Feeding Organs and Feeding Habits of Autolytus Edwarsi St. Joseph. (Studies on the Syllidae, I)
1928; The Company of Biologists; Volume: S2-72; Issue: 286 Linguagem: Inglês
10.1242/jcs.s2-72.286.219
ISSN1477-9137
Autores Tópico(s)Marine Biology and Ecology Research
ResumoIn connexion with experimental work, especially when an animal is required to be kept alive for a considerable time, it becomes highly important to find out exactly.what its food is and how it eats the food. The present work is the outcome of a suggestion made by Dr. E. J. Allen during my residence at Plymouth from June 1927.A. Malaquin (1893, p. 257) writes in his comprehensive work ‘sur les Syllidiens’, that ‘les aliments arrivent rapidement, grâce aux movements rapides du proventricule, dans l’intestin antérieur. Ces aliments sont de la vase fine, des petits animaux, des invidus appartenant aux colonies sur lesquelles les Syllidiens vivent; Bryozoaires (Bugula, Vesicularia, Membranipora, &c.), Hydraires (Sertularia, Hydralmania, &c.)’. However, he does not indicate what species of Bryozoa or Hydroides Syllids eat.Syllids at Woods Hole are described as living in a transparent case attached to Hydroids: Autolytus corn u t us A. Agassiz associating with Eudendrium and Penaria, Autolytus varians Verrill occurring in abundance on the stems of Parypha, and Autolytus ornatus Verrill among the colonies of Eudendrium and Parypha (P. C. Mensch, 1900, p. 269). But no account has been given of the feeding of these worms. So far as I am aware it is E. J. Allen (1921, p. 132) who has first described it clearly in Procerastea Hallenziana Malaquin.Procerastea is always associated with Syncoryne: it penetrates with its extruded proboscis the body-walls of the hydroid, just at the base of the hydranth, and pumps out the fluid or semi-fluid substance from the gastral cavity. The proventriculus acts like a pump. According to Allen the rhythm of this movement is at a rate of 150 to 200 per minute.Autolytus Edwarsi St. Joseph, upon which my observations and experiments have been carried out, is common at Plymouth. Here two forms exist, one of which lives in large numbers amongst colonies of the hydroid Obelia geniculata L., which occurs abundantly on Laminaria. The second form, found in dredgings from the outer ground of Plymouth Sound, is relatively longer and more slender in build (Allen, 1927, p. 874). This form seems to be associated with another species of Obelia (Obelia flabellata Hinck).Before going farther I wish to take this opportunity of expressing my gratitude to members of the staff of this Laboratory, especially to Dr. E. J. Allen, the director, and Mr. A. J. Smith, the chief laboratory attendant, for their kindness and help.The specimens of Autolytus supplied me seemed to have been living inside a membranous tube, which they had built on Laminaria covered by the colonies of Obelia geniculata L. When the Laminaria with the hydroid was placed in a dish of sea-water the Autolytus left their tubes, and in the course of a few hours crowded at the edge of the water. The worms show distinctly a photo-positive taxis not only to sunlight but also to electric light.In a glass dish of clean sea-water Autolytus can live for some days without food, and the majority of them form a tube which generally lies horizontally where the water meets the glass, but other tubes are found at the bottom. A few animals wander about the vessel without forming tubes, and still others creep above the level of the water when they dry up and perish.The tube is a little longer than the actual length of the worm and is open at both ends. It is transparent and, as has been described for Procerastea, sufficiently elastic for the dweller to turn round on itself and travel both up and down the tube. It appears to be woven by the worm itself, with very fine fibrils from a secretion of certain glands in the body-wall.At Plymouth at least Autolytus is always associated with Obelia, and since Bryozoa and Hydroids are known to be eaten by Syllids, it was probable that the present form lives upon Obelia. This could be most easily tested by giving the hydroid to the hungry worms. I have found that keeping them in a vessel of clean sea-water for two or three days is sufficient to make the worms hungry. With this preparation, when colonies of Obelia were put into the dish, the Autolytus left their tubes almost at once or in the course of a few hours. They first crept along the edge of the water but came down almost directly towards the hydroid. After a short while the animals were seen to creep along the stem of the Obelia and to keep on applying the protruded proboscis to the opening of the hydrotheca. From time to time they stopped at the same spot, and the pumping action, which Allen and Sexton had seen in Procerastea, was clearly observed in the muscular proventriculus. The movement was followed by slow but strong and more or less regularly periodical contractions of the intestine, and a stream of fluid flowed back through the proventricular lumen into the intestine; the animals were evidently feeding. They soon, however, withdrew the protruded pharynx and crept forwards and backwards to apply it to another hydranth. But sometimes they repeated the pumping action upon the same hydranth.Before entering into the main problem, i.e. the feeding mechanism, I give here with the aid of a diagram (Text-fig. 1) an illustration of the behaviour of a hungry worm when colonies of Obelia were put into the glass dish which contained it.In this case the experimental animal had built its tube in the middle of the bottom (position 1). As soon as the hydroids were put into the dish the animal left the tube and crept almost straight forwards, until near the edge of the bottom (position 2). Here it turned its head to the right side and, changing direction, crept back to the centre. Passing by one hydroid (c) it was attracted by the other (d), which was placed more centrally. The Autolytus fed three times on different polyps (IV, V, and VI) and abandoned this colony. It came up to the next hydroid (e), but making two complete rotations (at the positions 8 and 9) at the upper extremity of this hydroid, it proceeded forwards without touching any one of the hydranths. Arriving at the edge of the bottom (position 11), the animal seemed to hesitate to proceed farther. Actually it soon came back to position 14 by a backward movement and made a rotation; it then went forward and came down to the opposite side of the bottom of the dish (position 16). It again changed direction, and crept back towards the hydroid (e) which it previously arrived at. This time the Autolytus fed upon this colony, beginning with the hydranth of the subterminal branch (XVII) and its fellow of the opposite side (XVIII). It repeated the characteristic pumping action on a third (XIX) and fourth hydranth (XX). The well-fed animal came down to the base of the hydroid stem (position 21), then climbed the stem up to the summit and left the hydroid. On reaching colony a the Autolytus applied its proboscis twice to hydranths, and once (XXIII) was observed to feed for a short while, but soon gave up. Then the animal completely abandoned the hydroids. It proceeded forwards in a hurry to the edge of the bottom and, without stopping there for any time, continued upwards to the edge of the water (position 26): it began its habitual promenade around the glass at the water level. Next morning the animal was found to have formed a fresh tube, lying horizontally at the level where the water meets the glass instead of coming back to its old dwelling.It is quite clear that Autolytus lives upon the hydranths of Obeli a. But such a simple observation as described above still leaves doubt as to whether the worm sucks up the fluid substance from the gastric cavity of the polyp, as in the case of Procerastea, or whether it eats some part of, or the entire hydranth, as the Aeolids do.Hoping to throw light upon this problem I have made cameradrawings of all the hydranths attacked by the worm. Representative drawings are reproduced in Text-fig. 2. a represents a normal hydranth of Obelia geniculata L. with well-extended tentacles, b, c, and d are hydranths of the same hydroid but attacked by Autolytus in different degrees: in b the hypostome and most tentacles are missing, in c a still greater number of tentacles are wanting, and in d only a small basal portion of the hydranth is left. Autolytus apparently eats the tentacles and the upper portion of the hydranth as the Aeolids do, and does not only suck up the gastric fluid of the polyps as Procerastea does.An actual observation on the feeding animal showed Autolytus attacking the hydranth and eating its tentacles on one side. As will be shown later, the tentacles are drawn into the chitinous tube of the extruded pharynx (proboscis) owing to the negative pressure established there by an effective pumping action of the proventriculus, while the toothed crown (‘trépan’) was seen to be used as a saw to cut the tentacles from the hydranth. This action is performed by an upward and downward movement of the head, the protruded pharynx being pushed obliquely into the hydranth cavity and the toothed crown pressing the base of the tentacles against the inner wall of the perisarc (hydrotheca). To cut off all the tentacles from a hydranth requires about 70 to 75 seconds, but most worms abandon a hydranth in from 20 to 30 seconds, before cutting off all the tentacles, and creep up to another individual.The pumping action of the proventriculus is particularly pronounced at the outset of feeding. It is due to a strong pulsating contraction of the whole organ, the rhythm buieing at a rate of about twice per second.Weak contractions may be continued for some seconds longer, or sometimes a spontaneous pulsation is re-established; but in general the pumping action of the proventriculus does not last for the entire duration of feeding; it dies out after a short time, and a strong peristalsis of the intestine appears (this peristalsis is rarely observed in the resting animals).It is therefore quite certain that Autolytus eats 0be 1 ia, but hydranths in sound condition have always been found less liable to attack by the worm. The latter seems to search for the weaker individuals, and the same hydranth was attacked two or three times by the same or different Autolytus.While creeping up and down the hydroid stem the worms very often touch the dangerous tentacles of the hydroid, which seize the antennae and long cirri of the anterior segments. Nematocysts of the hydroid tentacles are doubtless discharged upon the enemy. The latter, however, shakes its head and quite easily frees itself without any injury.The gonophores of Obeli a are not protected by tentacles, but they are seldom attacked by the worms. In the whole course of my experiments only once was an Autolytus observed to penetrate with its extruded pharynx the cavity of a gonotheca and suck up the medusoid buds.The gonotheca of Obelia geniculata L. has the shape of a flower-vase with a small pore in the middle of the wider end. Whether or not this pore is large enough to let the pharynx in has not been studied, but the worm will hardly venture to insert its sucking apparatus through this narrow pore while plenty of the edible matter is more easily accessible.—Does this hydroid alone provide food for Autolytus or does the worm eat the other species also ? To determine whether or not the animal is monophagous, I put first several colonies of different hydroids including Obelia flabellata Hincks (this is the hydroid with which Autolytus in the dredgings is generally associated), Antennularia antennia L., Sertularia sp., &c., but not Obelia geniculata L., into a glass dish of clean sea-water in which a number of experimental animals had been kept. (The experiment was done with eighteen individuals.) The Autolytus left their tubes as usual and came down towards the colonies of Obelia flabellata Hincks, and fed upon the hydranths just as in the experiment with Obelia geniculata L. They were not, however, attracted by other hydroids. Next, in the same dish which had contained the species of hydroids named, there were put some colonies of Obelia geniculata L., and these were watched at frequent intervals to note the attitude of the experimental animals towards this hydroid when it was present in company with other species. During the first hour they fed five times upon Obelia geniculata L. and twice upon Obelia flabellata Hincks, but not at all upon other hydroids. In the next hour eight times upon the first species of Obelia and three times upon the second, but never upon the others. Lastly, when all the colonies of both species of Obelia were withdrawn from the dish the Autolytus did not come down again to the bottom: they appeared no longer to care about the presence of such hydroids as Antennularia and Sertu 1 aria.It may be mentioned here that Malaquin has recorded the Autolytus in question on the French side of the Channel living amongst Algae (Floridae) covered by Membranipora pilosa L. (loc. cit., p. 306).Although the structure and arrangement of the feeding organs in Autolytus have been dealt with in considerable detail by Malaquin (loc. cit., pp. 187-263), his description is somewhat scattered through the pages of his long monograph. It may therefore be useful to summarize it with such additions as I have been able to make out in the species under consideration. In Text-fig. 3 is a longitudinal section of an Autolytus. In this figure the principal organs of feeding and the general structure of the anterior part of the worm are shown, while the anatomical details of these organs will be found in subsequent figures.Text-fig. 3 is a median (not in the proventriculus) longitudinal section. Internal division is lacking in the dorsal portion of the body-cavity as far back as the tenth setigerous segment, i.e. the front part of the intestine; the peripharyngeal cavity ‘cavité péri-proboscidienne’ of Malaquin) is thus continuous (cp). In the ventral region, on the contrary, the body-cavity is distinctly divided by transverse septa into as many chambers (cs) as there are segments (the tentacular segment has no such cavity). The peripharyngeal cavity contains the principal organs of feeding, which consists from the anterior of (1) the mouth opening to the exterior on the mid-ventral surface of the head; (2) the pharynx (tr), a long and sinuate organ with a chitinous tube crowned by a band of small uniform teeth; (3) the proventriculus (prv), of an enormous size, with strongly muscular walls; (4) the ventriculus (v), which represents a short connecting portion between the pharyngeal part and the intestine; and (5) the intestine (in). Besides these there are a large number of unicellular glands which attain a considerable development and consist of two bodies, a large dorsal (gid) and a small ventral (glv), both stretching from the anterior end of the pharynx to the ventriculus. In Autolytus Edwarsi St. Joseph, as has been described, the glands are not incorporated into the tissue of the pharynx except in the short anterior part (tr) of the latter (‘région antérieure’ of the French author), which is extruded through the mouth when feeding is going on.With Malaquin the sinuate pharynx of the Syllids may be divided into three parts. In the present species the ‘région antérieure’ alone has the glandular sheath, while the other two regions are without it. So that the pharynx in this case consists of two parts: anterior region or proboscis, with glandular sheath, and posterior region, without it. The first part topographically represents the 1 région antérieure’, but structurally corresponds both to the ‘régions antérieure et moyenne’ of the other Syllids the second part topographically to the ‘régions moyenne et postérieure’ but structurally to the ‘région postérieure’. These differences are, however, due to the different state of development of the pharyngeal glands, and the principal structures of the pharynx remain the same both in the different species of the Syllids, as well as in the different regions of the organ in the one and same species. It consists of an epithelium with a thick chitinous investment, forming the internal tube (Text-fig. 4, ch), a muscular coat with internally circular and externally longitudinal fibres (Text-fig. 4, me et ml), and a glandular sheath in the anterior region (dt) or a very thin peritoneal membrane only in the middle and posterior regions (p).The chitin (ch) is almost uniformally thick (7μ) throughout the entire length of the tube, which has an internal diameter of 25-30/x. At the anterior end of the pharynx the tube widens and the chitin thickens, and thus are formed twenty-four small teeth regularly arranged in a row, the ‘trépan’. At the posterior end, where the pharynx meets the proventriculus, the tube widens also; but the chitin does not thicken here. There is a peculiar transverse depression at the junction of the tube of the pharynx and the proventricular lumen, and after this point the chitin diminishes suddenly to a thickness of less than 2 μ.The epithelium (ep) provides no particular interest in the present investigation.The muscular coat (m) is not conspicuous in the pharynx, its thickness not exceeding 2μ in the combined measurement of the outer longitudinal and inner circular fibres.As above stated, the anterior region of the pharynx or proboscis has a glandular sheath. This consists of a pair of pharyngeal glands, one of which discharges the secretion at the front end of the proboscis (dt2), while the other pours its contents into the buccal cavity at the base of the pharyngeal sheath (dt2). There seems, however, no difference between the two glands in the nature of their secretions.It must be mentioned that in Autolytus, as in other Sy Hid s with a sinuate pharynx, the anterior end of this organ when retracted lies far behind the opening of the mouth, and a wide space (buccal cavity) is formed by the invagination of the body-walls around the anterior part of the alimental tract.The proventriculus is an exceedingly conspicuous and very characteristic structure to which reference is made by all previous authors. It is an organ of the cylindrical shape more than 300μ. long. It measures about 120μ in thickness and is strongly muscular. The principal fibres are radially stretched from the centre to the periphery, and this arrangement of the muscle remains the same in every section of any direction, if the plane of the section passes through the centre of the organ. They are visible in the living state with a moderate magnification, even through the body-walls, as small spots arranged in annular bands transverse to the axis of the organ.The epithelium (ep) of the proventriculus (about 8 μ) is a little thicker than that of the pharynx, while the chitin is incomparably thin. At both ends, where the proventriculus joins the pharynx as well as where the organ is connected with the ventriculus, a remarkable histological differentiation has occurred in the cellular substance of the epithelium. Malaquin has already noticed (in Autolytus longeferiens St. Joseph) the peculiar striations in the epithelium near the anterior end of the proventriculus. ‘Dans la région antérieure de l’organe, l’épithélium prend un autre aspect, il devient en quelque sorte fibrillaire; les cellules en sont très allongées, avec noyau médian (Pl. v, fig. 7, Ep pr). Cette structure correspond à une disposition particulière, à un épaississement de la cuticule formant en avant du proventricule un aneau chitineux’ which is visible in the living state as a ‘coupe horizontale’ (loc. cit., p. 214). In a more recent publication W. A. Haswell (1921, p. 329) has also stated that the epithelium and cuticle ‘both become specially modified towards the anterior end of the organ in connexion with the valvular apparatus’ to be described later. Unfortunately both the French and English authors have overlooked the similar modification in the epithelium towards the posterior end of the same organ (see Text-fig. 7). Moreover, the idea of the muscular action of these modified cells does not seem to have occurred to them; they explain the mechanism of closing and opening in these parts, the function of which is valvular, simply by the construction and relaxation of the radial and annular fibres in the muscle proper of the proventriculus.The muscular walls are without doubt the seat of the proventricular function, and constitute the principal thickness of the organ. There are two kinds of fibres, one forming the radial columns (MR), and the other the slender semi-annular bands (MC). Each radial column is a hollow fibre (muscle-bundle or ‘Muskelsaule’ of Kblliker) with a more or less square crosssection (Text-fig. 6 A), and the large central space is occupied by an undifferentiated protoplasm (sarcoplasm in the more strict sense) with a nucleus near the outer surface. The column is not divided by a transverse septum as described in certain forms, such as Syllis, Eusyllis, &c. A large number of such unit structures are regularly arranged in annular rows from the anterior end of the proventriculus to the posterior.Each radial column apparently represents a single cell. As regards the contractile elements (the fibrils), these are strictly localized at the periphery of the protoplasm and are differentiated with haematoxylin into stainable and unstainable parts. The stainable part is always longer (12-25 μ.) than the unstainable part (8μ), and the contraction of the fibril seems due to the thickening and shortening of the first part. In the contracted state the stainable part therefore has an elongate fusiform shape with the unstainable part at both ends (see Text-fig. 6 B). According to Malaquin (loc. cit., p. 219) the fibril is composed of alternating zones of ordinary and double refracting material, as in the true striated muscles of the Arthropods and Vertebrates. There are four bands of Q (Text-fig. 6) (anisotrophic) in the fibril of Autolytus Ed war si St. Joseph. Haswell (1921, p. 331) states that the telophragms pass through the bands of J (isotropic). So far as my observations are concerned the so-called telophragm seems in this case to be represented by a series of intemodular nodules in the middle of the internodes between the contractible zones, the narrow unstainable part being thickened here a little more than usual. Whether the fibril in a bundle is really connected with the adjoining ones by a transverse septum, i. e. whether the telophragm passes through at the point under consideration, is still quite problematical. As I propose to write an account of the comparative histology of such striated muscles, a description of the 1 ino-phragmatic’ points is reserved until further studies have been made.Haswell (loc. cit., Pl. xv, figs. 1 and 2) has figured ‘some five or six’ nuclei in a single column of Syllis variegata (Grub.) and Malaquin (loc. cit., p. 218) has occasionally found a dinuclear column in Autolytus longeferiens St. Joseph. But these do not represent the usual condition. In general, on the contrary, the unit bundle of the radial fibres of the Syllids is mononuclear. In the present species of Autolytus the nucleus is placed between the third and fourth contractile zones, but more generally near the latter (n, Text-fig. 6 B).The columns of the radial muscle are separated from one another by annular (Text-fig. 6, st) and longitudinal septa (sl) of a fibrous nature with scattered nuclei. The annular septa are generally thicker than the others, and with Haswell (loc. cit., p. 332) they may be described as containing 1 another set of radiating elements’. ‘These elements, which for the sake of distinction may be called the accessory or non-striated radial fibres, like the striated, run from the outer fibrous membrane to the inner.’ They are placed at regular intervals between the columns of the striated fibres, and their chief function is to provide points d’appui for the annular fibres.The annular muscles (Text-fig. 5, MG) are non-striated. They are more or less compressed in the antero-posterior direction, running for the most part transversely between two adjoining of the radial column, and at the raphes (Ru and Rl) they seem to be continued straight across the middle line to the opposite side. From the raphes the fibres run in a semi-circularly radial way, and seem to be inserted in the outer membrane near the first (Q1) and the third quarter (Q3) of the proventricular circumference. According to Haswell (loc. cit., p. 332) these insertions occur between the radial columns, around the correspending accessory fibres mentioned above. Both Malaquin and Haswell are of the opinion that the annular fibres are constrictors by means of which the lumen of the proventriculus, dilated by the action of the radial muscles, is constricted.It will be seen, however, from the above description and from Text-fig. 5 that the so-called annular fibres (MC) in the present case are so arranged that their function seems to be rather co-operative with the radial fibres (MR) than antagonistic to them. In my opinion the constriction—it may be better to say the narrowness of the lumen—is rather the normal condition in the resting stages of the proventriculus, while dilation only requires a strong contraction of the muscles. The diaphragmatic semi-annular fibres seem to bring about some small adjustment of the internal condition of the dilated proventriculus, while the systole of this organ would follow as the natural consequence of the elasticity of the fibres.I have described the columns of radial muscle as being radially stretched from the centre to the periphery, and that this arrangement of the columns remains the same in every section, whatever the direction of the plane of any section passing through the centre of the organ. But the arrangement shows a little modification in those columns found near the anterior end, where the pharynx is inserted into the proventriculus and the chitin has a transverse groove. At this point the columns, departing from their arrangement in the regular annular zone, run more or less obliquely inwards and forwards or inwards and backwards. The meaning of such an oblique arrangement of the columns will not need further consideration; it can readily be understood when we consider the valvular action of the anterior end of the proventriculus. What is perhaps a similar modification is also found in the radial columns near the posterior end of the same organ. In the Autolytus under consideration two sets of fibres (one diagonal, Text-fig. 7, m1 and the other circular (m2)) are developed around the posterior orifice in addition to the radial columns, and the valvular structure is here more highly specialized than at the anterior end.This is a small intermediate chamber between the proventri cuius and the intestine. It is greatly reduced in A u t o 1 y t u s. The posterior end of the ventriculus represents the posterior limit of the stomodeal invagination in the embryonic development, and after the differentiation of the larval pharynx this part becomes a small muscular organ with a narrow lumen. The epithelium (about 10 μ.) is somewhat thicker than that of the proventriculus, but its chitinous investment is thinner. A fibrous metamorphosis has taken place in the epithelium, particularly on its outer side; but the original structure— the cells—is still distinctly visible. The cells are neither glandular nor syncytial as described in other Syllids.There are neither coecae nor post-ventricular parts in this case, the chamber of the ventriculus itself opening directly into the intestine. There is, however, a distinct separation between these two organs, especially in the morphology of their epithelia (see Text-fig. 7).The outer wall of the ventriculus is strongly muscular; the fibres (MV) arise from the posterior part of the proventriculus. They are especially thickened in the ventricular part, but their thickness very soon diminishes posteriorly over the intestinal walls. The anterior part of the intestine, at least, thus has a muscular coat, however thin it may be.In connexion with the anatomy of the feeding organs, we must now consider the muscles which project and retract the proboscis and move the other parts of the apparatus. Malaquin has already considered this problem, and his description of motor muscles is applicable here with but little change.‘Tous les muscles proboscidiens s’insèrent, d’une part sur la couche des fibres circulaires de la trompe et d’autre part sur la couche des muscles circulaires des téguments sur une ligne latérale. Ils se divisent naturellement, en muscles protracteurs, chargés de projecter la trompe hors de la bouche et en muscles rétracteurs, chargés de la ramener dans sa situation primitive à l’intérieur du corps. Certains muscles grâce à leur disposition, peuvent jouer à la fois le rôle de protracteurs et de rétracteurs. Il va sans dire que le premier acte étant brusque, rapide, nécessite une musculature plus puissante; tandis que la rétraction de la trompe se faisant plus lentement et nécessitant un effort beaucoup moins considerable que la sortie, s’opère avec une musculature beaucoup moins compliquée’ (p. 242).‘La musculature’ in the sinuate pharynx ‘est surtout condensée vers la première région de la trompe pharyngienne et vers le proventricule (see my figures, Text-fig. 8, which have been drawn from a series of obliquely transverse sections of an Autolytus). La 2e et la 3e region de la trompe pharyngienne (corresponding to the part of the pharynx without the glandular sheath) sont complètement dépourvues de muscles protracteurs et rétracteurs. Cela se conçoit facilement, car ces fibres ne pourraient que gêner l’extension des sinuosités de la trompe dans la projection’ (p. 244). Malaquin shows several weak muscles at the posterior end of the pharyngeal sheath (‘gaine pharyngienne’) where the sheath (‘gaine’) is inserted on the proboscis (‘trompe’). (‘Les unes, à direction antérieure insèrent sur les parois latérales du cor
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