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.