NEPHRIDIA OF CERTAIN EARTHWORMS. 397 On the Occurrence of numerous Nephridia in the same Segment in Certain Earthworms, and on the Relationship between the Excretory System in the Annelida and in the Platyhelminths. By Frank E. Beddard, M.A., Prosector to the Zoological Society of London, and Lecturer on Biology at Guy's Hospital. With Plates XXX and XXXI. A c a n t h o d r i l u s m u l t i p o r u s , F. E. B. 1 THE nephridia of this worm differ in their appearance from those of any other species of A c a n t h o d r i l u s at present known. In a dissection of the worm the nephridia can be recognised as a series of glandular tufts closely adherent to the body wall and to the intersegmental septa; each of the eight setse often appeared to have a nephridial tuft specially related to i t : thus by dissection there seemed to be eight separate nephridia in each segment. This, however, is not invariably the case, and in the anterior segments no relation between the setae and the nephridia could be detected by dissection. I have also studied these organs by transverse and longitudinal sections. By these means I have been able to ascertain that t h e r e are more t h a n one pair of n e p h r i d i o p o r e s in each segment o f t h e body. These observations depend upon the study of very well1 ' Proc. Zool. Soc.,' 1885. 398 PEANK E. BBDDAED. preserved material, for which I am indebted to Professor Parker, of Otago. One of the numerous specimens which he sent me was so preserved that the nuclei, not only of the nephridia but of the tissues generally, were stained dark yellow, and could not be subsequently stained by borax carmine; accordingly the nuclei were extremely conspicuous in such preparations ; and as the nuclei of the nephridial tubules differed in size and shape from other nuclei (e. g. those of peritoneal cells and blood-capillaries), the course of the tubules through the body walls could be easily followed. It must not, however, be inferred that such drawings (e.g. fig. 1) in the plate as illustrate the structure of the nephridial tubules are imaginary, except as concerns the nuclei. They are in every case accurate drawings, so far as I could make them ; but the conspicuous nuclei drew my attention to the delicate inconspicuous walls of the tubule, which would otherwise almost inevitably have been overlooked. The nephridia are arranged, as already stated, in tufts of tubules, closely adherent to the body wall (see figs. 2, 3); their structure is much like that of other earthworms; they consist of tubules with an intracellular duct, some (fig. n') larger than others (fig. n). The nephridial tufts are supplied with abundant blood-capillaries, upon some of which are those curious dilatations to which Lankester first drew attention in L u m b r i c u s . In spite of the most careful search I have hitherto failed to find any trace of the i n t e r n a l openings of the nephridia. The e x t e r n a l orifices, however, are obvious enough. The disposition of these is illustrated in figs. ] , 2, 3. Figs. 1, 2, 3 represent actual sections, or rather are compiled from a number of sections. Fig. 15 is schematic, and represent what I believe to be the general arrangement of the nephridia in certain segments of the body. Figs. 2, 3 are copied from sections through certain of the post-clitellar segments, fig. 1 the 8th or 9th. It will be noticed that the external pores are decidedly more numerous in the anterior segments of the body, while in the NBPHRIDIA OF CERTAIN EARTHWORMS. 399 posterior segments they tend to be arranged in accordance with the number of the setae, i. e. eight per somite. This disposition of the nephridiopores is associated with a corresponding regularity of the uephridial tufts, which tend to break up in the posterior segments into eight separate nephridia. There is, however, a connection between them, as shown iu figs. 2, 3. A series of tubules (figs. 1 n and 5 n) run from seta to seta, and unite the nephridial tufts of these setae; this tubule for the most part runs within t h e p e r i t o n e u m . The appearances presented, in fact, can hardly be explained, except on the assumption of a n e t w o r k of n e p h r i d i a l t u b u l e s . In no Annelid, except in P o n t o b d e l l a (Bourne 5) has the nephridial system been recorded to be a network. I can, however, find no evidence that the nephridial network of one side of the body is continuous with that of the other ; nor does there appear to be any connection between the nephridia of successive segments. The tubules leading to the exterior are, in the posterior segments, nearly invariably related to the setaj; occasionally (fig. 2 a) a tubule was observed to perforate the body wall between the setae, but in this case it must be noted that the tubule passes up a septum of connective tissue, which at this point breaks the continuity of the longitudinal muscle layer. It may be that such septa, which occur here and there, represent the last trace of setse which have now disappeared. Sometimes (fig. 3 a a') I noticed two nephridial tubules belonging to the same seta. I did not succeed in observing with certainty whether or not they opened on to the exterior by distinct orifices. The ductule is usually embedded in the lax connective tissue which surrounds the insertion of the seta (fig. 4); it passes up as far as the circular muscular layer without undergoing any changes in character, that is to say, the duct is iutracellular. At this point the tubule often runs for some distance along the junction between the circular and longitudinal muscles before perforating the former, and opening on to the exterior ; in other cases (fig. 4 b) the tubule at once perforates the circular muscular layer and the epidermis, and opens on to the exterior. VOL. XXVIII, PART 3 . NEW SEE. E E 400 FEANK E. BEDDARD. The distal section of the nephridium where it traverses the circular muscles is somewhat wider than the rest, and is lined by a single layer of small, delicate cells; the duct in this region is inter-cellular. Occasionally the distal section of the nephridium is branched (fig. 2 b) and opens by several (three) distinct orifices. In the anterior region of the body the nephridiopores of each segment are more numerous; they could be easily observed by a simple examination of the cuticle, and lie between the setse in a more or less regular row. There were over one hundred a p e r t u r e s in each of several segments that I examined in this way. In transverse sections the nephridial tubules were seen to pass through the body wall, not only in the immediate neighDourhood of the seta (fig. 1), but elsewhere. Very constantly the nephridial tubule did not open by a single pore, but branched, at the junction of the circular and longitudinal muscles, and opened on the exterior by a number of distinct orifices (fig. \b). This branching of the nephridial duct within the substance of the body wall is paralleled in the case of Capitella, where Fischer (8) has recorded a similar branching. Pig. 15 represents a diagram of what I believe to be the arrangement of the nephridia in one of the posterior segments of A. m u l t i p o r u s ; it maybe compared with fig. 14, which is a corresponding diagram of Perichseta. I am not able to give a satisfactory diagram of the anterior part of the body in Acanthodrilus. Perichseta, Schmarda. The peculiar " tufted " condition of the nephridia in this genus was first made known by Perrier, and has since been commented upon by others. This appearance of the nephridia led me to expect that I should find numerous nephridiopores in each segment. I was, however, unable to put this supposition to the test, until I received quite recently a number of NEPHBIDIA OF OEBTAIN EARTHWORMS. 401 excellently preserved examples from Bermuda, through the kindness of Mr. Shipley, Fellow of Christ's College, Cambridge. These specimens appear to be identical with Perrier's P. aspergillum. The nephridiopores could be easily observed, as in the case of A c a n t h o d r i l u s m u l t i p o r u s , upon the cuticle when stripped off and examined in water. I may take this opportunity of saying that there are other structures which might possibly be confounded with the nephridiopores; these are the impressions of sense cells upon the cuticle 1 which in Perichaeta often lie between the setae. A careful examination, however, soon serves to discriminate between the two; the circular bulgings of the cuticle, due to the prominent sense organs, although presenting the appearance of pores under a low power, are readily seen under a high power not to be pores at all, while the nephridiopores are clearly holes in the cuticle. The latter form a more or less irregular row surrounding each segment and lying between the setse (fig. 12). Often there are four or five between two setae. In transverse sections each pore is seen to be continuous with a nephridial tubule; the actual orifice is surrounded (fig. 8) by a very few large cells—smaller, however, than the cells of the epidermis; below these are smaller cells; that section of the tubule which lies within the circular muscle layer, has a wide lumeu whose walls are made up of excessively delicate flattened cells. At the junction of the circular and longitudinal fibres the duct becomes intracellular (fig. 10). The nephridial tubules are abundantly supplied with blood-vessels (figs. 10,11) in their passage through the body walls. The nephridial tubules agree with those of A. m u l t i p o r u s in the fact that the duct becomes inter-cellular at the junction of the longitudinal and circular muscles (cf. figs. 6 and 10). Fig. 9 represents the actual number of nephridial tubules and their external orifices in a small portion of the body wall; the figure would be equally correct, so far as my observations go, for any part of the body wall. I should state, however, that I have at present only 1 Vejdovsky (13), pi. xv,fig.13a. 402 FRANK B. BEDDARD. studied the anterior region of the body comprising the first sixteen or seventeen segments. I have never observed any branching of the nephridial tubules in the body wall like that which occurs in Acanthod r i l u s (see fig. 1); but I am not prepared to deny that it may occasionally happen. So far the nephridial system of Perichseta is closely similar to that of Acanthodrilus, with only some small differences in detail. An important point of difference is illustrated in fig. 7 ; in this figure it will be seen that the nephridial network of one segment is continuous through the septum with that of the next. The nephridial system in fact differs from that of any other earthworm, or indeed from that of any other Annelid except Pontobdella (Bourne) (5), in that it forms a continuous network u n i n t e r r u p t e d by the intersegmental septa. Furthermore, there appears to be a perfect continuity between the nephridial system of the right and left halves of the body. The nephridial system of one segment communicates with that of the neighbouring segments at numerous points; there is no question here of a pair of longitudinal ducts such as has been described recently in Lanice conchilega (Lang (11), Cunningham 6). The resemblance to Pontobdella is very striking, the only difference being that the external apertures in each segment are numerous instead of being only a single pair. With regard to internal apertures (funnels) I can say nothing. I have been entirely unable to find any trace of them. The diagrams (fig. 13) illustrates what I believe to be the arrangement of the nephridial network and the external pores (o) in a few segments. I should say that I cannot pretend to accuracy in the course of the tubules within the ccelom. To reconstruct from a series of sections the course of the comparatively simple nephridium of Lumbricus is a hard enough task ; to map out accurately the extremely complicated coils of the nephridial network of Perichaeta is for me an absolute impossibility. I can, however, assert most positively NEPHRIDIA OF CERTAIN EARTHWORMS. 403 that the external apertures do not each correspond to a nephridium isolated from its fellows; the nephridial tufts form a continuous layer coating the body wall; there must therefore be a network, although it may not be of course so complete a network as I have sketched in the figure just referred to. Typhseus, F. E. B., and Dichogaster, n. g. I have observed numerous nephridiopores in a single segment in both these genera; at present I can only record the fact without giving any details, which I hope to be able to do later. The E x c r e t o r y Organs of Annelids and Platyhelminths. Two views have been held respecting the relationship of the nephridia in Annelids to those of the Platyhelminths. Gegenbaur has held (c Comp. Anat./ Engl. trans,, p. 177) that there can be no direct homology between the nephridia in the two groups, because, in the Hirudinea at least, these organs are preceded by several pairs of embryonic excretory tubes. On the other hand, Lang and others believe that " the excretory system of the Platyhelminths is the starting point of that of all higher animals," that in fact the nephridia of Annelids are strictly comparable to those of the unsegmented worms. The former view has recently been extended and defended with great ability by Dr. R. S. Bergh, of Copenhagen (4). The latter view is the one which perhaps finds the most general acceptance among comparative anatomists. Bergh uses arguments which tend to prove that the provisional larval excretory organs of Polygordius, of Eupomatus, and other Polychseta, of the Hirudinea, of Echiurus, of certain Oligochseta (lately discovered by Vejdovsky), and of Mollusca, are homologous with each other and with the excretory system of the Platyhelminths ; the permanent nephridia of these various groups are therefore to be regarded as new formations (in the Annelida), or possibly to be derived from the geuital ducts of 404 PEANK B. BEDDARD. the flat-worms. Great stress is laid upon the structural identity of the Platyhelminth excretory system with the "head kidney" of larval P o l y g o r d i u s , Chtetopods, aud Gephyreans. In both there is a system of fine branched tubes formed of perforated cells, which unite to form a pair of wider tubes opening on to the exterior; the internal apertures open through a single cell, the so-called "flame cell;" in many of the larval forms the peculiarly modified flame cell is absent, but the aperture is plugged by a single cell. In the Hirudinea and Oligochseta there is no longer a special anatomical resemblance to the Platyhelminth; but this is due to the rudimentary condition of the larval excretory organ, rudimentary because there is no free swimming larva. Another argument is drawn from the apparent independence of the larval and permanent excretory organs in Annelids ; the fact that in many cases there is no connection between the larval nephridia and those of the adult, and the want of any confirmation of Hatchek's statements to the contrary, indirectly favour the hypothesis. Again, it is pointed out that while the larval nephridia of P o l y g o r d i u s lie in the head cavity, the persistent nephridia lie in the coelom ; and these two cavities are not similar. On the other hand, the Platyhelminths have no true coelom, only a series of minute clefts and spaces in the mesodermic tissue with which the flame cells are connected, and which form a " primary body cavity," comparable to the primary body cavity or head cavity of the Annelid larva. Dr. Bergh's conclusions largely depend upon his own researches into the nephridia of Hirudinea; these have been recently criticised by "Whitman (15), who meets Bergh's assertion that the larval nephridia have no connection with the permanent nephridia by an equally positive assertion that they have. With regard to the larval excretory organs of the Oligochseta, which have been discovered by Vejdovsky (13) in a variety of types, it is to my mind a significant fact that they occur at the anterior end of the body where no permanent nephridia are developed; furthermore, these organs lie in the NEPHRIDIA OF CERTAIN EARTHWORMS. 405 coelom perforating the mesentery which separates the first from the second segment j 1 hence Bergh's objection to the homology between the larval and permanent nephridia, on the score that the former do not lie in the true coelom, is removed. It is not yet a universal belief that a coelom is absent in the Platyhelminths; in any case, as Lang says, " the entire mesoderm of the Platyhelminths may very well be the equivalent of the entire mesoderm in the Enteroccela," apart altogether from the question of the enclosed cavity. In Capitellidae the nephridia seem, from Eisig's description, to lie in the somatopleure, i. e. not in the ccelomic cavity at all. The greater portion of the nephridium in P o l y g o r d i u s is similarly situated ; and Fraipont in his work upon the Archiannelida (9) remarks upon this as an archaic character. Again, Weldon (14) has brought forward reasons for believing that in Dinophilus, "which is literally no more than a larval Annelid with reproductive organs " (Lang), the body cavity may be really strictly comparable with that of Annelids, seeing thatin Saccocirrus—an undoubted Annelid—the body cavity may be secondarily (?) invaded by a ramifying network of mesodermic cells. In D i n o p h i l u s there are excretory organs of the Platyhelminth type, branched and ending in flame cells, which are in D. g y r o c i l i a t u s (according to Ed. Meyer, quoted by Lang) metamerically arranged, with a pair of external apertures to each segment. These facts taken together appear to me to do away with many of the difficulties urged by Bergh against the comparison of the Platyhelminth and Annelid excretory system. A difficulty in comparing the Platyhelminth with the Annelid excretory system is undoubtedly in certain structural differences; there is no trace in any Platyhelminth of a " funnel;" the excretory tubules end in the well-known "flame cells." This difficulty has led Lang (11) to regard the funnel in the Annelid as a new structure unrepresented in the Platyhelminths; this opinion is supported by the observations 1 Vejdovsky (13), pi. XVI,fig.6. 406 PRANK E. BJEDDAED. of E. Meyer and of Vejdovsky (13), that in Polychseta and Oligochseta the funnel is developed perfectly independently of the rest of the nephridium. It was important, however, to note that not only is the nephridial funnel formed by the proliferation of a single cell, but that in Stylaria this cell becomes ciliated and acquires a lumen before it undergoes division; repeating in fact the presumed ancestral condition. With regard to the presence of a single flagellum in the "flame cells," Hartog has recently pointed out (10 A) that the optical effect produced by the motion of minute cilia might readily give the impression of a single flagellum. In the adult Clepsine (Bourne 5) the funnel consists of only two cells, so that it is but a stage removed from the Platyhelminth funnel. The above facts lend at least some support to the views that it is unnecessary to regard the funnels of the Annelida as new s t r u c t u r e s . The facts recorded in the present paper fit in very well with the supposition that the Anuelid excretory system is directly traceable to that of the Platyhelminth; I shall suggest, however, a course of development rather different from that put forward by Lang. Lang has pointed out that in certain Plauarians a commencing metamerism (parallel with the commencing metamerism of the generative organs, &c.) is visible in the excretory system. Here and there " secondary" external orifices are formed through branches given off from the longitudinal trunks of either side; at first irregular, these secondary pores finally become regularly disposed, and a paired arrangement even is seen; the disappearance of at least the greater part of the network (and the development of internal funnels) brings about the conditions which occur in Lanice conchilega; in this Annelid, Meyer (11) and Cunningham (6) have shown that the longitudinal trunks connecting the nephridia of successive segments persist; Vejdovsky also (13) has figured traces of this same longitudinal duct in Anachseta; and Wilson has recently (16) been able to prove that the embryo Lumbricus, like the embryo Criodrilus, possesses a similar longitudinal NEPHRIDIA OF CURTAIN EARTHWORMS. 407 duct, one on each side of the body. Finally, the disappearance of the longitudinal duct leaves the paired nephridia of the majority of Annelids. The remarkable disposition of the nephridia of P o n t o b d e l l a , described by Bourne (5), is different in that there is not a single longitudinal duct on each side, but a continuous network. It resembles, in fact, as Lang has pointed out, the branched and anastomosing canals of the Trematode nephridium ; it must also be remembered that the longitudinal canals of G u n d a s e g m e n t a t a break up here and there into a network of anastomosing canals. It is this condition which has been inherited by P o n t o b d e l l a , and also by Perichseta ; Pericheeta appears to me to represent a more archaic structure than P o n t o b d e l l a since the external pores are more numerous; in P o n t o b d e l l a they have become reduced to a single pair in each somite. A c a n t h o d r i l u s m u l t i p o r u s offers the next stage; here the nephridial network is not continuous from segment to segment, but there is a separate network for each segment opening by numerous external pores. The Capitellidse (Eisig 7) agree in many particulars with A c a n t h o d r i l u s ; the nephridia of each segment are numerous, and occasionally are connected; the ducts opening on to the exterior are often (Fischer 8) branched and open by several distinct pores. In the posterior region of the body of A c a n t h o d r i l u s the external apertures are fewer, and are more particularly connected with the setse, while the nephridial network tends to become arranged in a series of tufts, corresponding in number to the setae; finally, the nephridial network of each half of the segment is independent. From A c a n t h o d r i l u s to L u m b r i c u s there is a considerable gap, only very partially bridged over by such forms as P l u t e l l u s (Perrier 12), where the irregularity in the position of the nephridial pores is, perhaps, to be regarded as a last trace of the numerous nephridial pores of A c a n t h o d r i l u s and Perichseta. The above considerations necessitate a further inquiry into the nature of the longitudinal canal in L a n i c e , &c.; if it be assumed that this latter is the homologue of the longitudinal canal in the Platyhelminths, it must follow that the 408 FRANK B. BEDDAED. Annelida have been derived from at least two Platyhelminth ancestors, i.e. one with a pair of longitudinal ducts, and another with a network of ducts. This would not perhaps be an unreasonable supposition were it not for the fact, that in this case L u m b r i c u s must have had a different origin from Perichseta. The nature of this longitudinal duct has been put in a fresh light by the observations of Wilson (16) j according to this author it arises from the epiblast, and is therefore comparable to the archinephric duct of Vertebrates, to which the observations of several writers have concurred in assigning an epiblastic origin. Haddon has recently (10) ingeniously suggested how a continuous groove, into which the nephridia opened, may have been converted into a canal opening into the cloaca. But while in the Vertebrata it seems to be generally agreed that the nephridial tubules are of mesoblastic origin,1 Wilson states, that in L u m b r i c u s they are budded out from the longitudinal duct, and are therefore epiblastic, with the exception of the funnel, which is mesoblastic. In any case his investigations only relate to early stages; and there is therefore nothing to negative the supposition that the portion which arises from the longitudinal duct is the vesicular region of the adult nephridium, which is known to be epiblastic, while the rest is mesoblastic. Lang (11) dwells upon the identity of the longitudinal duct of Annelida with the longitudinal canals of Platyhelminths, but apparently in the belief that the former is of mesoblastic origin like the latter. There are, however, now considerable reasons for believing that the longitudinal duct o f L u m b r i c u s , and possibly of L a n i c e , is epiblastic; this homology cannot therefore be at present definitely accepted. In the meantime, therefore, I would submit (1) that the origin of the Annelid excretory system from that of the Platyhelminths is as has been suggested in the present paper, (2) that the longitudinal duct of L u m b r i c u s , L a u i c e , &c, has not any relation to that of the Platyhelminths. 1 The pronephros has been described as formed by outgrowths of the archiuephiic duct, and therefore epiblastic. NEPHRIDIA OF CERTAIN EARTHWORMS. 409 L I S T OF M E M O I R S REFERRED TO. (1) BEDDARD, F. E.—" Preliminary Note on the Nephridia of a New Species of Earthworm," ' Proc. Roy. Soc.,' 1885, and of 'Ann. Sci. Nat.,' 1885. (2) BEDDARD, F. E.—"Preliminary Note on the Nephridia of Perichseta," •Proc. Roy. Soc.,' 1888. (3) BENHAM, W. B.—" Studies in Earthworms," 'Quart. Journ. Micr. Soi.,' 1886 and 1887. (4) BERGH, R. S.—" Die Exkretions Organe der Wiirmer," ' Kosmos,' ] 885. (5) BOURNE, A. G.—" Contributions to the Anatomy of the Hirudinea," ' Quart. Journ. Micr. Sci.,' 1884. (6) CUNNINGHAM, J. T.—"On the Nephridia of Lanice conchilega," • Nature,' June 16th, 1887. (7) EISIG, H.—" Die Segmental Organe der Capitelliden," ' Mitth. a. d. Zool. Stat. Neapel,' 1879. (8) FISCHER, W.—"Ueber Cap itella capitata," ' Zool. Anz.,' 1883. (9) FRAIPONT, J.—"Polygordius," • Naples Monographs,' 1887. (10) HADDON, A. C.—" Suggestion respecting the Epiblastic Origin of the Segmental Duct," ' Proc. Roy. Dublin Soc.,' 1887. (10 A) HARTOG, M.—" The True Nature of the Madriporia System of Echinodermata, with Remarks on Nephridia," ' Ann. and Mag. Nat. Hist.,' Nov., 1887. (11) LANG, A.—" Die Polycladen," ' Naples Monograph,' 1884. (12) PERKIER, E.—" Etudes sur un genre nouveau des Lombriciens," • Arch. Zool. Exp.,1 1873. (13) VEJDOVSKS, F.—'System und Morphologie der Oligochaeten,' Frag., 1884. (11) WELDON, W. F. R.—"On Dinophilus gigas," ' Quart Journ. Mior. Sci.,' 1886. (15) WHITMAN, C. 0.—" A Contribution to the History of the Germ Layers inClepsine," ' Journ. Morph.,' 1887. (16) WILSON, E. B.—"The Germ Bands of Lumbricus," ' Joum.Morph.,' 1887.
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