridia. In Ophelia many of the corpuscles contain a curious dumb-bell-shaped rod of chitin, and it has been shown^[306] that this substance is a highly complex form of excretory material,—more complex than guanin, for instance, which exists in the corpuscles of the Capitelliformia.

In Glyceridae, Capitelliformia, and Polycirrus haematodes (a Terebellid), the vascular system is absent, and the coelomic corpuscles become coloured by haemoglobin, and in order that the coelomic fluid may be distributed to the organs of the body, the peritoneum is ciliated along certain definite tracts. The fluid in these "anangian" worms thus combines originally separate functions, and behaves like the "blood" of Vertebrates.

The excretory system is represented by a pair of nephridia in each segment, with the exception of a few anteriorly and a few posteriorly. The nephridium of Nereis differs from that of most other Polychaetes hitherto examined carefully, and rather resembles that of the Oligochaetous Enchytraeids. It consists of a compact gland-like organ, containing a much coiled tube, ciliated for the greater part of its length, but deprived of cilia in its last coils; this latter part—or duct—leaves the "gland" and pierces the body-wall, opening to the exterior at the base of the parapodium. The ciliated canal passes forwards into the next segment, where it opens by a funnel into the coelom. The lip of the funnel is extremely curious, for the cells constituting it are drawn out into very long, delicate processes covered with cilia.^[307]

In most Polychaetes the nephridium is a wide, sac-like tube as in Arenicola^[308] (Fig. 129). Its walls are covered by a dense network of blood-vessels, and it not only acts as an excretory organ, but also as a genital duct (see p. 273).

Excretion, in the strict sense of the word, is carried out by the cells forming the wall of the tube; they remove waste materials from the blood distributed over the surface of the organ. But, in addition, there is a removal from the coelom, by means of the funnel, of any dead or dying coelomic corpuscles which in their turn have eaten up or otherwise destroyed foreign bodies (such as Bacteria, etc.) that may have entered the animal.

In Nereis there is in each segment, in addition to the pair of nephridia, a pair of "dorsal ciliated organs" (Goodrich) (cil.org in Fig. 124). Each appears as a wide-mouthed funnel, greatly folded, and without any permanent outlet. But it is possible that these organs function as genital ducts, and that the external aperture will make its appearance temporarily at the period of maturity. This "dorsal ciliated organ" has not been met with in allied genera—such as Eunice, Nephthys, Polynoë, Glycera—where the nephridium is a wide tube, and serves as a genital duct.

The nervous system, as in all Chaetopods, consists of a dorsal cerebral ganglion or "brain" (Fig. 127, br), connected by circum-buccal commissures with the anterior end of a ventral chain of ganglia. The brain occupies the prostomium,^[309] and from it nerves pass away to the prostomial tentacles and palps. The circum-buccal commissures spring from the outer corner of the brain, and from each arises a nerve to the first pair of peristomial cirri. The first ventral ganglion lies in the third segment, and represents at least two ganglion-pairs fused together, for from it arise (1) a pair of nerves to the second pair of peristomial cirri and (2) a pair to the first parapodium. In the remainder of the body there is a ganglion in each segment, whence nerves pass outwards to the parapodium and muscles of the segment (Fig. 124).

In Nereis the apparently single ganglion in each segment really consists of two halves, and the apparently single cord which traverses the whole length of the body consists of two closely apposed cords. In some worms, such as Serpulidae, the two cords are more or less widely separated, and the two ganglia of each segment are thus distinct, and connected by a transverse commissure. In Nereis, as well as in many other Polychaeta, the nerve-cords lie within the body-wall, but in other cases they lie in the epidermis, as they do in Archiannelida.

The visceral nervous system, supplying the muscles of the pharynx, is frequently highly developed. In Nereis it arises on each side by two roots, one from the brain, the second from the circum-buccal commissure.

The organs of sense in Nereis are eyes, tentacles, palps, and cirri. The four eyes, which rest upon the brain, have the structure represented in Fig. 130. The retina consists of a single layer of cells containing pigment; each cell is drawn out peripherally into a nerve-fibre, whilst centrally it forms a cuticular product—the "rod" (h). The edges of the retina are continuous with the surrounding epidermis, and the cup thus formed remains widely opened to the cuticle in a few Polychaetes, e.g. Autolytus, and in the young of Nereis, but more usually it has the relations represented in the figure. The lens is produced by the retinal cells (according to Andrews^[310]), and is in some cases (Eunice, Amphinome) continuous with the cuticle. It appears to be composed in other cases (Lepidonotus) of continuations of the retinal rods. The structure of the other sense organs indicates their adaptation to a tactile function; in each case a nerve traverses the axis of the organ, and the nerve-fibrils terminate in sensory cells. Very probably the palps have a certain power of testing the food—a combination of the senses of taste and smell.

The Generative System.—In all the Polychaeta, with very few exceptions, the sexes are separate; and the reproductive cells—ova and spermatozoa—are produced at certain seasons of the year by the rapid proliferation and modification of coelomic epithelial cells surrounding the blood-vessels in the parapodium and its immediate neighbourhood. The sexual cells remain in the coelom till they are ripe.

The egg-cells become filled with yolk globules; a vitelline membrane is present, and an outer coat of albuminous material. It is doubtful by what means these sexual cells are discharged in Nereis. There is some evidence that the "dorsal ciliated organ" may act as a genital duct. In some other worms the nephridia serve this purpose, whilst in others a rupture of the body-wall allows the products to escape into the sea. According to Wistinghausen,^[311] at the time of discharge the females of Nereis dumerilii become surrounded by a kind of gelatinous tube formed from a secretion of the parapodial glands, and into this tube the ova are discharged, and arranged in a single layer round its wall.

The common species Nereis diversicolor is viviparous. In a large number of species of Nereis the sexually-mature individuals undergo very marked changes in various parts of their body, so that they differ very greatly from the immature individuals.

These changes resulting in the "heteronereid" condition will be dealt with at some length in Chap. X. p. 276. The larvae of Polychaetes and other facts connected with reproduction are described in the same chapter.