Feeding Organs and Feeding Habits ofAutolytus Edwarsi St. Joseph.

(Studies on the Syllidae, I)

By

Y6 K. Okada, Naba, Hyogo-Ken (Japan).From the Marine Biological Laboratory, Plymouth.

With 10 Text-figures.

1. INTRODUCTION.

IN connexion with experimental work, especially when ananimal is required to be kept alive for a considerable time, itbecomes highly important to find out exactly .what its food isand how it eats the food. The present work is the outcome ofa suggestion made by Dr. E. J. Allen during my residence atPlymouth from June 1927.

A. Malaquin (1893, p. 257) writes in his comprehensive work' sur les Syllidiens ', that ' les aliments arrivent rapidement,grace aux movements rapides du proventricule, dans l'intestinanterieur. Ces aliments sont de la vase fine, des petits animaux,des invidus appartenant aux colonies sur lesquelles les Syllidiensvivent: Bryozoaires (Bugula, Vesicular ia , Membrani-pora, &c), Hydraires (Ser tular ia , Hydra lman ia , &c.)'.However, he does not indicate what species of Bryozoa orHydroides Syllids eat.

Syllids at Woods Hole are described as living in a transparentcase attached to Hydroids : Auto ly tus cornutusA. Agas-s.iz associating with Eudendr ium and Penar ia , Auto-lytus var ians Verrill occurring in abundance on the stemsof Pa rypha , and Autolytus o rna tus Verrill among thecolonies of Eudendr ium and Parypha (P. 0. Mensch,1900, p. 269). But no account has been given of the feedingof these worms. So far as I am aware it is E. J. Allen (1921,p. 132) who has first described it clearly in Proceras teaHal lenziana Malaquin.

220 YO K. OKADA

Procerastea is always associated with Syncoryne : it pene-trates with its extruded proboscis the body-walls of the hydroid,just at the base of the hydranth, and pumps out the fluid orsemi-fluid substance from the gastral cavity. The proventri-culus acts like a pump. According to Allen the rhythm of thismovement is at a rate of 150 to 200 per minute.

A u t o l y t u s E d w a r s i St. Joseph, upon which my obser-vations and experiments have been carried out, is common atPlymouth. Here two forms exist, one of which lives in largenumbers amongst colonies of the hydroid O b e l i a g e n i -c u l a t a L., which occurs abundantly on L a m i n a r i a . Thesecond form, found in dredgings from the outer ground ofPlymouth Sound, is relatively longer and more slender in build(Allen, 1927, p. 874). This form seems to be associated withanother species of O b e l i a (Obe l i a f l a b e l l a t a Hinck).

Before going farther I wish to take this opportunity of express-ing 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.

2. HABITS.

The specimens of A u t o l y t u s supplied me seemed to havebeen living inside a membranous tube, which they had builton L a m i n a r i a covered by the colonies of O b e l i a g e n i -c u l a t a L. When the L a m i n a r i a with the hydroid wasplaced in a dish of sea-water the A u t o l y t u s left their tubes,and in the course of a few hours crowded at the edge of thewater. The worms show distinctly a photo-positive taxis notonly to sunlight but also to electric light.

In a glass dish of clean sea-water A u t o l y t u s can live forsome days without food, and the majority of them form a tubewhich generally lies horizontally where the water meets theglass, but other tubes are found at the bottom. A few animalswander about the vessel without forming tubes, and still otherscreep above the level of the water when they dry up and perish.

The tube is a little longer than the actual length of the wormand is open at both ends. It is transparent and, as has been

FEEDING ORGANS AND HABITS OF AUTOLYTUS EDWARSI 221

described for Procerastea, sufficiently elastic for the dwellerto turn round on itself and travel both up and down the tube.It appears to be woven by the worm itself, with very fine fibrilsfrom a secretion of certain glands in the body-wall.

At Plymouth at least Autolytus is always associated withObelia, and since Bryozoa and Hydroids are known to beeaten by Syllids, it was probable that the present form livesupon Obelia. This could be most easily tested by giving thehydroid to the hungry worms. I have found that keeping themin a vessel of clean sea-water for two or three days is sufficientto make the worms hungry. With this preparation, when coloniesof Obelia were put into the dish, the Autolytus left theirtubes almost at once or in the course of a few hours. They firstcrept along the edge of the water but came down almost directlytowards the hydroid. After a short while the animals were seento creep along the stem of the Obelia and to keep on applyingthe protruded proboscis to the opening of the hydrotheca.Prom time to time they stopped at the same spot, and thepumping action, which Allen and Sexton had seen in Pro-cerastea, was clearly observed in the muscular proventriculus.The movement was followed by slow but strong and more orless regularly periodical contractions of the intestine, and astream of fluid flowed back through the proventricular lumeninto the intestine ; the animals were evidently feeding. Theysoon, however, withdrew the protruded pharynx and creptforwards and backwards to apply it to another hydranth. Butsometimes they repeated the pumping action upon the samehydranth.

Before entering into the main problem, i.e. the feedingmechanism, I give here with the aid of a diagram (Text-fig. 1)an illustration of the behaviour of a hungry worm when coloniesof Obelia were put into the glass dish which contained it.

In this case the experimental animal had built its tube in themiddle of the bottom (position 1). As soon as the hydroids wereput into the dish the animal left the tube and crept almoststraight forwards, until near the edge of the bottom (position 2).Here it turned its head to the right side and, changing direc-

NO. 286 Q

222 YO K. OKADA

tion, crept back to the centre. Passing by one hydroid (c) itwas 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 nexthydroid (e), but making two complete rotations (at the posi-tions 8 and 9) at the upper extremity of this hydroid, it pro-ceeded forwards without touching any one of the hydranths.Arriving at the edgn of the bottom (position 11), the animalseemed to hesitate to proceed farther. Actually it soon cameback to position 14 by a backward movement and made arotation ; it then went forward and came down to the oppositeside of the bottom of the dish (position 16). It again changeddirection, and crept back towards the hydroid (e) which itpreviously arrived at. This time the Autolytus fed upon thiscolony, beginning with the hydranth of the subterminal branch(XVII) and its fellow of the opposite side (XVIII). It repeatedthe characteristic pumping action on a third (XIX) and fourthhydranth (XX). The well-fed animal came down to the baseof the hydroid stem (position 21), then climbed the stem up tothe summit and left the hydroid. On reaching colony a theAuto ly tus applied its proboscis twice to hydranths, andonce (XXIII) was observed to feed for a short while, but soongave 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 theedge of the water (position 26) : it began its habitual promenadearound the glass at the water level. • Next morning the animalwas found to have formed a fresh tube, lying horizontally atthe level where the water meets the glass instead of comingback to its old dwelling.

It is quite clear that Auto ly tus lives upon the hydranthsof 0 b e 1 i a. But such a simple observation as described abovestill leaves doubt as to whether the worm sucks up the fluidsubstance from the gastric cavity of the polyp, as in the caseof Procerastea, or whether it eats some part of, or the entirehydranth, as the Aeolids do.

Hoping to throw light upon this problem I have made camera

TEXT-FIG. 1.

Behaviour of a hungry Autolytus when pieces of Obelia-colonies were put inthe glass dish. The different positions of the worm in the course of the observa-tion are indicated by figs. 1-26, the numbers and positions of its feeding beingreplaced by Roman figures (iv-xx). Small arrows indicate the direction, and thedotted line (in some places replaced by a full line) the course which the wormhas followed. The outline of the dish (with a diameter of 12-5 cm.) is shownby a circle in thick line, that of the bottom 6-5 cm.) by a light line, and theedge of the water by a circle in broken line. Observation was continued forabout half an hour.

LETTERING COMMON TO ALL TEXT-FIGURES EXCEPT TEXT-FIG. 6.a, anterior; ch, chitin; co, buccal cavity; cp, peripharyngeal cavity; cs, seg-mental cavity ; dt, pair of glands opening into proboscis; dv, dorsal vein; e,eye; ep, epithelium; g, ganglion ; gc, cephalic ganglion; gl, gland (I, ventral;u, dorsal); go, infra-oesophageal ganglion ; I, lower ; in, intestine ; m(M),muscle; MC, circular fibres of proventriculus ; ml, longitudinal fibres ; mm,motor muscle (a, anterior ; p, posterior); nip, parapodial muscle ; MR, radialcolumns of proventriculus ; mr, radial fibres ; ins, somatic muscle {I, ventral ;u, dorsal); MV, ventricular muscle; n, nerve; o, mouth or oral position; p,peritoneal membrane; pi, cytoplasm; prv, proventriculus; Q, quarter ofcircumference ; R, raphe {I, ventral; u, dorsal) ; st, septum (I, dorsal; u,ventral); tr, pharynx ; u, upper ; v, ventriculus.

Q2

224 YO K. OKADA

drawings of all the hydranths attacked by the worm. Repre-sentative drawings are reproduced in Text-fig. 2. a representsa normal hydranth of Obelia genicula ta L. with well-extended tentacles, b, c, and d are hydranths of the samehydroid but attacked by Auto ly tus in different degrees :in b the hypostome and most tentacles are missing, in c a stillgreater number of tentacles are wanting, and in d only a smallbasal portion of the hydranth is left. Auto ly tus appar-ent ly eats the ten tac les and the upper por t ion

TEXT-FIG. 2.

Hydranth of Obelia geniculata L. (a) and some of the same attacked(6-c) by Autolytus.

of the hyd ran th as the Aeolids do, and does notonly suck up the gas t r ic fluid of the polyps asProceras tea does.

An actual observation on the feeding animal showed Auto-lytus attacking the hydranth and eating its tentacles on oneside. As will be shown later, the tentacles are drawn into thechitinous tube of the extruded pharynx (proboscis) owing tothe negative pressure established there by an effective pumpingaction of the proventriculus, while the toothed crown (' trepan ')was seen to be used as a saw to cut the tentacles from thehydranth. This action is performed by an upward and down-ward movement of the head, the protruded pharynx beingpushed obliquely into the hydranth cavity and the toothed

FEEDING ORGANS AND HABITS OF AUTOLYTUS EDWARSI 225

crown pressing the base of the tentacles against the inner wallof the perisarc (hydrotheca). To cut off all the tentacles froma hydranth requires about 70 to 75 seconds, but most wormsabandon a hydranth in from 20 to 30 seconds, before cuttingoff all the tentacles, and creep up to another individual.

The pumping action of the proventriculus is particularly pro-nounced at the outset of feeding. It is due to a strong pulsatingcontraction of the whole organ, the rhythm being at a rate ofabout twice per second.

TABLE 1. PULSATION OF PROVENTRICTJLTJS.

Duration of thebeats.

15-3 seconds17-5

810-21714

67-55

10

Number of Contrac-tions.

20251317312612151021

Rhythm perSecond.

1-31-31-61-71-81-82222-1

Weak contractions may be continued for some seconds longer,or sometimes a spontaneous pulsation is re-established ; butin general the pumping action of the proventriculus does notlast for the entire duration of feeding ; it dies out after a shorttime, and a strong peristalsis of the intestine appears (this peri-stalsis is rarely observed in the resting animals).

It is therefore quite certain that Autoly tus eats Obe 1 ia,but hydranths in sound condition have always been found lessliable to attack by the worm. The latter seems to search forthe weaker individuals, and the same hydranth was attackedtwo or three times by the same or different Au to ly tus .

While creeping up and down the hydroid stem the wormsvery often touch the dangerous tentacles of the hydroid, whichseize the antennae and long cirri of the anterior segments.Nematocysts of the hydroid tentacles are doubtless dischargedupon the enemy. The latter, however, shakes its head and quiteeasily frees itself without any injury.

The gonophores of Obeli a are not protected by tentacles,

226 YO K. OKADA

but they are seldom attacked by the worms. In the wholecourse of my experiments only once was an A u t o l y t u sobserved to penetrate with its extruded pharynx the cavityof a gonotheca and suck up the medusoid buds.

The gonotheca of Obe l i a g e n i c u l a t a L. has the shapeof a flower-vase with a small pore in the middle of the widerend. Whether or not this pore is large enough to let the pharynxin has not been studied, but the worm will hardly venture toinsert its sucking apparatus through this narrow pore whileplenty of the edible matter is more easily accessible.

A u t o l y t u s E d w a r s i S t . Jo seph l ives u p o nObe l i a g e n i c u l a t a L.—Does this hydroid alone providefood for A u t o l y t u s or does the worm eat the other speciesalso ? To determine whether or not the animal is monophagous,I put first several colonies of different hydroids includingObel ia f l a b e l l a t a Hincks (this is the hydroid with whichx \ u t o l y t u s in the dredgings is generally associated), An-t e n n u l a r i a a n t e n n i a L., S e r t u l a r i a sp., &c, but notObe l i a g e n i c u l a t a L., into a glass dish of clean sea-waterin which a number of experimental animals had been kept.(The experiment was done with eighteen individuals.) TheA u t o l y t u s left their tubes as usual and came down towardsthe colonies of Obe l i a f l a b e l l a t a Hincks, and fed uponthe hydranths just as in the experiment with Obe l ia gen i -c u l a t a L. They were not, however, attracted by otherhydroids. Next, in the same dish which had contained thespecies of hydroids named, there were put some colonies ofObel ia g e n i c u l a t a L., and these were watched at frequentintervals to note the attitude of the experimental animalstowards this hydroid when it was present in company withother species. During the first hour they fed five times uponObe l i a g e n i c u l a t a L. and twice upon Obe l ia f l abe l -l a t a Hincks, but not at all upon other hydroids. In the nexthour eight times upon the first species of Obe l ia and threetimes upon the second, but never upon the others. Lastly, whenall the colonies of both species of Obe l i a were withdrawnfrom the dish the A u t o l y t u s did not come down again to

FEEDING ORGANS AND HABITS OF AUTOLYTUS EDWARSI 227

the bottom : they appeared no longer to care about the presenceof such hydroids as A n t e n n u l a r i a and S e r t u l a r i a .

It rnay be mentioned here that Malaquin has recorded theA u t o l y t u s in question on the French side of the Channelliving amongst Algae (Moridae) covered by M e m b r a n i p o r ap i l o s a L. (loc. cit., p. 306).

3. FEEDING ORGANS (Text-fig. 3).

Although the structure and arrangement of the feedingorgans in A u t o l y t u s have been dealt with in considerabledetail by Malaquin (loc. cit., pp. 187-263), his description issomewhat scattered through the pages of his long monograph.

csXmmp

TEXT-FIG. 3.

glu glL

It maj' therefore be useful to summarize it with such additionsas I have been able to make out in the species under considera-tion. In Text-fig. 3 is a longitudinal section of an A u t o -l y t u s . In this figure the principal organs of feeding and thegeneral structure of the anterior part of the worm are shown,while the anatomical details of these organs will be found insubsequent figures.

Text-fig. 3 is a median (not in the proventriculus) longitu-dinal section. Internal division is lacking in the dorsal portionof the body-cavity as far back as the tenth setigerous segment,i.e. the front part of the intestine ; the peripharyngeal cavity' cavite peri-proboscidienne ' of Malaquin) is thus continuous

228 YO K. OKADA

(cp). In the ventral region, on the contrary, the body-cavityis distinctly divided by transverse septa into as many cham-bers (cs) as there are segments (the tentacular segment has nosuch cavity). The peripharyngeal cavity contains the principalorgans of feeding, which consists from the anterior of (1) them o u t h opening to the exterior on the mid-ventral surfaceof the head ; (2) the p h a r y n x (tr), a long and sinuate organwith a chitinous tube crowned by a band of small uniformteeth ; (3) the p r o v e n t r i c u l u s (prv), of an enormous size,with strongly muscular walls; (4) the v e n t r i c u l u s (v),which represents a short connecting portion between thepharyngeal part and the intestine ; and (5) the i n t e s t i n e (in).Besides these there are a large number of unicellular glandswhich attain a considerable development and consist of twobodies, a large dorsal (gld) and a small ventral (glv), bothstretching from the anterior end of the pharynx to the ven-triculus. In A u t o l y t u s E d w a r s i St. Joseph, as has beendescribed, the glands are not incorporated into the tissue ofthe pharynx except in the short anterior part (tr) of the latter(' region anterieure ' of the French author), which is extrudedthrough the mouth when feeding is going on.

A. P h a r y n x (Text-fig. 4).

With Malaquin the sinuate pharynx of the Syllids may bedivided into three parts. In the present species the ' regionanterieure ' alone has the glandular sheath, while the other tworegions are without it. So that the pharynx in this case consistsof two parts : anterior region or proboscis, with glandularsheath, and posterior region, without it. The first part topo-graphically represents the ' region anterieure ', but structurallycorresponds both to the ' regions anterieure et moyenne ' of theother Syllids ;" the second part topographically to the ' regionsmoyenne et posterieure ' but structurally to the ' region pos-terieure '. These differences are, however, due to the differentstate of development of the pharyngeal glands, and the prin-cipal structures of the pharynx remain the same both in thedifferent species of the Syllids, as well as in the different regions

FEEDING ORGANS AND HABITS OF AUTOLYTUS EDWAHSI 229

of the organ in the one and same species. It consists of anepithelium with a thick chitinous investment, forming theinternal tube (Text-fig. 4, ch), a muscular coat with internallycircular and externally longitudinal fibres (Text-fig. 4, me et ml),and a glandular sheath in the anterior region (dt) or a verythin peritoneal membrane only in the middle and posteriorregions (p).

The chitin (ch) is almost uniformally thick (7/x) throughout

TEXT-FIG. 4.

Segmental cavity

Front part of the feeding apparatus (first region of the pharynx(proboscis) and its sheath).

the entire length of the tube, which has an internal diameterof 25-30/x. At the anterior end of the pharynx the tube widensand the chitin thickens, and thus are formed twenty-four smallteeth regularly arranged in a row, the ' trepan '. At theposterior end, where the pharynx meets the proventriculus, thetube widens also ; but the chitin does not thicken here. Thereis a peculiar transverse depression at the junction of the tubeof the pharynx and the proventricular lumen, and after thispoint the chitin diminishes suddenly to a thickness of lessthan 2/x.

230 YO K. OKADA

The epithelium (ep) provides no particular interest in thepresent investigation.

The muscular coat (TO) is not conspicuous in the pharynx, itsthickness not exceeding 2/x in the combined measurement ofthe outer longitudinal and inner circular fibres.

As above stated, the anterior region of the pharynx or pro-boscis has a glandular sheath. This consists of a pair of pharyn-geal glands, one of which discharges the secretion at the frontend of the proboscis (dty), while the other pours its contents intothe buccal cavity at the base of the pharyngeal sheath (dt2).There seems, however, no difference between the two glandsin the nature of their secretions.

It must be mentioned that in A u t o 1 y t u s, as in otherBy Hid s with a simiate pharynx, the anterior end of this organwhen retracted lies far behind the opening of the mouth, anda wide space (buccal cavity) is formed by the invagination ofthe body-walls around the anterior part of the alimental tract.

B. P r o v e n t r i c u l u s (Text-figs. 5 and 7).

The proventriculus is an exceedingly conspicuous and verycharacteristic structure to which reference is made by allprevious authors. It is an organ of the cylindrical shape morethan 300/x long. It measures about 120/x in thickness and isstrongly muscular. The principal fibres are radially stretchedfrom the centre to the periphery, and this arrangement of themuscle remains the same in every section of any direction, if theplane of the section passes through the centre of the organ.They are visible in the living state with a moderate magnifica-tion, even through the body-walls, as small spots arranged inannular bands transverse to the axis of the organ.

The epithelium (ep) of the proventriculus (about 8/.i) is alittle thicker than that of the pharynx, while the chitin isincomparably thin. At both ends, where the proventriculusjoins the pharynx as well as where the organ is connected withthe ventriculus, a remarkable histological differentiation hasoccurred in the cellular substance of the epithelium. Malaquinhas already noticed (in A u t o l y t u s l o n g e f e r i e n s St.

FEEDING ORGANS AND HABITS OF AUTOLYTUS EDWARSI 231

Joseph) the peculiar striations in the epithelium near the an-terior end of the proventriculus. ' Dans la region anterieurede l'organe, l'epithelium prend un autre aspect, il devient enquelque sorte fibrillaire ; les cellules en sont tres allongees, avecnoyau median (PI. v, fig. 7, Ep y?r). Cette structure corresponda une disposition particuliere, a un epaississement de la cuticuleformant en avant du proventricule un aneau chitineux' which

gfc Q>

Proventriculus in transverse section, x 360.

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 ' bothbecome specially modified towards the anterior end of the organin connexion with the valvular apparatus ' to be described later.Unfortunately both the French and English authors have over-looked the similar modification in the epithelium towards theposterior end of the same organ (see Text-fig. 7). Moreover,the idea of the muscular action of these modified cells does not

232 YO K. OKADA

seem to have occurred to them ; they explain the mechanismof closing and opening in these parts, the function of which isvalvular, simply by the construction and relaxation of theradial and annular fibres in the muscle proper of the pro-ventriculus.

The muscular Avails are without doubt the seat of the pro-ventricular function, and constitute the principal thickness ofthe organ. There are two kinds of fibres, one forming the radialcolumns (MR), and the other the slender semi-annular bands(MC). Each radial column is a hollow fibre (muscle-bundleor ' Muskelsaule ' of Kolliker) with a more or less square cross-section (Text-fig. 6 A), and the large central space is occupiedby an undifferentiated protoplasm (sarcoplasm in the morestrict sense) with a nucleus near the outer surface. The columnis not divided by a transverse septum as described in certainforms, such as S y l l i s , E u s y l l i s , &c. A large number ofsuch unit structures are regularly arranged in annular rowsfrom the anterior end of the proventriculus to the posterior.

Each radial column apparently represents a single cell. Asregards the contractile elements (the fibrils), these are strictlylocalized at the periphery of the protoplasm and are differen-tiated with haematoxylin into stainable and unstainable parts.The stainable part is always longer (12-25/x) than the unstain-able part (8/x), and the contraction of the fibril seems due to thethickening and shortening of the first part. In the contractedstate the stainable part therefore has an elongate fusiformshape with the unstainable part at both ends (see Text-fig. 6 B).According to Malaquin (loc. cit., p. 219) the fibril is composedof alternating zones of ordinary and double refracting material,as in the true striated muscles of the Arthropods and Verte-brates. There are four bands of Q (Text-fig. 6) (anisotrophic)in the fibril of A u t o l y t u s E d w a r si St. Joseph. Haswell(1921, p. 831) states that the telophragms pass through thebands of J (isotropic). So far as my observations are concernedthe so-called telophragm seems in this case to be representedby a series of internodular nodules in the middle of the inter-nodes between the contractible zones, the narrow unstainable

TEXT-FIG. 6.

Some radial columns of the proventricular wall, (a) In transversesection and (6) in longitudinal cut. f, muscle-fibres ; i, internodularnodule ; J, unstainable part of fibre ; n, nucleus ; pi, plasm ;Q, stainable part of fibre ; si, longitudinal septum ; st, transverseseptum, x 550.

234 YO K. OKADA

part being thickened here a little more than usual. Whether thefibril in a bundle is really connected with the adjoining ones bya transverse septum, i. e. whether the telophragm passes throughat the point under consideration, is still quite problematical.As I propose to write an account of the comparative histologyof such striated muscles, a description of the ' ino-phragmatic 'points is reserved until further studies have been made.

Haswell (loc. cit., PL xv, figs. 1 and 2) has figured ' some fiveor six ' nuclei in a single column of S y l l i s v a r i e g a t a(Grub.) and Malaquin (loc. cit., p. 218) has occasionally founda dinuclear column in A u t o l y t u s l o n g e f e r i e n s St. Joseph.But these do not represent the usual condition. In general,on the contrary, the unit bundle of the radial fibres of theSyllids is mononuclear. In the present species of A u t o l y t u sthe nucleus is placed between the third and fourth contractilezones, but more generally near the latter (n, Text-fig. 6 B).

The columns of the radial muscle are separated from oneanother by annular (Text-fig. 6, st) and longitudinal septa (si)of a fibrous nature with scattered nuclei. The annular septaare generally thicker than the others, and with Haswell (loc.cit., p. 332) they may be described as containing ' another setof radiating elements '. ' These elements, which for the sakeof distinction may be called the accessory or non-striated radialfibres, like the striated, run from the outer fibrous membraneto the inner.' They are placed at regular intervals between thecolumns of the striated fibres, and their chief function is toprovide p o i n t s d ' a p p u i for the annular fibres.

The annular muscles (Text-fig. 5, MC) are non-striated. Theyare more or less compressed in the antero-posterior direction,running for the most part transversely between two adjoiningof the radial column, and at the raphes (Ru and Rl) they seemto be continued straight across the middle line to the oppositeside. From the raphes the fibres run in a semi-circularly radialway, and seem to be inserted in the outer membrane near thefirst (Ql) and the third quarter (Q3) of the proventricularcircumference. According to Haswell (loc. cit., p. 332) theseinsertions occur between the radial columns, around the corre-

FEEDING ORGANS AND HABITS OF AUTOLYTUS EDWARSI 235

sponding accessory fibres mentioned above. Both Malaquinand Haswell are of the opinion that the annular fibres are con-strictors 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 fromText-fig. 5 that the so-called annular fibres (MG) in the presentcase are so arranged that their function seems to be ratherco-operative with the radial fibres (ME) than antagonistic tothem. In my opinion the constriction—it may be better tosay the narrowness of the lumen—is rather the normal conditionin the resting stages of the proventriculus, while dilation onlyrequires a strong contraction of the rnuscles. The diaphrag-matic semi-annular fibres seem to bring about some smalladjustment of the internal condition of the dilated proventri-culus, while the systole of this organ would follow as the naturalconsequence of the elasticity of the fibres.

I have described the columns of radial muscle as being radiallystretched from the centre to the periphery, and that this arrange-ment of the columns remains the same in every section, what-ever the direction of the plane of any section passing throughthe centre of the organ. But the arrangement shows a littlemodification in those columns found near the anterior end,where the pharynx is inserted into the proventriculus and thechitin 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 andbackwards. The meaning of such an oblique arrangement ofthe columns will not need further consideration ; it can readilybe understood when we consider the valvular action of theanterior end of the proventriculus. What is perhaps a similarmodification is also found in the radial columns near theposterior end of the same organ. In the A u t o l y t u s underconsideration two sets of fibres (one diagonal, Text-fig. 7, mv

and the other circular (m2)) are developed around the posteriororifice in addition to the radial columns, and the valvularstructure is here more highly specialized than at the anteriorend.

236 YO K. OKADA

C. Ventr iculus (Text-fig. 7).This is a small intermediate chamber between the proventri

culus and the intestine. It is greatly reduced in Au to ly tus .The posterior end of the ventriculus represents the posterior

TEXT-FIG. 7.

Stu

Posterior part of the feeding apparatus (posterior half of the proventrioulus,the ventriculus, and the anterior end of the intestine), x 320.

limit of the stomodeal imagination in the embryonic develop-ment, and after the differentiation of the larval pharynx thispart becomes a small muscular organ with a narrow lumen.The epithelium (about 10 .̂) is somewhat thicker than that ofthe proventriculus, but its chitinous investment is thinner.A fibrous metamorphosis has taken place in the epithelium,

FEEDING ORGANS AND HABITS OF AUTOLYTUS EDWARSI 237

particularly on its outer side ; but the original structure—the cells—is still distinctly visible. The cells are neitherglandular nor syncytial as described in other Syllids.

There are neither coecae nor post-ventricular parts in thiscase, the chamber of the ventriculus itself opening directly intothe intestine. There is, however, a distinct separation betweenthese two organs, especially in the morphology of their epithelia(see Text-fig. 7).

The outer wall of the ventriculus is strongly muscular ; thefibres (MV) arise from the posterior part of the proventriculus.They are especially thickened in the ventricular part, but theirthickness very soon diminishes posteriorly over the intestinalwalls. The anterior part of the intestine, at least, thus has amuscular coat, however thin it may be.

4. MOTOR MUSCLES (Text-fig. 8).

In connexion with the anatomy of the feeding organs, wemust now consider the muscles which project and retract theproboscis and move the other parts of the apparatus. Malaquinhas already considered this problem, and his description ofmotor muscles is applicable here with but little change.

Tous les muscles proboscidiens s'inserent, d'une part sur lacouche des fibres circulaires de la trompe et d'autre part sur lacouche des muscles circulaires des teguments sur une lignelaterale. Us se divisent naturellement, en muscles pro-t r a c t e u r s , charges de projecter la trompe hors de la boucheet en muscles r e t r a c t e u r s , charges de la ramener danssa situation primitive a l'interieur du corps. Certains musclesgrace a leur disposition, peuvent jouer a la fois le role de pro-tracteurs et de retracteurs. II va sans dire que le premier acteetant brusque, rapide, necessite une musculature plus puissante ;tandis que la retraction de la trompe se faisant plus lentementet necessitant un effort beaucoup moins considerable que lasortie, s'opere avec une musculature beaucoup moins com-pliquee ' (p. 242).

' La musculature ' in the sinuate pharynx ' est surtout con-densee vers la premiere region de la trompe pharyngienne et

NO. 286 R

238 YO K. OKADA

vers le proventricule (see my figures, Text-fig. 8, which havebeen drawn from a series of obliquely transverse sections of anA u t o 1 y t u s). La 2e et la 3° region de la trompe pharyngienne(corresponding to the part of the pharynx without the glandularsheath) sont completement depourvues de muscles protracteurset retracteurs. Cela se concoit facilement, car ces fibres ne pour-raient que gener l'extension des sinuosites de la trompe dans laprojection ' (p. 244). Malaquin shows several weak musclesat the posterior end of the pharyngeal sheath (' gaine pharyn-gienne ') where the sheath (' gaine ') is inserted on the proboscis(' trompe '). (' Les unes, a direction anterieure inserent sur lesparois laterales du corps, les autres beaucoup plus longues vonts'inserer dans le voisinage de la tete. Enfin d'autres a directionposterieure ont un role retracteur.') Besides these I have foundfibres (mm) of a similar nature near the anterior end of thepharyngeal sheath where the sheath is separate from the body-walls. These muscles have been drawn by Malaquin inM y r i a n i d a P inn ige ra Montagu (see his fig. 3 in PI. 4) andalso A u t o l y t u s longefe r i ensS t . Joseph (see also his fig. 4in PI. 4).

As has been demonstrated in many Syllids, there is a pair ofstrong muscle-bundles on each side of the sinuate pharynx,the function of which may be considered as protractor. These(mma) start at the anterior corner of the proventriculus and areinserted on either side of the body-wall near the first segmentalseptum. I was unable to find in the present species of A u t o -l y t u s a posterior pair of similar muscles, but a bundle offibres (mmp), as strong as those of the anterior pair, was foundstretching between the dorsal wall of the intestine and thepharyngeal glands, which seems to be in some way connectedto the dorsal wall of the proventriculus.

Muscle-fibres are also differentiated in the tissue of thesepta : these may be to some extent taken into account in con-nexion with the motor muscles of the feeding apparatus, whilethe muscles of the body walls (ms) and those connected to themovement of the cirri and parapodia (mp) need not be speciallydescribed here.

TEXT-FIG. 8.

Four sections from the anterior part of an Autolytus cut in anobliquely transverse direction, the upper and lower belonging tothree different segments, x 120.

R2

240 Y6 K. OKADA

V. MECHANISM OF FEEDING.

That the proventriculus of the Syllids functions as a pumphas been recognized by St. Joseph (1886, p. 152). Malaquin(1893, p. 247) has mentioned it also in his work. However,' their descriptions do not suggest', states Allen (1921, p. 134),' that they have realized the rapidity of action or the strongcurrent which it can produce '. Allen records 150 to 200 pulsa-tions per minute in the proventriculus of P r o c e r a s t e aH a l l e n z i a n a Malaquin. I have counted about two persecond, so that there are 120 pulsations per minute in Auto-l y t u s E d w a r s i St. Joseph. Without any doubt the pump-ing action of the organ plays an important role in the suctionof nourishment through the chitinous tube of the pharynx.' Les Syllidiens, en meme temps que leurs aliments, avalenttoujours une certaine quantite d'eau ' (Malaquin, loc. cit.,p. 247).

The food of P r o c e r a s t e a H a l l e n z i a n a Malaquin,according to Allen, really consists of semi-fluid matter from thegastral cavity of a hydroid, Synco ryne eximia Allman.

The entire organization of the feeding apparatus, as will beunderstood from the description of the anatomy of the organs,suggests the system of a suction pump, the pharynx representingthe pipe, the proventriculus the pump itself with two valves,one at the anterior and one at the posterior end, and the ventri-culus the governor and regulator. But there still remains aquestion whether the suction is due to an incessant beat of theproventriculus, or whether the pumping movement of thisorgan is an initial phase of the suction, which is due to theestablished negative pressure in the anterior part of the alimentaltract, i.e. the feeding apparatus. If one observes a feedingA u t o l y t u s the pumping movement dies away from the pro-ventriculus in ten to fifteen seconds in most cases, while thesucking action is apparently continued for a longer time. Thefluid can be distinctly seen passing through the ventricularlumen into the intestine where it continues in movement. Onthe other hand a peristaltic movement, with a more or less

FEEDING ORGANS AND HABITS OF AUTOLYTUS EDWAESI 241

regular rhythm (about twice per 5 seconds) begins to appear inthe anterior part of the intestine at about the same time thatthe pulsation is disappearing from the proventriculus.

I shall try to illustrate my idea regarding this feeding mechan-ism by a series of figures (Text-fig. 9) in combination with agraph (Text-fig. 10), 'as I think it will be better understood inthis way than by a long description. Text-fig. 9 A representsan A u t o l y t u s in the resting state with the principal organsof feeding shown diagrammatically in longitudinal section. Theproboscis (trx) is retracted into the buccal cavity (eo), theposterior two-thirds of the pharynx (tr2) being folded in a loop.The proventriculus (prv) is seen as an ovoid organ (shaded)with a narrow lumen, which opens anteriorly into the chitinoustube and posteriorly into the intestine (in) by a short inter-mediate channel, the ventriculus (v). The motor muscles(mm) are shown by parallel lines, the body-walls by two lines,and the septa by a single line. An object to be shallowed isindicated by a small sphere obliquely shaded ; it is placed infront of the mouth.

When the worm is going to feed (Text-fig. 9 B) the anteriorone-third of the pharynx, i.e. the proboscis, is projected for-wards through the mouth opening (o). This action is very quickand seems to be achieved by a forward movement of the entirefeeding apparatus, including the anterior part of the intestine,due to the strong contraction of the somatic muscles, with theaid of the protractor muscles in front of the proventriculus(mma). The sinuate pharynx is straightened and is appliedto the object to be eaten. Then the radial muscles of the proven-triculus contract with the anterior valve open and the posteriorclosed. The widened lumen withdraws a certain quantity offluid from the chitinous tube and the aliment is carried with thestream of Avater into the tube.

Next (Text-fig. 9 c) the anterior valve is closed and theposterior is opened, the ventriculus being also opened. In thisstate, when the contracted muscles of the proventriculus relax,all the fluid contained in its lumen will be driven posteriorlyinto the intestine. By repeating very quickly these actions in

TEXT-FIG. 9

Diagrammatic illustration of the feeding mechanism ofAuto ly tus .

FEEDING ORGANS AND HABITS OF AUTOLYTUS EDWAHSI 2 4 3

the proventriculus—the action may be called with Allen' pump-action ' and is represented by a succession of sharpcurves in the graph—a negative pressure will be produced in thetube of the pharynx and the food gradually moves back witha current of water.

But when a continuous water-column is established in thefront part of the alimental tract the pumping action will nomore be needed. The muscular movement now ceases in theproventriculus and the anterior valve remains open, whilethe water-column is maintained and the suction continued by

TEXT-FIG. 10.

O 1 2 3 4 5 6 7 8 9 10 II 12 13 14 15 16Pulsation of proventriculus Peristalsis of Intestine

Graphic representation of the feeding mechanism in Autolytus.

the peristalsis of the intestine, the posterior valve together withventriculus now controlling the current. The mechanism ofthis second period is represented in two figures, Text-fig. 9,d and e, and the peristaltic movement of the intestine by alarge gradual curve in the graph.

Finally (Text-fig. 9,/), when the worm stops feeding it retractsthe extruded proboscis into the buccal cavity : it extends thecontracted segments, draws back the organs of feeding into theirproper positions, and the last powerful contraction in the an-terior part of the body drives all the food—the hydroid ten-tacles in this case—farther backwards towards the digestiveregions of the epithelium which is characterized by the presenceof numerous unicellular glands.

244 YO K. OKADA

Before closing the description of the present observations, itmay be added that the front portion of the intestine at the out-set of feeding swells up enormously and overlaps the posteriorpart of the proventriculus. This phenomenon is particularlyclearly seen on the dorsal side.

5. SUMMARY.

A u t o l y t u s E d w a r s i St. Joseph at Plymouth lives uponObeli a. It deprives the hydroid of the hydranths and eatsthem.

The worm cuts off the tentacles from the hydranth with thetoothed crown of the chitinous tube (the ' trepan '), and sucksthem up through the protruded pharynx by establishing inthe front part of the alirnental tract by the activity of theproventriculus a continuous water-column which is drawn backinto the intestine.

The pulsation or pumping action of the proventriculus isparticularly strong and distinctly visible at the outset of feed-ing. After a short time it dies away and the action is followedby peristalsis in the intestine.

The entire organization in the front part of the alirnentaltract, which is the feeding apparatus of the A u t o l y t u s ,suggests the system of a suction pump, the pharynx representingthe pipe, the proventriculus the pump itself with a valve ateach entrance, and the ventriculus the regulator of the water-column.

The proventricular activity is due to the strong musculardevelopment in the radial columns, which are stretched fromthe centre of the organ to the periphery. In each fibre are fourcontractile zones, three internodes, and two insertion parts.The contractile zones only are stainable with iron haematoxylin,and these may be comparable to the anisotropic bands of thestriated fibre of the Arthropods and Vertebrates. In the middleof the internode there is a thickening, the internodular-nodule :the problem whether this point can be referred to the intra-fibrillar part of the inophragm (telophragm in this case) isreserved for future discussion.

FEEDING ORGANS AND HABITS OF AUTOLYTUS EDWARSI 245

R E F E R E N C E S .

Agassiz, A. (1862).—" On alternate generation of Annelids and the embryo-logy of Autolytus cornutus ", ' Journ. Nat. Hist. Soc. Boston', vol. 7,p. 392.

Allen, E. J. (1921).—" Regeneration and Reproduction of the Syllid Pro-cerastea ", ' Phil. Trans. R. Soc. London', B, vol. 211, p. 131.

(1927).—"Fragmentation in the Genus Autolytus and in otherSyllids ", ' Journ. Mar. Biol. Assoc.', vol. xiv, p. 869.

Fauvel, P. (1923).—' Faune de France (5. Polychetes errantes)', Paris.Haswell, W. A. (1890).—"A Comparative Study of Striated Muscle",

' Quart. Journ. Micr. Sci.', vol. xxx, p. 31.(1921).—" The Proboscis of the Syllidea (I. Structure)", ibid.,

vol. lxv, p. 323.Malaquin, A. (1893).—" Recherches sur les Syllidiens ", ' Mem. Soc. Sc.

Arts, Lille ', p. 1.Mensch, P. C. (1900).—" Stolonisation in Autolytus varians ", 'Journ.

Morph.', vol. 16, p. 269.Potts, F. A. (1911).—" Methods of Reproduction in the Syllids ", ' Ergeb.

u. Fortschr. d. Zoologie', Bd. iii, Heft 1.St. Joseph, de (1886).—" Annelides Polychetes des Cotes de Dinard ",

' Ann. Sci. Nat. Zool.', 7, torn, i, p. 127.