ON THE NEPHRIDIA. OF THE POLTOHJ1TA.
185
On the Nephridia of the Polychseta.
Fart I,—On Hesione, Tyrrhena, and Nephthys.
By
Edwin S. Ooodrich, B.A.,
Assistant to the Linacre Professor, Oxford.
With Plates 6—9.
THE following observations on Hesione sicula, Dch.
(Fallacia sicula), and Tyrrhena Claparedii, Quatref.,
were begun last year at Naples, and completed at Oxford;
those onNephthys scolopendroides, Dch., andNephthys
cseca, Fabr., were begun at Roscoff, continued at Naples, and
finished here.1 The material was examined in all cases both
fresh and preserved.
HESIONE.
The Ciliated Organ.—When full grown, Hesione
sicula is of about the size and appearance of Peripatus
capensis, and can be easily dissected. On opening up the
worm dorsally, and turning back the cut edges of the bodywall, the segmental dorso-lateral blood-vessels are seen extending outwards from the intestine to large bundles of oblique
vertical muscles attached to the body-wall between each pair
of parapodia. On reaching these bundles the vessels pass
downwards amongst the muscles, and reappear near the median
1
I must express my sincere thanks to the directors and staff Of the Zoological Stations at Naples and at Roscoff for the. kind and helpful way in which
they received me.
186
EDWIN S. GOODRICH.
ventral line, entering the ventral vessel of that side above the
nerve-cord. Dr. Eisig has accurately described and figured
the vascular system of Hesione.1 I can refer the reader to his
paper for further details. It is at the point where the dorsolateral vessel (A of Eisig) first touches the hinder edge of the
oblique muscles that the " ciliated organ." is situated.
Fig. 1 is a careful drawing of an inner view of the left side
of a portion of a worm hardened and cut in half. It shows
the position and relative size of the ciliated organ, c. o., in two
segments about the mid-region of the body in front of the
posterior extremity of the long pharynx, which has been
removed, together with the longitudinal dorsal vessels.
Below are seen the longitudinal ventral vessels (v. v. of
Eisig), into which enter the ventro-lateral vessels, vl. v.
(v. vv. of Eisig). The ciliated organ, of considerable size, is
crescent-shaped, with two free horns or limbs, the internal
one alone being visible in this drawing. The external horn
curls round to the outer side of the bundle of muscles.
A microscopic examination shows that that surface of the
organ which faces backwards and away from the muscle is
furrowed with deep grooves, alternating with sharp-edged
ridges, running transversely to its long axis (figs. 3, 14, and
20). The ridges (fig. 3, c. r.) extend up to the very edge along
the dorsal free margin; ventrally, on the contrary, they stop
short of the edge, leaving a narrow smooth strip beyond. The
whole of this grooved surface is densely covered with fine cilia.
A comparison of three transverse sections (figs. 9,10, and 11),
taken from before backwards, of three sagittal sections (figs.
14, 15, and 16), taken from within outwards, of three frontal
sections (figs. 20, 21, and 22), taken from above downwards,
and of the reconstruction in fig. 2 will make clear the structure
of the ciliated organ. It is free along its dorsal margin; but
for about the middle third of its length the lower edge is
attached to the muscles by a thin septum, formed by a double
layer of peritoneum (figs. 3, 21, and 16, at v. e). About half1
H. Eisig, "Ueber das Vorkommen eines schwimmblaseu ahnliclien Organs
bei Anneliden," 'Mittheil. Zool. St. Neapel,' vol. ii, 1881.
ON THE NEPHRIDIA OF THE POLYCH2ETA.
187
way the ventral edge is produced downwards into a sort ot
hollow groove (figs. 2, 10, 13, 16, v. prol), which becomes
directly continuous with the lip of the nephridial funnel, neph.f.
This point will be dealt with again later. The ventral prolongation of the ciliated organ (uot ciliated at its lowest extremity) lies very near the epidermis lining the iutersegmental
groove, being attached to it by a fold of peritoneum (fig. 13).
The histology of the ciliated organ presents no striking
peculiarity. Like that of Nereis, 1 it is similar throughout,
and shows no trace of glandular structure. No cell walls are
visible ; the cytoplasm is even, but stains more deeply towards
the ciliated surface (fig. 5). Numerous small round or oval
nuclei are situated near the outer surface, chiefly along the base
of each ridge. The anterior surface of the organ, which is
turned towards the muscle, is lined with flat coelomic epithelium (fig. 5, c. ep.).
A pair of ciliated organs occurs in the anterior region of
every segment of the body after the third parapodium. The
organs are largest in the median segments, where they attain
a length of 2 mm. from the end of one horn to that of the
other, and possess from fifty to eighty transverse ridges.
The Nephridium.—The nephridium of Hesione opens
internally into the ccelom by means of a simple funnel, provided with long, stiff, curved cilia (fig. 17). The lips are
reflected all round the aperture, on one side curving round
the dorso-ventral blood-vessel, to which the nephrostome is
attached (figs. 2 and 13). A narrow neck of varying length
leads from the funnel to a wide and somewhat twisted tube
(figs. 2, 16, and 17, neph. t), which in turn becomes narrower
and more convoluted, forming a mass flattened dorso-ventrally,
stretching backwards on the floor of the segment (fig. 2).
The nephridial tube does not branch in its course. Finally it
widens slightly, and runs into the body-wall, through which it
opens by a small pore immediately below the base of the
parapodium (fig. 2, neph. p.).
1
" On a New Organ in the Lycoridea, &c," ' Quart. Journ. Mior. Soi.,'
vol. xxxiv, 1893.
188
EDWIN S. GOODEIOH.
Sections show that, as already mentioned, the lip of the
nephrostome is directly continuous with the ventral prolongation of the ciliated organ. Since this connection is, I believe,
of considerable morphological importance, I have figured it in
detail. A transverse section of the two organs is shown in
fig. 12 (an enlarged view of part of fig. 10), a frontal section
in fig. 22, a sagittal section in fig. 16, and a transverse in
fig. 13. Prom these it will be seen that the ventral prolongation of the ciliated organ is distinguishable from the lip of the
nephridial funnel,—the cells of the former being small, deeply
staining, and not ciliated; those of the latter being ciliated,
less deeply staining, and larger. The convex outer surface of
the large cells forming the funnel can be seen in the living
tissue (fig. 17).
Passing downwards, a section through the wide tube (fig. 4)
shows that the lumen is intra-cellular, and the cilia arise from
various places round the inner surface; cil., fig.6, represents a
section through the convoluted mass, where the lumen is cut
through seven times. The whole organ is, of course, covered
with ccelomic epithelium (c. ep.).
Such nephridia occur in all the segments of the body
occupied by the ciliated organs.
In T y r r h e n a
TVRRHENA.
C l a p a r e d i i the condition of the ciliated
organ and of the nephridium is very much the same as in
Hesione. As in the latter, the nephridial funnel is in direct
continuity with the ventral prolongation of the ciliated organ.
The nephridium is of simpler structure, the tube being very
little convoluted. The ciliated organ itself is in the same
position, but it is less elongated in shape, and its ciliated
surface has fewer ridges.
NEPHTHYS.
T h e C i l i a t e d Organ.—When describing the ciliated
organ of the Ly cor idea1 I stated that I had been unable to
1
Loc. cit.
ON THE NEPHEIDIA OF THE POLYOHJilTA.
189
discover it in Nephthys. At that time I had only been able
to study poorly preserved material. After the examination of
a large number of living and well-preserved worms, I am able
to say that what I had before mistaken for the nephrostome is
really the "ciliated organ."
In fig. 7 is given a careful enlarged drawing of the inner
view of the right side of some segments taken from the midregion of the body of a large hardened specimen of N e p h t h y s
caeca/ and cut in half. The musculature is much more developed and complicated than in Hesione. Thin strands of
muscle stretch from the dorsal surface of the intestine outwards to the body-wall, forming an incomplete longitudinal
oblique septum, obi. sept. Two powerful strap-like longitudinal
muscles lie beneath the intestine on either side of the ventral
blood-vessel, v. v., and give off transverse muscles at every
segment. This ventral band overlies the thick muscular
transverse septa, sept., which extend upwards to the dorsal
longitudinal muscles, d. I. m. Various bundles of vertical
oblique muscles extend outside the main longitudinal muscles.
The dorsal vessel, d. v., gives off a dorso-lateral vessel at
each segment, d.l.v. (dorso-pedal of Jaquet 3 ), which passes
down to the large bundle of oblique muscles, obi. m., corresponding to those described above in Hesione, and on which
are situated the ciliated organs, c. o. Thence the dorso-ventral
blood-vessel (branch a of Jaquet) runs downwards and inwards
to join the ventral subintestinal vessel, v. v. An offshoot of
the ventro-lateral vessel goes to the neural longitudinal vessel
of that side.
The ciliated organ when dissected out resembles somewhat
the shell of Pecten (fig. 19). It is smaller and more rounded
in shape than that of Hesione. The ciliated surface of the
organ faces outwards and forwards; it is raised into about
twenty sharp ridges, alternating with deep grooves, which
1
A specimen from St. Andrew kindly given to me by Dr. W. B.
Benham.
2
M. Jaquet, "Recherches sur le Systeme vasculaire des Ann61ides,"
•Mittheil. Zool. St. Neapel,'vol. vi, 1886.
190
EDWIN S. GOODRICH.
converge towards the ventral and posterior extremity. The
edge of the ridges is extremely thin and jagged (figs. 19 and
26). The clear protoplasm of which it is formed contains a
number of fine refringent granules.
Sections show that the organ is composed of the loose tissue
characteristic of these worms, which has a fibrous appearance
when preserved (figs. 23, 24, and 25, c, o.). The nuclei are
scarce and scattered irregularly.
In Nephthys the position of the ciliated organ is essentially
the same as in Hesione (figs. 7 and 8). Its upper expanded
portion rests on the same dorso-lateral vessel, d. I. v., and its
lower end forms a sort of deep groove or ventral prolongation,
v. prol., running down the body-wall near the intersegmental
groove. There appears to be no communication whatever with
the lumen of the nephridium.
These ciliated organs occur in both sexes throughout the
body in every segment except about the first ten. They are
more fully developed in mature than in young specimens.
The Nephridium.—The nephridium of Nephthys is of
very remarkable structure, representing, indeed, an entirely
new type of Chsetopod nephridium, unlike that of any
member of that group hitherto described.
The small external aperture lies on the ventral surface of
the body below the parapodium, and a little beyond the outer
edge of the ventral longitudinal muscles. Leading from this
nephridiopore (fig. 8, neph. p.) is a narrow canal running
upwards, then obliquely forwards through the muscular
septum, at which point it becomes narrower still (at all events
in sections). Emerging from the septum the nephridial canal
runs inwards and forwards, clinging closely to a blood-vessel
from the body-wall which joins the ventro-lateral vessel.
Ascending the dorso-ventral vessel, and increasing slightly in
diameter, it passes along the inner and anterior edge of the
ciliated organ on the posterior non-ciliated surface. Finally it
emerges on the top of the ciliated organ, where it divides into
free branches forming a sort of plume.
The structure of the minute nephridial tube is simple. The
ON THE NEPHRIDIA OP THE POLYOHKTA.
191
wall is composed of loose fibrous-looking tissue (an appearance probably due to the presence of a large quantity of water
in the living cells). A denser layer surrounds the lumen
(figs. 24 and 25, neph. t.). Nuclei are seen in the wall here
and there, but the lumen is probably intra-cellular. As in
Nereis, the cilia are disposed along one side of the tube only
(occasionally, however, in two opposite rows), and in a nephridium freshly dissected out, the characteristic undulation produced by such an arrangement of cilia is very marked.
The path of the canal as it passes up behind through the
substance of the ciliated organ is shown in fig. 19 by the dotted
line, p. neph. t.y and in the sections drawn in figs. 23, 24, and 25,
neph, t. On reaching the upper edge of the ciliated organ the
tube, with its lumen, divides into three, four, or five branches,
more generally four, which float freely in the coelom. One or
more of the branches usually has a T-shaped extremity, and
the multiplication of the branches (to the maximum number
of five) would appear to take place by the splitting of such a
T-shaped branch to its base. The lumen of the nephridial
canal ends blindly at the tip of each branch (as far as I have
been able to make out). But the chief interest lies in the
minute structure of the branches themselves.
Roughly speaking, each branch may be said to consist of a
double row of cells, with swollen bases containing the nuclei,
enclosing the lumen of the canal (figs. 26, 27, and 28). Each
cell tapers off into a long narrow neck, we., which stretches out
at right angles to the axis of the branch on which the cells are
set. At its distal extremity the neck-like process becomes
slightly swollen, and sharply bent round towards the corresponding cells of the other side. This sort of crook bears at
its extreme end a long narrow tube, tu., which runs down
parallel to the neck towards the nephridial canal at the base of
the cell. Piercing the wall of the canal the delicate tube
leads directly to its lumen, even projecting slightly into it.
A very long and slender flagellum undulates freely in the tube.
Attached by its base at the distal end of the tube, the flagellum
passes downwards and out from the tube into the lumen of the
192
EDWIN S. QOODEIOH.
canalj where it is continued for some length,,/?. Undulations
swiftly pass along the flagellum from its base to the free end
in the canal.
The protoplasm of the tube-bearing cells is very granular,
many of the granules being probably of an excretory nature.
At the distal curved end of the neck are generally seen delicate
protoplasmic projections, often of great length, floating in the
ccelomic fluid, pr. These are not cilia, but appear to be rather
of the nature of amoeboid processes. I have not observed
them moving. The tube itself is rather narrower at its base
than at the end which enters the canal. It is quite straight
as a rule, and oval in section. The wall is composed of a clear
refringent substance, apparently of a cuticular nature, which
resists the action of caustic potash longer than the protoplasmic parts of the cell.
The large oval nuclei (figs. 26—29, n.) have in the fresh
tissue a vacuolated appearance. They are remarkable for the
extreme avidity with which they take up ordinary nuclear
stains, such as carmine or haematoxylin. So pronounced is
this tendency that in a preparation or section they become
deeply stained when the other nuclei are hardly yet affected,
and become intensely overstained by the time the other nuclei
are sufficiently coloured (see fig. 25, term. pi. neph.), A stained
preparation of a whole branch of the terminal plume, somewhat flattened out, is figured (fig. 29), showing the nuclei closely
packed in an irregular double row.
So far as I have observed the tube-bearing cells are never
placed singly, but are ranged in pairs along each side of the
canal (fig. 28). The bases and necks of two adjacent cells are
closely applied to each other along one side to near the distal
extremity, where they diverge to form the terminal crooks.
Although the cells are thus firmly fixed to each other, yet a
clear line of demarcation can always be detected separating
them along the middle line. Occasionally three cells are joined
together, as shown in the middle of the branch in fig. 26.
The nephridia occur throughout the body of the worm, excepting in the first and last few segments.
ON THE NEPHBIDIA OF THE POLYCH2ETA.
193
From the above description it appears that in Nephthya
there is no internal opening to the nephridium, which ends in
a hunch of short blind branches. The current in the lumen
of the tube produced by the flagella of the tube-bearing cells
and the cilia along the canal travels from the terminal branched
organ towards the external pore. It seems obvious, then, that
excretion must take place through the walls of the nephridium
as it does in these organs in the Platyhelmia and Nemertina.
Possibly the thin-walled tubes in which the flagella work act as
osmotic niters, allowing liquid to pass through from the ccelom.
Solid excretory products are more probably conveyed to the
lumen of the canal by the cells themselves. The wall of the
nephridial canal often contains such a number of granules as
to appear of a distinctly brown or greenish hue.
A discussion of the bearing of the facts described above on
the question of the morphology of the nephridium and ciliated
organ is reserved for a second paper, in which it will be shown
that the nephridium of the Grlycerids is built on essentially
the same plan as that of Nephthys, with flagellated " tubebearing" cells.
EXPLANATION OF PLATES 6—9,
Illustrating Mr. Edwin S. Goodrich's paper " On the Nephridia
of the Polychteta."
LIST OF REFE-RENCE LETTEBS.
ac. Aciculum. at. v. e. Attached ventral edge of the ciliated organ, b.w.
Body-wall. e.ep. Ccelomic epithelium, c.f. Ciliated furrow, cil. Cilia.
e.o. Ciliated organ, cml. Ccelom. cosl.corp. Coelomic corpuscles, e.r.
Ciliated ridge, cut. Cuticle, c. te. int. Cut wall of the intestine, d. I. m.
Dorsal longitudinal muscles, dl. v. Dorso-lateral vessel, dp. v. Dorso-pedal
vessel, d.v. Dorsal vessel, do.v. Dorso-ventral vessel, epid. Epidermis.
f.d.e. Free dorsal edge of the ciliated organ, fi. Plagellum. go. Gonads.
int. Intestine, irr.m. Iridescent muscle, l.v.v. Left ventral vessel, lu.
Lumen, m. Muscle, n. Nucleus, n.c. Nerve-cord, ne. Neck-like proVOL. 40, PART 1. NEW SEE.
N
194
EDWIN S. GOODRICH.
cess of the cell, neph.f. Nephridial funnel, neph. p. Nephridial pore.
neph. t. Nephridial tube. obi. m. Oblique muscles, obi. sept. Oblique muscular septum, par. Parapodium. ph. Pharynx, p. neph. t. Path of the
nephridial tube. pr. Protoplasmic process, r. v. v. Right ventral vessel.
sept. Septum, subint.tn. Subintestinal muscular band, term.pl. neph. Terminal plume of the nephridium. tie. Tube, v.l.m. Ventral longitudinal
muscle, v. I. v. Ventro-lateral vessel, v. prol. Ventral prolongation of the
ciliated organ, v. v. Ventral vessel.
PLATE 6.
Figs. 1—6.—Hesione sicula.
FIG. 1.—Enlarged inner view of the right half of two segments from the
mid-region of the body. Drawn from fresh and hardened specimens.
FIG. 2.—Diagrammatic reconstruction of the ciliated organ, the nephridium,
and accompanying blood-vessels, as seen from in front. The cilia are not
represented.
FIG. 3.—Portion of the ciliated organ much enlarged. From the fresh.
X 95, cam.
FIG. 4.—Section through the wide part of the nephridial tube. X 400,cam.
FIG. 5.—Section through the ciliated organ, across the ridges, and showing an accumulation of ccelomic corpuscles, x 400, cam.
FIG. 6.—Section through the narrow and convoluted region of the nephridial
tube, cutting the lumen seven times, x 400, cam.
FIG. 7.—Enlarged inner view of the right half of four segments from the
mid-region of Nephthys ceeca. A portion of the intestine is represented
in front. Drawn from a hardened specimen.
FIG. 8.—Diagrammatic reconstruction of the ciliated organ, nephridium,
and accompanying blood-vessels of Nephthys scolopendroides, as seen
from iu front. The cilia are not represented.
PLATE 7.
Figs. 9—17.—Hesione sicula.
FIGS. 9,10, 11.—Portions of three transverse sections, taken from before
backwards, showing the relation between the ciliated organ and the nephridium.
X 20, cam.
FIG. 12.—More enlarged view of portion of Fig. 10, showing the connection
between the ciliated organ and the nephridial funnel. X 130, cam.
FIG. 13.—Similar figure of a portion of a transverse section from another
series, showing the continuity between the ventral prolongation of the
ciliated organ and the lip of the nephridial funnel. X 400, cam.
ON THE NEPHRIDIA OP THE POLYCHJiTA.
195
FIGS. 14, 15,16.—Portions of three sagittal sections, taken from within
outwards, illustrating the relation of the nephridial funnel to the ciliated
organ. X 250, earn.
FIG. 17.—Enlarged view of the nephridial funnel freshly dissected out.
FIG. 18.—Piece of the dentated edge of a ridge of the ciliated organ of
Nephthys scolopendroides, much enlarged.
FIG. 19.—Enlarged view of the ciliated organ of Nephthys scolopendroides, freshly dissected out. The cilia are not represented.
PLATE 8.
Figs. 20—22, Hesione sicula. Figs. 23—25, Nephthys soolopen<• d r o i d e s .
FIGS. 20, 21, 22.—Portions of three frontal sections, taken from above
downwards, showing the ciliated organ and its ventral connection with the
nephridium. X 40, cam.
FIG. 23.—Portion of a frontal section of a female, showing the ciliated
organs and nephridial tubes. X 100, cam.
FIG. 24.—More enlarged view of the ciliated organ and nephridial tube,
from the same series as Fig. 23. X 400, cam.
FIG. 25.—Portion of a transverse section, showing the nephridial tube cut
twice, the ciliated organ, and a piece of the terminal branch of the nephridium.
X 130, cam.
PLATE 9.
Figs, all of Nephthys scolopendroides.
FIG. 26.—Enlarged view from a fresh specimen of a small piece of the
ciliated organ and a branch of the nephridial plume, showing the tube-bearing
cells.
FIG. 27.—Semi-diagrammatic transverse section of a branch of the terminal
nephridial plume.
FIG. 28.—Semi-diagrammatic longitudinal section of the same.
FIG. 29.—Branch of the nephridial plume stained and somewhat flattened
out. x 500, cam.
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