BALANOGLOSSUS, the general name given to certain peculiar, opaque, worm-like animals which live an obscure life under stones, and burrow in the sand from between tide-marks down to the abyssal regions of the sea. Their colour is usually some tone of yellow with dashes of red, brown and green, and they frequently emit a pungent odour. The name has reference to the tongue-shaped muscular proboscis by which the animal works its way through the sand. The proboscis is not the only organ of locomotion, being assisted by the succeeding segment of the body, the buccal segment or collar. By the waves of contraction executed by the proboscis accompanied by inflation of the collar, progression is effected, sometimes with marvellous rapidity. The third body region or trunk may attain a great length, one or two feet, or even more, and is also muscular, but the truncal muscles are of subordinate importance in locomotion, serving principally to promote the peristaltic contractions of the body by which the food is carried through the gut. The function of alimentation is closely associated with that of locomotion, somewhat as in the burrowing earthworm; in the excavation of its burrows the sand is passed through the body, and any nutrient matter that may adhere to it is extracted during its passage through the intestine, the exhausted sand being finally ejected through the vent at the orifice of the burrow and appearing at low tide as a worm casting. In accordance with this manner of feeding, the mouth is kept permanently open and prevented from collapsing by a pair of skeletal cornua belonging to a sustentacular apparatus (the nuchal skeleton), the body of which lies within the narrow neck of the proboscis; the latter is inserted into the collar and surrounded by the anterior free flap of this segment of the body.
When first discovered by J. F. Eschscholtz at the Marshall Islands in 1825, Balanoglossus was described as a worm-like animal belonging to the Echinoderm order of Holothurians or sea-cucumbers. In 1865 Kowalevsky discovered that the organs of respiration consist of numerous pairs of gill-slits leading from the digestive canal through the thickness of the body-wall to the exterior. On this account the animal was subsequently placed by Gegenbaur in a special class of Vermes, the Enteropneusta. In 1883-1886 Bateson showed by his embryological researches that the Enteropneusta exhibit chordate (vertebrate) affinities in respect of the coelomic, skeletal and nervous systems as well as in regard to the respiratory system, and, further, that the gill-slits are formed upon a plan similar to that of the gillslits of Amphioxus, being subdivided by tongue-bars which depend from the dorsal borders of the slits.
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In correspondence with the tri-regional differentiation of the body in its external configuration, the coelom (body-cavity, perivisceral cavity) is divided into three portions completely separated from one another by septa: - (I) proboscis-coelom, or first body-cavity; (2) the collar-coelom, or second body-cavity; (3) truncal coelom, or third body-cavity. Of these divisions of the coelom the first two communicate with the exterior by means of a pair of ciliated pore-canals placed at the posterior end of their respective segments. The proboscis-pores are highly variable, and frequently only one is present, that on the left side; sometimes the pore-canals of the proboscis unite to open by a common median orifice, and sometimes their communication with the probosciscoelom appears to be occluded, and finally the pore-canals may be quite vestigial. The collar-pores are remarkable for their constancy; this is probably owing to the fact that they have become adapted to a special function, the inhalation of water to render the collar turgid during progression. There are reasons for supposing that the truncal coelom was at one time provided with pore-canals, but supposed vestiges of these structures have only been described for one genus, Spengelia,in which they lie near the anterior end of the truncal coelom.
Not only is the coelom thus subdivided, but the enteron (gut, alimentary canal, digestive tube) itself shows indications of three main subsections in continuity with one another: - (I) proboscis-gut (Eicheldarm, stomochord, vide infra); (2) collar-gut (buccal cavity, throat); (3) truncal gut extending from the collar to the vent.
The proboscis-gut occurs as an outgrowth from the anterior dorsal wall of the collar-gut, and extends forward into the basal (posterior) region of the proboscis, through the neck into the proboscis-coelom, ending blindly in front. Although an integral portion of the gut, it has ceased to assist in alimentation, its epithelium undergoes vacuolar differentiation and hypertrophy, and its lumen becomes more or less vestigial. It has, in fact, become metamorphosed into a resistant supporting structure resembling in some respects the notochord of the true Chordata, but probably not directly comparable with the latter structure, being related to it solely by way of substitution. On account of the presence and mode of origin (from the gut-wall) of this organ Bateson introduced the term hemichorda as a phyletic name for the class Enteropneusta. As the proboscis-gut appears to have undoubtedly skeletal properties, and as it also has topographical relations with the mouth, it has been designated in English by the non-committal term stomochord. It is not a simple diverticulum of the collar-gut, but a complex structure possessing paired lateral pouches and a ventral convexity (ventral caecum) which rests in a concavity at the f_ ont end of the body of the nuchal skeleton (fig. 3). In some species (Spengelidae) there is a long capillary vermiform extension of the stomochord in front. The nuchal skeleton is a non-cellular laminated thickening of basement-membrane underlying that portion of the stomochord which lies between the above-mentioned pouches and the orifice into the throat. At the point where the stomochord opens into the buccal cavity the nuchal skeleton bifurcates, and the two cornua thus produced pass obliquely backwards and downwards embedded in the wall of the throat, often giving rise to projecting ridges that bound a dorsal groove of the collar-gut which is in continuity with the wall of the stomochord (fig. 3) Nervous System. - At the base of the epidermis (which is in general ciliated) there is over the entire surface of the body a layer of nervefibres, occurring immediately outside the basement-membrane which separates the epidermis from the subjacent musculature. The nervous system is thus essentially epidermal in position and diffuse in distribution; but an interesting concentration of nerve-cells and fibres has taken place in the collar-region, where a medullary tube, closed in from the outside, opens in front and behind by anterior and posterior neuropores. This is the collar nerve-tube. Sometimes the central canal is wide and uninterrupted between the two neuropores; in other cases it becomes broken up into a large number of small closed medullary cavities, and in others again it is obsolete. In one family, the Ptychoderidae, the medullary tube of the collar is connected at intermediate points with the epidermis by means of a variable number of unpaired outgrowths from its dorsal wall, generally containing an axial lumen derived from and in continuity with the central canal. These hollow roots terminate blindly in the dorsal epidermis of the collar, and place the nervous layer of the latter in direct connexion with the fibres of the nerve-tube. The exact significance of these roots is a matter for speculation, but it seems possible that they are epiphysial structures remotely comparable with the epiphysial (pineal) complex of the craniate vertebrates. In accordance with this view there would be also some probability in favour of regarding the collar nerve-tube of the Enteropneusta as the equivalent of the cerebral vesicle only of Amphioxus and the Ascidian tadpole, and also of the primary forebrain of vertebrates.
Special thickenings of the diffuse nervous layer of the epidermis occur in certain regions and along certain lines. In the neck of the proboscis the fibrous layer is greatly thickened, and other intensifications of this layer occur in the dorsal and ventral middle lines of the trunk extending to the posterior end of the body. The dorsal epidermal nerve-tract is continued in front into the ventral wall of the collar nerve-tube, and at the point of junction there is a circular commissural thickening following the posterior rim of the collar and affording a special connexion between the dorsal and ventral nervetracts. From the ventral surface of the collar nerve-tube numerous motor fibres may be seen passing to the subjacent musculature. These fibres are not aggregated into roots.
FIG. I. - Ptychodera flava (New Caledonia), from above; about life size.
The possession of gill-slits is as interesting a feature in the organization of Balanoglossus as is the presence of tracheae in Peripatus. These gill-slits occupy a variable extent of the anterior portion of the trunk, commencing immediately behind the collartrunk septum. The branchial bars which constitute the borders of the clefts are of two kinds: - (i) Septal bars between two contiguous clefts, corresponding to the primary bars in Amphioxus; (2) Tongue bars. The chief resemblances ------ between Balanoglossus an Amphioxus in respect of `'?'the gill-slits may be stated briefly as follows: - (a) the presence of two kinds of branchial bars in all species and also of small cross bars (synapticula) in many species; (s) numerous gill slits, from forty to more 1 - _ than a hundred pairs; (y) the addition of new gill-slits by fresh perforation at the posterior end of the pharynx throughout life. The chief differences are, that (a) the tongue-bar is the essential vm, organ of the gill-slit in Balanoglossus, and exceeds FIG. 2. - Structure of branchial region. the septal bars in bulk, bc, coelom. gp, gill-pore. while in Amphioxus the tb, tongue-bars. dn, dorsal nerve. reverse is the case; (b) the ds, mesentery. dv, vessel. tongue-bar contains a large pr, ridge. ce, oesophagus. coelomic space in Balano- vv, vessel. vs, mesentery. glossus, but is solid in Am- vn, ventral nerve. phioxus; (c) the skeletal rods in the tongue-bars of Balanoglossus are double; (d) the tongue-bar in Balanoglossus does not fuse with the ventral border of the cleft, but ends freely below, thus producing a continuous U-shaped cleft. The meaning of this singular contrast between the two animals may be that we have here an instance of an interesting gradation in evolution. From serving primitively as the essential organ of the cleft the tongue-bar may have undergone reduction and modification, becoming a secondary bar in Amphioxus, subordinate to the primary bars in size, vascularity and development; finally, in the craniate vertebrates it would then have completed its involution, the suggestion having been made that the tongue-bars are represented by the thymusprimordia.
Gill-pouches and Gill-pores.--Only rarely do the gill-slits open freely and directly to the exterior (fig. 1). In most species of Balanoglossus each gill-slit may be said to open into its own atrial chamber or gill-pouch; this in its turn opens to the exterior by a minute gill-pore. There are, therefore, as many gill-pouches as there are gill-slits and as many gill-pores as pouches. The gill-pores occur on each side of the dorsal aspect of the worm in a longitudinal series at the base of a shallow groove, the branchial groove. The respiratory current of water is therefore conducted to the exterior by different means from that adopted by Amphioxus, and this difference is so great that the theory which seeks to explain it has to postulate radical changes of structure, function and topography.
It seems likely that the coelomic pore-canals were originally excretory organs, but in the existing Enteropneusta the pore-canals (especially the collar canals) have, as we have seen, acquired new functions or become vestigial, and the function of excretion is now mainly accomplished by a structure peculiar to the Enteropneusta called the glomerulus, a vascular complex placed on either side of the anterior portion of the stomochord, projecting into the proboscis-coelom. The vascular system itself is quite peculiar, consisting of lacunae and channels destitute of endothelium, situated within the thickness of the basementmembrane of the body-wall, of the gut-wall and of the mesenteries. The blood, which is a non-corpuscular fluid, is propelled forwards by the contractile dorsal vessel and collected into the central bloodsinus; this lies over the stomochord, and is surrounded on three sides by a closed vesicle, with contractile walls, called the pericardium (Herzblase). By the pulsation of the pericardial vesicle (best observed in the larva) the blood is driven into the glomerulus, from which it issues by efferent vessels which effect a junction with the ventral (sub-intestinal) vessel in the trunk. The vascular system does not readily lend itself to morphological comparison between such widely different animals as Balanoglossus and Amphioxus, and the reader is therefore referred to the memoirs cited at the end of this article for further details.
The sexes are separate, and when mature are sometimes distinguished by small differences of colour in the genital region. Both male and female gonads consist of more or less lobulated hollow sacs connected with the epidermis by short ducts. In their disposition they are either uniserial, biserial or multiserial. They occur in the branchial region, and also extend to a variable distance behind it. In exceptional cases they are either confined to the branchial region or excluded from it. When they are arranged in uniserial or biserial rows the genital ducts open into or near the branchial grooves in the region of the pharynx and in a corresponding position in the post-branchial region. An important feature is the occurrence in some species (Ptychoderidae) of paired longitudinal pleural or lateral folds of the body which are mobile, and can be approximated at their free edges so as to close in the dorsal surface, embracing both the median dorsal nerve-tract and the branchial grooves with the gill-pores, so as to form a temporary peri-branchial and medullary tube, open behind where the folds cease. On the other hand, they can be spread out horizontally so as to expose their own upper side as well as the dorsal surface FIG. 3. - Structure of anterior end.
a, Arrow from proboscis-cavity (pc) passing to left of peri cardium (per) and out through proboscis pore-canal.
b', arrow from central canal of neurochord (cnc) passed out through anterior neuropore. b 2 , ditto, through posterior neuro pore.
c, arrow intended to pass from 1st gill-pouch through collar pore-canal into collar-coelom (cc).
of the body (fig. I). These folds are called the genital pleurae because they contain the bulk of the gonads. Correlated with the presence of the genital pleurae there is a pair of vascular folds of the basement membrane proceeding from the dorsal wall of the gut in the postbranchial portion of the branchio-genital region, and from the dorsal angles made by the pleural folds with the body-wall in the pharyngeal region; they pass, in their most fully developed condition, to the free border of the genital pleurae. These vascular membranes are called the lateral septa. Since there are many species which do not possess these genital pleurae, the question arises as to whether their presence or their absence is the more primitive condition. Without attempting to answer this question categorically, it may be pointed out that within the limits of the family (Ptychoderidae) which is especially characterized by their presence there are some species in Y art dY YY cts, posterior limit of collar.
dv, dorsal vessel passing into central sinus (bs).
ev, efferent vessel passing into ventral vessel (vv).
epr, epiphysial tubes.
vs, ventral septum of proboscis. sk, body of nuchal skeleton. m, mouth.
tc, trunk coelom.
which the genital pleurae are quite obsolete, and yet lateral septa occur (e.g. Ptychodera ruficollis), seeming to indicate that the pleural folds have in such cases been secondarily suppressed.
The development of Balanoglossus takes place according to two different schemes, known as direct and indirect, correlated with the occurrence in the group of two kinds of ova, large and small. Direct development, in which the adult form is achieved without striking metamorphosis by a gradual succession of stages, seems to be confined to the family Balanoglossidae. The remaining two families of Enteropneusta, Ptychoderidae and Spengelidae, contain species of which probably all pursue an indirect course of development, culminating in a metamorphosis by which the adult form is attained. In these cases the larva, called Tornaria, is pelagic and transparent, and possesses a complicated ciliated seam, the longitudinal ciliated band, often drawn out into convoluted bays and lappets. In addition to this ciliated band the form of the Tornaria is quite characteristic and unlike the adult. The Tornaria larva offers a certain similarity to larvae of Echinoderms (sea-urchins, star-fishes, and sea-cucumbers), and when first discovered was so described. It is within the bounds of possibility that Tornaria actually does indicate a remote affinity on the part of the Enteropneusta to the Echinoderms, not only on account of its external form, but also by reason of the possession of a dorsal water-pore communicating with the anterior body-cavity. In the direct development Bateson showed that the three divisions of the coelom arise as pouches constricted off from the archenteron or primitive gut, thus resembling the development of the mesoblastic somites of Amphioxus. It would appear that while the direct development throws light upon the special plan of organization of the Enteropneusta, the indirect development affords a clue to their possible derivation. However this may be, it is sufficiently remarkable that a small and circumscribed group like the Enteropneusta, which presents such a comparatively uniform plan of composition and of external form, should follow two such diverse methods of development.
Some thirty species of Balanoglossus are known, distributed among all the principal marine provinces from Greenland to New Zealand. The species which occurs in the English Channel is Ptychodera sarniensis. The Ptychoderidae and Spengelidae are predominantly tropical and subtropical, while the Balanoglossidae are predominantly arctic and temperate in their distribution. One of the most singular facts concerning the geographical distribution of Enteropneusta has recently been brought to light by Benham, who found a species of Balanoglossus, sensu stricto, on the coast of New Zealand hardly distinguishable from one occurring off Japan. Finally, Glandiceps abyssicola (Spengelidae) was dredged during the "Challenger" expedition in the Atlantic Ocean off the coast of Africa at a depth of 2500 fathoms.
Authorities.-W. Bateson, "Memoirs on the Direct Development of Balanoglossus," Quart. Journ. Mier. Sci. (vols. xxiv.-xxvi., 1884-1886); W. B. Benham, "Balanoglossus otagoensis, n. sp," Q. J. M. S. (vol. xlii. p. 497, 1899); Yves Delage and Ed. Herouard, Traite de zoologie concrete (t. viii.), "Les Procordes" (1898); S. F. Harmer, "Note on the Name Balanoglossus," Proc. Camb. Phil. Soc. (x. p. 190, 1900); T. H. Morgan, "Memoirs on the Indirect Development of Balanoglossus," Journ. Morph. (vol. v., 1891, and vol. ix., 1894); W. E. Ritter, "Harrimania maculosa, a new Genus and Species of Enteropneusta from Alaska," Papers from the Harriman Alaska Exhibition (ii.), Proc. Washington Ac. (ii. p. I11, 1900); J. W. Spengel, "Die Enteropneusten," Eighteenth Monograph on the Fauna and Flora des Golfes von Neapel (1893); A. Willey, "Enteropneusta from the South Pacific, with Notes on the West Indian Species," Zool. Results (Willey), part iii., 1899; see also Q. J. M. S. (vol. xlii. p. 223, 1899); J. P. Hill, "The Enteropneusta of Funafuti," Mem. Austral. Mus. (iii., 1897-1898); M. Caullery and F. Mesnil, "Balanoglossus Kochleri, n. sp. English Channel," C. R. Soc. Biol. lii. p. 256 (19 Ao). (A. W.*)
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