The Enteronepliric Type of Nephridial System
in the Genus Tonoscolex (Gates).
By
Karm Narayan BaM, D.Sc. (Panj), D.PML, B.Sc. (Oxon.),
Professor of Zoology, University of Lucknow, India.
With 10 Text-figures.
CONTENTS.
PAGE
1. INTRODUCTION
443
2. T H E GENUS T O N O S C O L E X
445
3 . T H E N E P H R I D I A L SYSTEM O F T O N O S C O L E X
.
.
.
.
445
(a) T h e General Plan of t h e System, p . 445. (6) The Septal
Nephridia, p . 446. (c) T h e Ducts a n d Openings of the Septal
Nephridia, p . 457. (d) T h e Pharyngeal Nephridia a n d their
Ducts, p . 460. (e) The Integumentary Nephridia, p . 461.
.
462
5. T H E MORPHOLO&Y AND O R I G I N O F T H E SEPTAL E N T E R O N E P H E I C
4 . T H E B L O O D - S U P P L Y O F THE N E P H R I D I A
.
.
.
.
463
NEPHRIDIA
6. SUMMARY
465
1. INTRODUCTION.
IN a series of memoirs published in this journal I have described the 'enteronephric' type of nephridial system in three
genera of earthworms, namely, P h e r e t i m a , L a m p i t o
( M e g a s c o l e x ) , and W o o d w a r d i e l l a 1 (1, 3, 4, and 5), all
belonging to the sub-family Megascolecinae of the family
Megascolecidae. The nephridia of this type are remarkable in
that they discharge their excretory products through segmentally arranged apertures into the gut instead of on to the surface
of the body. I am now able to add a fourth genus, i.e. T o n o scolex (also belonging to the sub-family Megascolecinae), to the
category of earthworms possessing the ' enteronephric' type of
nephridia. But the enteronephric system of T o n o s c o l e x
1
Gates has recently instituted a new genus Nellogaster for Woodwardia=Woodwardiella (sRec. Ind. Mus.', vol. xl, Pt. 4, Dec. 1938).
444
KAEM NABAYAN BAHL
differs in important particulars from that previously described
by me in the other three genera; in fact, the system in Tonoscolex is decidedly simpler and therefore probably more
primitive; there is neither a s e p t a l e x c r e t o r y c a n a l nor
a s u p r a - i n t e s t i n a l e x c r e t o r y d u c t , the two structures
which form important and essential features of the system as
found in P h e r e t i m a , L a m p i t o , and W o o d w a r d i e l l a .
Since thenephridialsystemofTonoscolexlacks the elaborate
arrangement Avhich obtains in the other three enteronephric
genera, it throws some light on the origin of the enteronephric
type of nephridial system. What I wrote in 1926 (5) about this
type of nephridial system is worth repeating here: ' The chief
point of interest which may well be emphasised here is that this
type of excretory system seems to be widely spread amongst
earthworms, which would seem to need re-examination from the
point of view of the occurrence and origin of the "enteronephric"
excretory system.'
An historical account of nephridial systems other than the
ordinary meganephric type has already been given by me in a
previous paper (1), and it is therefore unnecessary to give such
an account again.
Specimens o f T o n o s c o l e x o n which the present investigation is based Avere kindly sent to me by Professor Gordon E.
Gates of Judson College, Eangoon (Burma), in three lots, in
May, July, and September 1937, and I am deeply indebted to
him for the opportunity he has given me of examining the
material collected by him. Further, at my request he specially
obtained four more specimens at considerable inconvenience,
cleaned their guts by feeding them on blotting-paper, fixed them
in Bouin's fluid, and sent them to me in December 1938 and
January 1939. He wrote to me; 'The genus T o n o s c o l e x
comprises several Burmese species and a few Indian species, the
latter having been included by Stephenson in the genus Megas e o l e x . Stephenson's Megascolex is, as he pointed out,
polyphyletic and should be revised. I suggest that one basis of
a successful revision will be provided by your classification of
the nephridia.'
A preliminary account of the nephridia of T o n o s c o l e x
ENTEBONBPHRIC SYSTEM OF TONOSCOLEX
445
was communicated by me to tbe Jubilee Session of the Indian
Science Congress in January 1938, and tbe completed work is
being published now.
My best thanks are due to Dr. M. L. Bhatia for staining
several series of sections for me and for assisting me in the
preparation of illustrations. My thanks are also due to Mr.
G. N. Natu for making a number of diagrams for this paper.
2. THE GENUS TONOSCOIEX.
The genus Tonoscolex has been instituted only recently
by Gates (8, 1933) for Burmese earthworms formerly referred
toNotoscolex. To these were added three Indian species of
Notoscolex, one species of Megascolides, and one species
of Megascolex. Gates (8) has described altogether eight
species of Tonoseolex, of which I have examined three,
namely, Tonoscolex depressus, Tonoscolex mont a n u s , and Tonoscolex birmanicus, for the study of
their nephridia. He instituted this genus mainly on the position
of the male and female pores, the gizzard, and the stalked
calciferous glands. He did not examine the nephridia, since he
wrote to me:' The excretory organs have notbeencarefully
examined, but are probably exonephric micronephridia and
possibly also enteronephric micro- or meganephridia.' My study
of the nephridial system leading to the discovery of a primitive
type of enteronephric system inTonoscolex amply justifies,
to my mind, Gates's institution of the new genus.
3. THE NEPHRIDIAL SYSTEM OF TONOSCOLEX.
(a) The General Plan of the System.
The nephridial system of Tonoscolex, like that of Pher etima, Lampito, or Woodwardiella, consists of three
sets of nephridia, namely, the septal, the integumentary, and
the pharyngeal. Of these, the septal nephridia are the
largest and the most prominent; they are distributed as four
tofifteenpairs of micronephridia in each segment in the intestinal region. These nephridia do not open to the exterior on the
skin but into the intestine in each segment. They are, therefore,
' e n t e r o n e p h r i c ' micronephridia.
446
KAEM NAEAYAN BAHL
The i n t e g u m e n t a r y n e p h r i d i a are very small in size
and are noticed with difficulty in specimens preserved in spirit.
They occur in almost all the segments of the worm except the
first few, but are specially abundant in the clitellar segments.
Each integumentary nephridium opens separately on the bodywall through a minute nephridiopore. These nephridia are,
therefore, ' e x o n e p h r i c ' m i c r o n e p h r i d i a .
The p h a r y n g e a l n e p h r i d i a form a large cylindrical tuft,
surrounding the oesophagus just in front of the gizzard in the
s i x t h and fifth segments. The tuft contains hundreds of
micronephridia; the individual nephridia are very small but
discrete; their ductules join together and run forward in sheaves,
and open anteriorly into the pharynx. These nephridia, therefore, are also to be classed as ' e n t e r o n e p h r i c ' m i c r o nephridia.
The general plan of the nephridial system showing the three
sets of nephridia is represented in Text-fig. 1.
(b) The S e p t a l N e p h r i d i a .
These nephridia are the most remarkable of the three sets,
and the determination of their individuality and structure
presented considerable difficulty.
(i) P o s i t i o n and D i s t r i b u t i o n . — I n the pre-clitellar
region there are no septal nephridia, nor are they to be seen for
many segments behind the clitellum. In P h e r e t i m a the
septal nephridia begin from the fifteenth segment, but in
Tonoscolex they begin very far behind. In a specimen
of Tonoscolex m o n t a n u s with a total number of 129
segments, the septal nephridia were seen to begin from the fiftysixth segment, while in a specimen of Tonoscolex d e p r e s s u s, 260 mm. in length, the septal nephridia begin from the
ninety-first segment.
They first appear as a few (four or five) slender thread-like
nephridia closely applied to the intestine on each side of the
dorsal vessel, but towards the middle of the body they increase
in number and size and become so large and prominent as to
conceal the intestine entirely from view in a mid-dorsal dissection (Text-fig. 2). Towards the posterior end of the worm
ENTEHONEPHEIC SYSTEM OF TONOSCOLEX
447
e.g.
•ph. n. d.
TEXT-FIG. 1.
The general plan of the nephridial system (semi-diagrammatic).
eg., cerebral ganglion; el., clitellum; d.v., dorsal vessel; giz., gizzard ; i.n., integumentary nephridia; int., intestine; ph., pharynx;
ph.n., pharyngeal nephridia; ph.n.d., ductules of the pharyngeal
nephridia; s.n., septal nephridia; t.n.d., terminal nephridial duct.
t.n.d?
TEXT-FIG. 2.
v.n.c.
I. n.v.
spt. nph.
The lay-out of the septal nephridia in the intestinal region on a mid-dorsal incision, cotn.v., commissural
vessel connecting the dorsal vessel with the lateral neural; d.v., dorsal vessel; /., funnels of septal
nephridia; int., intestine; l.n.v., lateral neural blood-vessel; nph.d.v., nephridio-dorsal vessel; o., common median opening of the two terminal nephridial ducts of a segment; spt.nph., septal nephridia;
t.n.d.1, terminal nephridial duet as it emerges from the septal nephridia and enters the intestine;
t.n.d.2, terminal nephridial duct as it penetrates the typhlosole to join with its fellow of the opposite
side and open into the intestine by the median aperture o.; v.n.c, ventral nerve-cord; v.v., ventral
vessel.
Post.
Anl
cotn.v. nph.d.v. d.v. t.n.d.1
f
!
H
a
2
ENTERONEPHRIC SYSTEM OF TONOSCOLEX
449
the nephridia gradually become fewer in number again. The
septal micronephridia on each side of a segment are so compactly
arranged together as to look like a meganephridium on each side
of the dorsal vessel; in fact, I myself mistook them at first for
a pair of meganephridia in each segment, and my greatest
difficulty in this piece of research has been to unravel these
apparent meganephridia into their component micronephridia,
and to trace the course of the nephridial canal in an individual
nephridium. The difficulty was enhanced by the fact that I had
to work all the time on preserved specimens and could not have
access to any living specimens at all.
Two peculiarities of these nephridia are noticed at once: the
first is that all the nephridia on each side of a segment are closely
connected together so as to form an apparently continuous mass
covering the intestine (Text-fig. 2), looking like a pair of meganephridia in each segment, but instead of lying against the
body-wall they closely surround and conceal the intestine. The
second peculiarity is that they are connected at their dorsal ends
directly with the median dorsal blood-vessel through a pair of
very short but big nephridio-dorsal blood-vessels, and also with
the mid-dorsal area of the gut into which they open.
On a superficial examination, each apparent meganephridium
is seen to be thickest and widest at its dorsal end, while during
its course towards its ventral end it gives off, along its anterior
margin, a number of digitate processes, each of which is connected by a very slender cord with the intersegmental septum
in front. But on unravelling an apparent meganephridium it is
found that it consists of a number (four to fifteen) of micronephridia closely bound together by connective tissue, and that
each of these septal nephridia is V-shaped in outline, one limb
of which is directed antero-ventrally towards the septum in
front, and is connected with it through a narrow nephridial
canal following the funnel, while the other limb is directed
ventrally and is attached through connective tissue with the
corresponding limbs of the preceding and succeeding nephridia
of the series. Each nephridium has its pre-septal runnel, so that
there are as many funnels on each septum as there are micronephridia in the succeeding segment (Text-fig. 4).
450
KARM NABAYAN BAHL
(ii) Attachment.—The line of attachment of the septal
nephridia on each septum lies just external and parallel to the
commissural vessel connecting the dorsal with the ventral and
lateral neural vessels. This blood-vessel runs along the anterior
face of each septum (Text-fig. 4) very near and parallel to its
outer margin, i.e. the margin attached to the body-wall. Only
the funnel together with a very short portion (about 22 //.) of the
following nephridial canal lies in front of the septum, the funnels
lying in a linear row parallel to and all along the length of the
commissural vessel. Text-fig. 3 is a microphotograph of a preparation of a group of septal nephridia; while Text-fig. 4 is a
semi-diagrammatic representation of the septal nephridia, as
they occur on the right side of a segment, showing their relative
position with regard to the dorsal and commissural vessels, and
their connexion with the intersegmental septum in front which
bears the funnels.
(iii) Number.—The number of nephridia in different segments varies within limits. As already stated, the first few
segments possessing septal nephridia have only four or five of
them on each side, but in the succeeding segments the number
increases to from twelve to fifteen on each side, this number
being met with in most of the segments of the intestinal region.
Each of these septa thus carries twenty-four to thirty nephridia.
(iv) I n d i v i d u a l i t y . — E a c h nephridium is a separate and
discrete structure a s i n P h e r e t i m a , but as the posterior limbs
of all the nephridia are joined together by connective tissue and
form an apparently continuous and single mass, one is led at first
sight to the mistaken conclusion that the whole set of nephridia
of each side is a meganephridium.
(v) The S t r u c t u r e of a Single Nephridium.—Each
septal nephridium is more or less V-shaped in outline (Text-fig.
5), one limb of which is longer than the other. The short anterior limb lies just behind the septum and is connected with
the latter through the free nephridial canal following the funnel;
the longer posterior limb is a continuation of the shorter anterior
limb, but lies at an angle with it away from the intersegmental
septum in front and, in fact, near the posterior intersegmental
septum. The anterior limbs of all the nephridia lie separately
451
ENTERONEPHKIC SYSTEM OF TONOSCOLEX
from one another, but the posterior limbs of all the nephridia
are connected with one another and form one connected mass,
the individual elements of which can be separated only with
difficulty. That they are actually distinct and separate is made
>-nph.m.
b.v.
mt.w.
s.c.ep,
mt.c.
TEXT-FIG. 3.
A reconstruction of three consecutive sections (6 jx in thickness)
showing the course of the two terminal nephridial ducts of a
segment as they traverse the typhlosole and join together to
open into the lumen of the intestine, b.v., blood-vessels of the
nephridia; cil.ep., ciliated epithelium of the intestine; d.v., dorsal
vessel; int.c, capillaries in the wall of the intestine; int.w., intestinal wall; nph.c, nephridial canals; nph.m., nephridial mass;
nph.s., nephridial set; o., common median opening through which
the two terminal excretory ducts open into the lumen of the
intestine; s.c.ep., splanchnic layer of coelomic epithelium; t.n.d.,
terminal nephridial duet; ty., typhlosole.
out easily by a study of serial sections (Text-fig. 8). There
is one exception in the arrangement of the two linibs of a
Post
Ant.
t-n.d.
l.p.l.
t.n.c.,
com.v.
TEXT-FIG. 4.
The arrangement of the septal nephridia (semi-diagrammatic).
com.v., commissural vessel; d.v., dorsal vessel; /., funnel; f.n.c,
first part of the nephridial canal following the funnel; l.p.l., long
posterior limbs; nph.d.v., nephridio-dorsal vessel; s.a.l., short
anterior limbs; spt., intersegmental septum; t.n.c, terminal
nephridial canals; t.n.d., terminal nephridial duct; AB, line of
section as shown in Text-fig. 8.
-t.n.c.
s. &. 1.
cii.1.
l.p.1..
f.
TEXT-FIG. 5.
A single septal nephridium showing the course of the nephridial
canal (semi-diagrammatic), cil.l., brown ciliated loop with excretory granules; /., funnel; f.n.c, first part of the nephridial
canal; l.p.l., long posterior limb; s.a.l., short anterior limb; spt.,
intersegmental septum; t.n.c, terminal nephridial canal; 1-6, the
limbs of the nephridial canal as it courses through the anterior and
posterior limbs; V, first part of the nephridial canal as it enters the
anterior limb and passes into the brown ciliated loop.
454
KAEM NAEAYAN BAHL
nephridium which may be noted here. In the most ventral
nephridium of the whole series the short anterior limb lies
towards the posterior septum while the posterior limb lies towards the anterior septum (Text-fig. 4). Why the normal arrangement is reversed in the case of this nephridium I cannot say.
Each nephridium (Text-fig. 5) begins with a very small preseptal funnel which lies in the segment preceding the one in
which lies the body of the nephridium. The funnel is followed
by a long ciliated canal which pierces the septum just behind
the funnel and travels obliquely upwards to enter the anterior
limb of the nephridium. In the body of the nephridium the
nephridial canal makes several loops till it passes into the terminal nephridial canal, which runs along the surface of the
shorter anterior limb and leaves the nephridium at the place of
junction of the two limbs. We shall now describe the different
parts of a septal nephridium in detail.
The P r e - S e p t a l Funnel.—Each nephridiostome (Textfig. 6) is a minute bulb-like structure with a crescentic aperture
opening into the coelomic cavity. In its general shape and
structure the funnel closely resembles that of a septal nephridium o f P h e r e t i m a (1), consisting of a large hood-like upper
lip and a small lower lip. The funnel measures 38 fi in diameter
in a surface view, while in a longitudinal section (Text-fig. 7) it
measures about 20 /x dorso-ventrally, the greatest width of the
aperture in a longitudinal section being 11 /x. The body of the
funnel is formed of a single large semicircular c e n t r a l cell
which is bounded by a number (eleven or twelve) of m a r g i n a l
c e l l s . The central cell forms the body "of the upper lip and has
a large and prominent nucleus in its centre. The outer margin
of the central cell is beset with the small marginal cells, each
with a small rounded nucleus. All the marginal cells are equal
in size and form an incomplete circle bordering the upper lip.
Both the central and the marginal cells are profusely ciliated
along their inner surface; the cilia are closely set and in sections
present a characteristic bushy appearance (Text-fig. 7).
The lower lip is much smaller and much thinner than the
upper lip. It has a crescentic and convex border and consists
of six small marginal cells and a number of very small compactly
455
ENTEBONEPHEIC SYSTEM OF TONOSCOLEX
arranged cells forming its body. The lower lip is also ciliated
like the upper. The aperture measures about 22 fj. from side to
side and about 11 p, from the upper to the lower lip. A number
of coelomic epithelial cells invest the funnel here and there.
e.c.
TEXT-HG. 6.
TEXT-ITG. 7.
Kg. 6. The pre-septal funnel in a surface view, f.n.t., first part of
the nephridial canal.
Fig. 7. The funnel in longitudinal section, ex., central cell; c.e.c,
coelomic epithelial cell; f.n.t., first part of the nephridial canal;
11., lower lip; m.c, marginal cell; u.l., upper lip.
The F r e e N e p h r i d i a l Tube.—The free nephridial tube
following the funnel is fairly long, about 200 /t or more in length,
and is ciliated all along its course. It has an intracellular
lumen, and runs obliquely backwards and upwards alongside
a narrow blood-vessel, and forms a narrow thread-like structure
hanging freely across the coelom between the .septum in front
and the anterior limb of each nephridium behind. On reaching
the anterior end of the anterior limb, the canal becomes incorporated at once into this limb.
The B o d y of t h e Nephridium.—As already stated, the
body of the nephridium consists" of a short anterior limb and
a long posterior limb. The short limb is, on an average, about
380 /* in length and 60 JU, in thickness, while the posterior limb
456
KARM NARAYAN BAHL
is about twice as long as the anterior limb. The free nephridial
canal on entering the anterior limb loses its cilia and runs for
a short distance close to the surface until it forms a bulbous
enlargement (Text-fig. 5). From this bulbous enlargement
arises a large ciliated canal which travels upwards and then
downwards, thus forming a wide ' c i l i a t e d l o o p ' . This
ciliated loop forms a very prominent feature of the anterior limb
on account of its following peculiarities: (1) it is the widest part
of the nephridial canal, (2) it is ciliated, (3) it forms an Z-shaped
loop, and (4) it is laden with brownish or brownish-black excretory granules all along its length. In whole mounts as well as
in sections the loop at once attracts attention because of the
presence of excretory granules in its walls. In sections (Textfig. 8) the cells surrounding this part of the canal are seen to
contain a large number of dark excretory granules. This ciliated
loop seems to be the special excretory area of the nephridium,
as one never finds excretory granules embedded in any other
part of the nephridial canal. This ciliated loop is closely comparable to the 'brown ciliated tube' which I described in the
septal nephridium of P h e r e t i m a (1, fig. 2, PI. 7). The
nephridial canal following the ciliated loop makes three 'rounds',
so to speak, in each of the two limbs of the nephridium, thus
forming six canals in each of the two limbs, besides the terminal
nephridial canal in the anterior limb. The exact course of the
nephridial canal within the two limbs is represented in Textfig-5.
It will be seen that the nephridial canal along the greater part
of its length within the nephridium is non-ciliated, but that
there are four ciliated tracts in each nephridium, three of which
lie in the anterior limb. The f i r s t ciliated tract lies in the free
nephridial canal following the funnel in which the cilia beat
towards the body of the nephridium; the second is the socalled 'ciliated loop' in the walls of which excretory granules
are present, the cilia carrying the fluid along the course of the
loop first downwards and then towards the apex of the anterior
limb; the t h i r d tract occurs in the second limb (marked S in
Text-fig. 5) of the second loop in which cilia are directed towards
the base of the anterior limb; the f o u r t h tract occurs in the
ENTEKOOT3PHEIC SYSTEM OF TOKOSCOLBX
457
terminal nephridial canal which leaves the nephridinm and in
which the cilia are directed outwards.
The terminal nephridial canal of each nepfaridiam runs along
the surface of the anterior limb and is easily seen in sections to
lie superficially (Text-fig. 8). It leaves its nephridium at the
junction of the two limbs, and then travels dorsally across the
posterior limbs of the nephridia lying dorsally to it until it
reaches the posterior border of the nephridial mass (Text-figs. 4
and 8). Thus the terminal canals of successive nepbxidia of each
side of a segment travel dorsally along the posterior border of
the mass of posterior limbs for a long distance and then open
into the terminal canals of succeeding nephridia, until they form
a large t e r m i n a l d u c t on each side of a segment (Test-fig. 4).
Each terminal duct is, therefore, formed by the union of terminal canals of all the nephridia lying on one side of a segment.
Thus there are two large terminal ducts, right and left, in each
segment, one from each set of twelve to fifteen nephridia. Textfig. 8 represents a section passing through four anterior limbs,
seven posterior limbs, and one junction of anterior and posterior
limbs of a set of septal nephridia. The direction of the section
is shown roughly by the line AB in Text-fig. 4. Text-fig. 8 shows
the nephridial canals as seen in sections of the two limbs, the
ciliated loop with dark granules, the terminal nephridial canal
as it runs on the surface of the three anterior limbs, and the
terminal canals as they lie on the posterior border of the posterior limbs of the nephridial set before forming the terminal
nephridial duct.
(c) The D u c t s a n d O p e n i n g s of t h e S e p t a l N e p h r i d i a .
The terminal canals of all the nephridia of each side of a segment unite to form a terminal duct; the two terminal duets in
each segment leave their nephridial masses at their dorsal ends,
one on each side of the dorsal vessel (Text-fig. 2), and at once
enter the roof of the intestine in the region of the typhlosole
(Text-fig. 3). Each terminal duct is a thin-walled tube which
runs for a short distance of about 135 \L before it enters the roof
of the intestine. On entering the typhlosole the two terminal
ducts run obliquely downwards along the two flanks of the
NO. 327
H
h
t.n.c.
TEXT-FIG. 8.
A section across the septal nephridia of a series of one side (approximately along the line AB in Text-fig. 4) passing through four
ENTEEONBPHEIC SYSTEM OF- TONOSCOLEX
459
typhlosole just within the intestinal epithelium. The typhlosole
i n T o n o s c o l e x i s triangular in shape in a transverse section,
and Text-fig. 10 shows the two terminal ducts, each running
along each side of the triangle. Each of these ducts travels a
distance of about 200 ^ within the typhlosole, and just within
the internal epithelial lining. At the apex of the triangular
typhlosole the two ducts unite, and then open by a single
median aperture into the lumen of the intestine (Text-fig. 3).
This median aperture is very narrow, being only about 12 fc in
diameter. All along its length within the typhlosole, each of the
two terminal ducts is accompanied by a narrow blood-vessel,
the t y p h l o s o l a r v e s s e l , and just as the two terminal ducts
unite at the apex of the typhlosole, so do these two typhlosolar
vessels.
It will be seen, therefore, that the terminal canals of all the
septal nephridia of each side of a segment unite together to form
a terminal duct alongside the nephridial mass itself (Text-fig. 4),
there being no septal excretory canal such as wefindin the other
three enteronephric genera. Further, the two terminal ducts
enter the typhlosole independently and directly, the longitudinal
supra-intestinal excretory ducts o f P h e r e t i m a , L a m p i t o ,
and W o o d w a r d i e l l a being also absent in T o n o s e o l e x .
The two terminal ducts enter the typhlosolar region of the
intestine in the posterior part of each segment (Text-fig. 2), just
behind the posterior pair of dorso-intestinal vessels.
anterior and s e v e n posterior limbs and one at the junction of
the two limbs, and showing the nephridial canals and the terminal
nephridial canals. cil.L, ciliated loop with dark excretory granules;
com.v., commissural vessel; e.g., excretory granules; /., funnel;
f.n.c, first part of the nephridial canal; s.n.b., a branch of the septonephridial vessel accompanying the first part of the nephridial
canal; spt., intersegmental septum; t.n.c, terminal nephridial
canal; l'—4', the anterior limbs in section; 5', junction of anterior
and posterior limbs; 1-7, posterior limbs in section. Each
anterior limb carries six nephridial canals in two sets of three,
besides the terminal nephridial canal, while each posterior limb
also carries six nephridial canals. 5' shows three canals of the anterior and three of the posterior limb, the other two sets of three
each have joined with one another in a preceding section of the
series. A number of terminal nephridial canals are seen on the
right of the posterior limbs.
460
KARM NARAYAN BAHL
(d) The Pharyngeal Nephridia and their D u c t s .
The pharyngeal nephridia in Tonoscolex occur as a large
and conspicuous tuft of nephridia surrounding the oesophagus
in the sixth and fifth segments. The septum 6/7 is thick; its
insertion on the hody-wall is normal, i.e. on the inner surface
phn.
f.n.c.
TEXT-FIG. 9.
A transverse section of the oesophagus in front of the gizzard,
showing the tufts of pharyngeal nephridia in the s i x t h segment.
d.v., dorsal vessel; oe., oesophagus; ph.n., tufts of pharyngeal
nephridia; v.n.c, ventral nerve-cord.
of the intersegmental groove 6j7, hut its insertion on the alimentary canal is far behind and lies at the posterior end of the
gizzard, almost opposite the intersegmental groove 8/9, so that
the septum forms an elongated cone-like structure directed
backwards (Text-fig. 1). The gizzard occupies the posterior half
of this septal cone, while the anterior half is occupied by the
oesophagus in front of the gizzard. This part of the oesophagus
in the sixth segment is completely surrounded by the bunches
of pharyngeal nephridia, which form a thick cylindrical ring
around the oesophagus (Text-fig. 9). Further, the septum 5/6
is ill-developed and consists only of a number of muscular
ENTEKONEPHRIC SYSTEM OF TONOSCOLEX
461
strands from the body-wall to the oesophagus; thus several of the
pharyngeal nephridia extend forward into the fifth segment also.
On a superficial examination the pharyngeal nephridia look
like compact masses of short threads, but on a microscopical
examination it is seen that each pharyngeal nephridium is
distinct, but that the terminal canals of several nephridia join
together to form ductules which run forwards and open into the
pharynx in the fourth and third, segments. There are several
such ductules leading from the tufts of the pharyngeal nephridia
and opening into the pharynx. These ductules travel a long
distance along the muscular strands that extend from the
anterior region of the oesophagus to the pharynx in front and.
have a characteristic appearance in sections. They have an
external covering of cells, but the lumen is surrounded by a noncellular thick membrane. Generally the walls of the ductules
are closely adpressed, but at several places they present a large
ellipsoid lumen. Once they enter the wall of the pharynx, the
lumen within them is seen all along their course till they open
into the pharyngeal lumen (Text-fig. 10).
Each pharyngeal nephridium is V-shaped in outline, consisting of a short straight lobe and a long slightly twisted lobe,
there being no funnel. In size these nephridia are much smaEer
than the septal nephridia, but are slightly larger than the
integumentary nephridia. The short lobe is about 56 p. in
length, while the long lobe is 464 JU. in length, i.e. the long lobe
is about eight times as long as the short lobe. The disproportion
between the length of the two limbs is much greater in the
pharyngeal nephridia than in either the septal or the integumentary nephridia.
The blood-glands which form a constant feature of the
pharyngeal nephridia of P h e r e t i m a are absent in T o n o scolex.
(e) The I n t e g u m e n t a r y N e p h r i d i a .
The integumentary nephridia are attached to the inner
surface of the integument, i.e. to the somatic layer of the
peritoneal lining of the coelom. They are absent in the first three
segments, but are present in all the succeeding segments.
462
KAKM NARAYAN BAHL
These nephridia are extremely small and have no funnel; each
is a V-shaped structure consisting of a short lobe and a long lobe,
and is attached to the body-wall through the terminal ductule
which emerges from the nephridium at the junction of the two
lobes. The two lobes are unequal in size, the short lobe being
about 108 [i in length and the long lobe about 298 \i in length.
ph.gl.m.
A.M.
i.n.
v.n.c.
o.d.
TEXT-FIG. 10.
A transverse section of the pharynx in the f o u r t h segment, showing
four ductules of the pharyngeal nephridia in the ventral wall of
the pharynx and another opening into the pharyngeal lumen.
d.v., dorsal vessel; i.n., integumentary nephridia: ph.gl.m., mass
of pharyngeal glands on the surface of the pharyngeal bulb;
ph.n.d., ducts of the pharyngeal nephridia; o.d., opening of one of
the pharyngeal nephridial ducts; v.n.c, ventral nerve-cord.
In structure and distribution they closely resemble the
integumentary nephridia o f P h e r e t i m a .
4. THE BLOOD-SUPPLY OF THE NBPHEIDIA.
The blood-supply of the nephridia closely resembles that
found in P h e r e t i m a . The septal nephridia of each segment
receive their blood-supply from the septo-nephridial vessel
which runs along the posterior face of each septum and is given
off as a branch from the ventral vessel as it pierces the septum.
This nephridial vessel should be carefully distinguished from the
commissural vessel which runs along the anterior face of each
ENTERONEPHRIC SYSTEM OP TQNOSCOJLEX
468
septum and receives a large number of branches from the bodywall. Each septal nephridium receives a branch from the septonephridial vessel; this branch (Text-fig. 8) accompanies the
free nephridial canal following the funnel and supplies the
nephridium with blood. The blood from the septal nephridia of
each side of a segment is collected by a large number of small
blood-vessels which unite together to form a large nephridiodorsal vessel (Text-fig. 4), which leaves the dorsal end of each
septal nephridial set and immediately enters the dorsal vessel,
there being thus a pair of nephridio-dorsal vessels in each segment possessing septal nephridia.
The pharyngeal nephridia receive their blood-supply from
the dorsal vessel, while the blood from them is collected by the
supra-intestinal vessel.
The integumentary nephridia are supplied with blood by
the paired branches of ventral vessel in each segment, while the
blood is collected from them by the paired lateral neural vessels
and the commissural vessels.
5. THE MORPHOLOGY AND ORIGIN OP THE SEPTAL
ENTERONEPHRIC NEPHRIDIA.
We have already indicated that the septal nephridial system
of T o n o s c o l e x differs from that of P h e r e t i m a, L a m p i t o ,
o r W o o d w a r d i e l l a i n that the former lacks both the septal
excretory canals and the supra-intestinal excretory ducts. In
the last three genera the terminal excretory canals of the septal
nephridia of a segment become attached to the intersegmental
septum which bears the funnels, but in T o n o s c o l e x the
septum bears only the funnels, while the terminal nephridial
canals run along the posterior border of the nephridial set and
unite together to form the terminal nephridial duct which opens
directly into the intestine in the posterior part of each segment
without having any connexion whatever with the septum, either
in front or behind. Further, there is no connexion between the
pair of terminal nephridial ducts of one segment with that of
the next, and thus the supra-intestinal excretory duct is also
absent. Taking into account these two features, we are justified
in concluding that the septal nephridial system of T o n o s c o l e x
464
KAEM NARAYAN BAHL
is simpler than that of P h e r e t i m a , L a m p i t o , or Woodwar die lla, and may be its precursor.
It is commonly agreed that the primitive condition of the
Oligochaete nephridial system is that in which a pair of exonephric meganephridia exists in each segment, a condition found
i n L u m b r i c u s and in the great majority of species of earthworms. Prom this condition evolution has taken place in two
directions: one in which each meganephridium has apparently
broken up into a large number of micronephridia which are still
exonephric, and the other in which the meganephridia themselves or the micronephridia derived from them open into the
intestine instead of to the exterior. The breaking up of the
meganephridium into micronephridia is illustrated in the development of the nephridia i n O c t o c h a e t u s a s worked out by
Beddard (6), in Megascolides as worked out by Vejdovsky
(1$), and i n l u t y p h o e u s a s worked out by myself.1 This process is also indicated in the nephridia of L a m p i t o d u b i u s
(S), in which I showed that there was a compact cluster of five
micronephridia, each with its own funnel. But, as Stephenson
(11) points out, the line of evolution is not quite clear since we
find many intermediate forms between the mega- and micronephridial conditions, and also many combinations of mega- and
micronephridia.
But of immediate interest is the second line of evolution,
namely, the derivation of the enteronephric from the original
exonephric condition. This may or may not be preceded by the
breaking up of the meganephridia, since in L a m p i t o and
W o o d w a r d i e l l a the meganephridia themselves are enteronephric and coexist with the exonephric micronephridia, while
in P h e r e t i m a and T o n o s c o l e x the septal micronephridia
are enteronephric.
While working out the development of nephridia in P h e r e t i m a (3) and comparing it with that previously worked out in
O c t o c h a e t u s (6), M e g a s c o l i d e s (12), and M a h b e n u s
(7), I made the suggestion that the possible stages in the evolution of the exonephric micronephridia and the enteronephridia
are: (1) the severance of the connexion between the embryonic
* I have not yet published these results, but hope to do so before long.
ENTERONEPHKIC SYSTEM OP TONOSCOLEX
465
septal funnel together with a part of the following duct on the
one hand, and the rudiment of the body of the nephridium of
a meganephridium on the other; (2) the septal funnel together
with a part of the following duct leads to the formation of either
a septal meganephridium or breaks up into a large number of
septal micronephridia, each with its own funnel, while the rudiment of the body of the nephridium, on the other hand, breaks
up into a large number of integumentary micronephridia with
no funnels. This suggestion was based on embryological evidence collected by Bourne, Beddard, Vejdovsky, and myself.
But there is certainly a big gap between the exonephric condition on the one hand and the enteronephric condition on the
other. Stephenson (11) remarked that ' the stages in the evolution of such an enteronephric system as that ofMegascolex
m a u r i t i i and that of P h e r e t i m a are difficult to visualise
when one bears in mind that each successive stage must be at
least physiologically possible, if not also more advantageous
than the previous one'. In the absence of any physiological
data, one is forced to rely entirely on the structural characters
of the nephridial systems. From a purely morphological standpoint, I have no doubt that one such intermediate stage in
evolution is provided by the nephridial system ofTonoscolex,
which is, in fact, the simplest enteronephric system so far known
to us. I believe that an intensive study of the nephridial
systems of other Megascolecine earthworms will probably reveal
other intermediate stages which may enable us to bridge the
gap between exonephric and enteronephric conditions of the
nephridial system.
6. SUMMABY.
1. The 'enteronephric' type of nephridial system, previously
described by the author in P h e r e t i m a , L a m p i t o , and
W o o d w a r d i e l l a ( N e l l o g a s t e r ) , has now been shown to
characterize the genus T o n o s c o l e x as well. It seems that
this type of excretory system is widely distributed in the subfamily Megascolecinae.
2. The nephridia are of three kinds: the enteronephric septal
nephridia, the exonephric integumentary nephridia, and the
466
KARM NARAYAN BAHL
enteroriephric pharyngeal nephridia. There are twenty-four to
thirty septal nephridia in each of those segments where they are
best developed, these nephridia being much larger in size than
the septal ruicronephridia of P h e r e t i m a . The pharyngeal
nephridia form a cylindrical bunch around the oesophagus in
the sixth segment and open into the pharynx in front by a large
number of ducts. The integumentary nephridia are extremely
minute and open singly on the body-wall.
3. The elaborate system of septal excretory canals and supraintestinal ducts characteristic of the septal nephridial systems
of P h e r e t i m a , L a m p i t o , and W o o d w a r d i e l l a , does
not exist in T o n o s c o l e x . The system in T o n o s c o l e x is
therefore much simpler and probably more primitive, and may
represent an intermediate stage between the purely exonephric
rneganephridia o f L u m b r i c u s and the elaborate enteronephric
system of P h e r e t i m a , L a m p i t o , and W o o d w a r d i e l l a .
7. EEFERENCES.
1. Bahl, K. N., 1919.—"New Type of Nephridial System found in . . .
Pheretima", 'Quart. Journ. Micr. Sci.', 64.
2.
1921.—"Blood-Vascular System of Pheretima", ibid., 65.
3.
1922.—"Development of the Enteronephric Type of Nephridial
System in Pheretima", ibid., 66.
4.
1924.—"Enteronephric Type of Nephridial System in Lampito",
ibid., 68.
5.
1926.—"Enteronephric System in Woodwardia, with remarks on
the Nephridia of Lampito dubius", ibid., 70.
6. Beddard, F. E., 1892.—"Embryology of the Oligochaeta", ibid., 33.
7. Bourne, A. G., 1894.—"Development and Anatomy of some Earthworms", ibid., 36.
8. Gates, G. E., 1933.—"Earthworms of Burma. IV", 'Rec. Ind. Mus.',
35.
9. ^—1936.—"Earthworms of Burma. V " ; ibid., 38.
10. Stephenson, J., 1923.—"Oligochaeta", 'Fauna of British India'.
11.
1930.—'Oligochaeta', Oxford.
12. Vejdovsky, F., 1892.—"Entwickl. des Nephridial-Apparates von
Megascolides", 'Arch. Mikr. Anat.', 40.