STBUOTUBB OF EXCRKTOEY ORGANS OP AMPHIOXUS. 493

On the.Structure of the Excretory Organs ofAmphioxus.

Part I.

ByEdwin S. Ooodricli, M.A.,

Follow of Merton College, Oxford.

With Plate 27.

THE excretory organs of Amphioxus were independentlydiscovered by Weiss and Boveri in the year 1890 (1 and 13).Weiss described a series of small tubules regularly dis-tributed at the top of each secondary tongue-bar throughoutthe region of the pharynx. The tubules are situated, for themost part, in the wall separating the dorsal ccelom from theatrial cavity; they lie, therefore, between the cceloniic andthe atrial epithelium, generally separated from the latter bya network of fine blood-vessels. These kidney tubules openinto the atrium by a pore just opposite the dorsal end of thesecondary gill-bar. Weiss suspected the presence of aninternal opening, but could not find it. The physiologicalsignificance of these organs he established by means offeeding experiments with carmine and other colouringmatters.

In 1892 Boveri published a detailed and beautifully illus-trated account of the excretory organs of Amphioxus (2).In this paper such a clear and accurate description of theappearance, general structure, and distribution of thekidneys is given that little remains to be said on these

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494 EDWIN S. GOODRICH.

subjects. It will be necessary only to deal in detail herewith certain points on which we differ, and concerning whichI am able to correct Boveri's account in some importantparticulars.

The following is a brief statement of Boveri's descriptionof the excretory organs :—Each consists of a tubule ciliatedinternally, and opening into the atrium by a pore near thetop of the secondary gill-bar. In the mid-region of thepharynx, where the canal is best developed, it extendsforwards to near the origin of the primary bar in front, andbackwards to the primary bar behind, down which it runsfor some little distance. Along its course the tubule is saidto open into the dorsal coelom by means of a varying numberof small funnels; and spread over the ccelomic wall in tlieneighbourhood of each funnel are many peculiar pin-shapedcells called " fadenzellen." A long, slender process, startingfrom each of the " fadenzellen," is attached to the lip of thefunnel. To quote from Boveri: " Jede Zelle lauft namlichin einen feinen, aber deutlich doppelt contourirten Fadenaus, der mit den iibrigen Auslaufern der gleichen Zellengruppezu einem Trichter hinzieht und in der Miindung desselbeneine Strecke weit verfolgt werden kann;" and further :" Die Faden ziehen frei dnrch die Leibeshohle schragabw'arts in die Trichteroffnung hinein gegen die lateraleWand des Canalchens und heften sich mifc ihnen Enden andie Zellen des Nierenepithels an" (2).

Some years ago, being struck with the resemblance these"fadenzellen" bear to the solenocytes I had just dis-covered in the nephridia of Polychaste worms, I examined thekidneys of Amphioxus, and came to the conclusion that thesimilarity was only superficial, and that Boveri's descriptionwas essentially correct (5, Part III). This winter, however,whilst occupying the British Association table at the StazioneZoologica in Naples, I determined to re-examine theseorgans, and I am now able to definitely state that the"fadenzellen" of Amphioxus are indeed solenocytes oEtypical, though somewhat pecul ia r s t ruc tu re (7).

STRUCTURE OF EXCRETORY ORGANS OF AMPHIOXUS. 495

The methods pursued are of the most simple kind, and itis within the power of any one with living material at hand toeasily verify my results. The Amphioxus is pinned out onits back in a shallow dish of sea water. The atrium is rippedup with a needle along the mid-ventral line, and the twometaplenral folds pinned aside. The exposed pharynx isthen also ripped up with a needle, and portions of the rightor left side of the pharynx cau then be torn out with forceps

Figure of a portion of a section across the gill-bars showing theexcretory canal cut through. A. Atrium. C. Dorsal ccelom.pb. Primary gill-bar. ' bv. Blood-vessel, ae. Atrial epithelium.ce. Coelomic epithelium. /. Lumen of the excretory canal, n.Nucleus of asolenocyte. t. Tube of a solenocyte. Cam. and oilimmersion.

and placed on a slide,1 care being taken to lay the outerside uppermost. When covered and examined under themicroscope the general structure of the kidney can be quiteeasily seen; but the details which I am about to describecan, unfortunately, only be made out after prolonged studywith the highest powers (-j - oil immersion and No. 8 eyepiece,for instance).

1 Such pieces can be stained and mounted, or cut into sections.

496 EDWIN S. GOODKIOH.

Examined in this way, the " fadenzellen " are seen to con-sist of a small cell-body containing a nucleus. The cell-bodyis of somewhat irregular shape, being circular, triangular, orelongated, and. occasionally drawn out into a process, re-minding one of the outer processes present on some Poly-chsete solenocytes (5). A neck-like region, sometimesstraight, sometimes curved, gradually narrows down andjoins the cell-body to the distal extremity of the "thread,"which is, in fact, a slender hollow tube of great length (Fig.in text, p. 495, and PL 27, figs. 1 and 4).

The longest tubes belong, of course, to those cells whichare situated furthest from the renal canal; they reach some-times a length of 90 [i, or nearly T\j- mm. The wall of thetube does not appear to be as stiff as in the case of Poly-chsBte solenocytes; and under the pressure of the cover-glass it is often much curved. In the living animal, however,I believe the tubes are always straight. The proximal endpierces the wall of the excretory duct, and projects a littleinto the lumen of the canal (figs. 3 and 4). A longflagellum,attached at its base to the cell placed at the end of the tube,works rapidly down the tube and far into the excretory canal(figs. 3 and4).!

BoAreri (influenced perhaps by the current dogma, whichaffirms, in spite of all evidence to the contrary, firstly, that alltubular excretory organs are of homologous nephridial nature ;and secondly, that nephridia are derived from the coclom,and generally, if not always, open into it) described opencoclomic funnels in Amphioxus, as already mentioned above.Neither in the living nor in sections of preserved specimenshave I been able to detect any direct communication betweenthe excretory canal and the ccelom. The branches of thetubule may be very numerous, of considerable length, andmay themselves divide, but they end b l ind ly (fig. 1). Itis to these blind ends that the tubes of the solenocytes con-verge, and here the wall of the canal is less loaded with

1 I was fortunately able to demonstrate the correctness of these observa-tions to Prof. Boven himself at the zoological station in Naples.

STRUCTURE OF KXCRETOBY ORGANS OP AMPHIOXUS. 497

excretory granules, and thinner than elsewhere. The nucleialso, which are so numerous in the other regions of thetubule, are not preseut just in those parts where thesolenocytes traverse its wall (Fig. in. text, p. 495).

Briefly to summarise the observations described above, itmay be stated that in Amphioxus there is a series ofexcretory tubules opening into the atrium, but not into theccelom, and provided at their blind internal ends with a largenumber of solenocytes. These tubules are situated " mor-phologically" outside the ccelom, being covered with ccelo-mic epithelium ; the solenocytes alone push through into thecoeloinic cavity.

At each end of the pharynx the excretory organs dwindlein size, as already pointed out by Boveri. The tubule inthese regions becomes shorter, the branches become reducedin size, or are not developed at all, and the number of soleno-cytes becomes much less. This is also the case throughoutthe pharyngeal region of small specimens. Fig. 3 repre-sents a small portion of the kidney of a young Amphioxus31 mm. long. Not only are the solenocytes not so crowded,but the average length of the tubes is less than in full-grown individuals (fig. 1).

That the segmental kidneys of Amphioxus really fulfil anexcretory function has been amply demonstrated by Weiss;md Boveri; but the part played by the solenocytes them-selves is less clear. Boveri, who remarked that their dis-tribution over the wall of the cceleni coincides with that of anetwork of blood-vessels, concluded that the "fadenzellen "were concerned in the elimination of waste products from theblood : " diese Zellen dem Chemismus der Excretion dieneu."He could not find that they took up colouring matters—aresult which agrees with my own observations on the soleno-cytes of PolychEetes (5, Part II). It seems to me probable,therefore, that, as I have already suggested for worms(5, Part II), the solenocytes are concerned chiefly with theelimination of fluid substances which can pass by osmosisthrough the thin walls of the tube, well adapted for such a

498 NDWIN H. GOODftlCfl.

purpose. The flagellum would serve to propel the fluid intothe excretory canal and thence to the exterior. That a con-siderable amount of fluid could pass through the tubes be-comes evident when we remember that in a full-grownAmphioxus there are, roughly speaking, 100 kidneys on eachside, or some 200 in all. Now each of these has, on an average,about 500 solenocytes—to take a low estimate,—making thenumber of solenocytes in the whole animal roughly 100,000.The average length of the solenocyte tube may be taken atY$ mm., or 50 fi. There are, therefore, about 5 metres of thisthin-walled tube in each full-grown individual, representingno inconsiderable area for osmotic exchange in an animal ofsuch small bulk.

Conclusion.—I do not propose in this paper to enterinto a detailed discussion of the homology and taxonomicimportance of the segmental kidneys of Amphioxus, butthe extraordinary resemblance they bear to the nephridia Ihave described in the Nephthyidas, G-lyceridse, and Phyllo-docidee must be insisted upon. For the purpose of com-parison, figures are given of the inner end of the nephridiumof Phyllodoce Pare t t i (figs. 2 and 5), which, of all thePolychsetes I have studied, most closely resembles Amphioxusin the structure of its renal organ. The nephridium of thisbeautiful Phyllodocid is large enough to be dissected out.It is then seen to end in the ccelom in a bunch of blindbranches, which are provided with a number of solenocytesarranged like the ribs of a fan. The tubes are in doublerows, while the cell-bodies of the two rows of solenocytes areclosely packed together, and wedged in alternately.1 Infig. 5 I have given a diagrammatic representation of theextremity of a branch of the nephridium, to compare withthe similar diagrammatic figure of a small portion of thekidney of Amphioxus (fig. 4). These figures bring outclearly the wonderful likeness of the two organs.

1 I estimate the number, of solenocytes in a Phyllodoce Paretti roughlyat 600,000, there be ing about 1500 to each nephridium, and some 200segments.

STRUCTURE OF EXCRETORY ORGANS OF AMPHIOXUS. 490

It results from these observations, as I have already pointedout in a preliminary paper (7), that in their segmentalarrangement, in their function, and in their histo-logical s t ructure, the excretory organs of Am-phioxus and the nephridia of Phyllodoce are in allessentials identical.

Before committing ourselves to new theories, somethingmust be known of the development of these organs; but,considering how remarkably close is the agreement betweenthe two, it seems more than probable that they are homologousstructures. If two such excretory organs as the solenocyte-bearing nephridia of Phyllodoce, and the solenocyte-bearingkidneys of Amphioxus, could be shown to have been inde-pendently involved, we should have to give up structuralresemblance as a guide to homology.1 But there seems to beno danger of our being driven to abandon the problem asyet, and all we need assume is, not that the vertebrates havebeen evolved from the Polychastes, but that the remotecommon ancestor of these now highly differentiated phyla wasof more elaborate structure than most authors have been hither-to inclined to suppose. We must assume that it possessed notonly paired coelomic (genital) sacs and ccelomostomes (6 and8), but also nephridia, whose blind internal end was providedwith solenocytes.2 We may conclude provisionally thatnow, for the first time, true nephridia have been shown tooccur in the vertebrate phylum; and further, we may hopeto trace in the vertebrates the same two series of organs—the nephridium and the ccelomostome—which I have elsewhere

1 The only case which seems to me at all comparable is that of thenematocysts in Ccelenterates, Planarians, and Molluscs.

2 This is all the more easy to believe since I have found these cells at theblind inner end of the nephridium of the larva of Phoronis (it will be remem-bered that Masterman observed cells similar to Boveri's " fadenzellen" inActinotrocha [9], and they have been described by Wagener [12]) ; and" flame-cells " very like solenocytes have been described in Nemertines byBurger (4), in Molluscs by Meisenheimer (10), and in .Rotifers byShephard (11). Also the "flame-cells" of Platyhelminths and EntoproctousPolyzoa are probably of the same nature (6).

500 EDWIN S. GOODRICH.

endeavoured to prove exist in the majority of coelomates(6, and 5, Part III).

It follows, from the conclusion provisionally adopted above,that the many theories which have been built on the assumedhomology between the separate segmental excretory organsof Amphioxus and the renal organs of coelomic origin of thehigher vertebrates must be allowed to drop for the present.These latter organs (pronephros, niesonephros, and genitalducts) have nothing to do with nephridia, and appear tobelong undoubtedly to the category of ccelomostoraes (5,Part III, and 8). Their homologues in Amphioxus may besought in the opening of the larval " head cavities," in the"brown funnels" described by Lankester, and in the segmentalgenital sacs as already suggested by Boveri (3). It is notimpossible, however, that true nephridia may yet be found atsome stage of development amongst the craniate vertebrates,and more especially in the Cyclostomes.1

L I S T OP REFEEENCES.

1. BOVERI, T.—" Ueber die Niere des Amphioxus," 'Munch, med. Wochen-

schrift,' No. 26, 1890.

2. BOVEKI, T.—"Die Nierencanalchen des Ampliioxus," ' Zool. Jalnb.,'vol. v, 1892.

3. BOVEKI, T.—"Ueber die Bilduugslate der Gesclikchtsdruseii, etc.,"' Anat. Anzeig.,' vol. vii, 1892.

4. BuKGbB, O.—" Die Nemertinen," ' fauna und flora des Golfes vonNeapcl,' vol. xxii, 1895.

5. GOODBICH, E. S.—"On the Nephridia of the Polychseta," pt. i, 'Quart.Journ. Micr. Sci.,' vol. xl, 1897; pt. ii, ibid., vol. xli, 1898; pt. iii,ibid., vol. xliii, 1900.

6. GOODUICH, E. S.—" On the Ccelom, Genital Ducts, and Nephridia,"'Quart. Journ. Micr. Sci.,' vol. xxxvii, 1895.

7. GOODRICH, E. S.—"On the Excretory Organs of Amphioxus," 'Proc.Roy. Soc.,' 1902.

1 I fully expect that nephridia will some day be found in the Enteropneustaand even in the Tunicata.

STBUPTUKE OF EXCRETORY ORGANS OP AMPHIOXUS. 501

8. L\NKESTER, E. RAY.—"The Enterocoela and Hie Coelomocoela," 'Treatiseon Zoology,' pt. 2, 1900.

9. MASTERMAN, A. T.—"On the Diplochorda," ' Quart. Journ. Micr. Sci.,'vol. xl, 1897.

10. MEISENHEIMEII, J.—"Entwickl. von D reissensia poly morpha, Pall,"' Zeit. f. wiss. Zool.,' vol. lxix, 1901.

11. SHEPHARD, J.—"On the Structure of the Vibratile Tags or Flame-cellm Rotilera," ' Pioc. Roy. Soc. Victoria,' vol. xi, 1899.

12. WAGENER, K.—"Ueber den Bau der Actinotrocha branchiata,"• Archiv f. Anat. und Phys.,' 1847.

13. WEISS, E.—"Excretory Tubules in Amphioxus lanceolatus,"'Owuait.Journ. Micr. Sci.,' vol. xxxi, 1890.

EXPLANATION OF PLATE 27,

Illustrating EDWIN S. GOODRICH'S paper " On the Structureof the Excretory Organs of Amphioxus."

FIG. 1.—Enlarged view of an excretory organ of Amphioxus, drawn fromthe living.

FIG. 2.—Enlarged view of the terminal tuft ot the nephridium of Phyllo-doce Pa re t t i , drawn from the living.

FIG. 3.—A small portion of the excreloiy canal of a young Amphioxus,with its solenocytes, from the living. Cam. T^ oil immeision, oc. 8.

FIGS. 4 and 5.—Semi-diagrammatic views of portions of the excretoryorgans of Amphioxus and Phyllodoce Pare t t i , from living and preservedspecimens.