STBUOTUBB OF EXCRKTOEY ORGANS OP AMPHIOXUS.
493
On the.Structure of the Excretory Organs of
Amphioxus.
Part I.
By
Edwin S. Ooodricli, M.A.,
Follow of Merton College, Oxford.
With Plate 27.
THE excretory organs of Amphioxus were independently
discovered by Weiss and Boveri in the year 1890 (1 and 13).
Weiss described a series of small tubules regularly distributed at the top of each secondary tongue-bar throughout
the region of the pharynx. The tubules are situated, for the
most part, in the wall separating the dorsal ccelom from the
atrial cavity; they lie, therefore, between the cceloniic and
the atrial epithelium, generally separated from the latter by
a network of fine blood-vessels. These kidney tubules open
into the atrium by a pore just opposite the dorsal end of the
secondary gill-bar. Weiss suspected the presence of an
internal opening, but could not find it. The physiological
significance of these organs he established by means of
feeding experiments with carmine and other colouring
matters.
In 1892 Boveri published a detailed and beautifully illustrated account of the excretory organs of Amphioxus (2).
In this paper such a clear and accurate description of the
appearance, general structure, and distribution of the
kidneys is given that little remains to be said on these
VOL, 4 5 , PABT 4.—NEW SERIES.
LL
494
EDWIN S. GOODRICH.
subjects. It will be necessary only to deal in detail here
with certain points on which we differ, and concerning which
I am able to correct Boveri's account in some important
particulars.
The following is a brief statement of Boveri's description
of the excretory organs :—Each consists of a tubule ciliated
internally, and opening into the atrium by a pore near the
top of the secondary gill-bar. In the mid-region of the
pharynx, where the canal is best developed, it extends
forwards to near the origin of the primary bar in front, and
backwards to the primary bar behind, down which it runs
for some little distance. Along its course the tubule is said
to open into the dorsal coelom by means of a varying number
of small funnels; and spread over the ccelomic wall in tlie
neighbourhood of each funnel are many peculiar pin-shaped
cells called " fadenzellen." A long, slender process, starting
from each of the " fadenzellen," is attached to the lip of the
funnel. To quote from Boveri: " Jede Zelle lauft namlich
in einen feinen, aber deutlich doppelt contourirten Faden
aus, der mit den iibrigen Auslaufern der gleichen Zellengruppe
zu einem Trichter hinzieht und in der Miindung desselben
eine Strecke weit verfolgt werden k a n n ; " and further :
" Die Faden ziehen frei d n r c h die Leibeshohle schrag
abw'arts in die Trichteroffnung hinein gegen die laterale
Wand des Canalchens und heften sich mifc ihnen Enden an
die Zellen des Nierenepithels a n " (2).
Some years ago, being struck with the resemblance these
"fadenzellen" bear to the s o l e n o c y t e s I had just discovered in the nephridia of Polychaste worms, I examined the
kidneys of Amphioxus, and came to the conclusion that the
similarity was only superficial, and that Boveri's description
was essentially correct (5, Part III). This winter, however,
whilst occupying the British Association table at the Stazione
Zoologica in Naples, I determined to re-examine these
organs, and I am now able to definitely state that the
"fadenzellen" of Amphioxus are indeed s o l e n o c y t e s oE
typical, t h o u g h somewhat p e c u l i a r s t r u c t u r e (7).
STRUCTURE OF EXCRETORY ORGANS OF AMPHIOXUS.
495
The methods pursued are of the most simple kind, and it
is within the power of any one with living material at hand to
easily verify my results. The Amphioxus is pinned out on
its back in a shallow dish of sea water. The atrium is ripped
up with a needle along the mid-ventral line, and the two
metaplenral folds pinned aside. The exposed pharynx is
then also ripped up with a needle, and portions of the right
or left side of the pharynx cau then be torn out with forceps
Figure of a portion of a section across the gill-bars showing the
excretory canal cut through. A. Atrium. C. Dorsal ccelom.
pb. Primary gill-bar. ' bv. Blood-vessel, ae. Atrial epithelium.
ce. Coelomic epithelium. /. Lumen of the excretory canal, n.
Nucleus of asolenocyte. t. Tube of a solenocyte. Cam. and oil
immersion.
and placed on a slide,1 care being taken to lay the outer
side uppermost. When covered and examined under the
microscope the general structure of the kidney can be quite
easily seen; but the details which I am about to describe
can, unfortunately, only be made out after prolonged study
with the highest powers (-j^- oil immersion and No. 8 eyepiece,
for instance).
1
Such pieces can be stained and mounted, or cut into sections.
496
EDWIN S. GOODKIOH.
Examined in this way, the " fadenzellen " are seen to consist of a small cell-body containing a nucleus. The cell-body
is of somewhat irregular shape, being circular, triangular, or
elongated, and. occasionally drawn out into a process, reminding one of the outer processes present on some Polychsete solenocytes (5). A neck-like region, sometimes
straight, sometimes curved, gradually narrows down and
joins the cell-body to the distal extremity of the "thread,"
which is, in fact, a slender hollow tube of great length (Fig.
in text, p. 495, and PL 27, figs. 1 and 4).
The longest tubes belong, of course, to those cells which
are situated furthest from the renal canal; they reach sometimes a length of 90 [i, or nearly T\j- mm. The wall of the
tube does not appear to be as stiff as in the case of PolychsBte solenocytes; and under the pressure of the coverglass it is often much curved. In the living animal, however,
I believe the tubes are always straight. The proximal end
pierces the wall of the excretory duct, and projects a little
into the lumen of the canal (figs. 3 and 4). A longflagellum,
attached at its base to the cell placed at the end of the tube,
works rapidly down the tube and far into the excretory canal
(figs. 3 and4).!
BoAreri (influenced perhaps by the current dogma, which
affirms, in spite of all evidence to the contrary, firstly, that all
tubular excretory organs are of homologous nephridial nature ;
and secondly, that nephridia are derived from the coclom,
and generally, if not always, open into it) described open
coclomic funnels in Amphioxus, as already mentioned above.
Neither in the living nor in sections of preserved specimens
have I been able to detect any direct communication between
the excretory canal and the ccelom. The branches of the
tubule may be very numerous, of considerable length, and
may themselves divide, but they end b l i n d l y (fig. 1). It
is to these blind ends that the tubes of the solenocytes converge, and here the wall of the canal is less loaded with
1
I was fortunately able to demonstrate the correctness of these observations to Prof. Boven himself at the zoological station in Naples.
STRUCTURE OF KXCRETOBY ORGANS OP AMPHIOXUS.
497
excretory granules, and thinner than elsewhere. The nuclei
also, which are so numerous in the other regions of the
tubule, are not preseut just in those parts where the
solenocytes traverse its wall (Fig. in. text, p. 495).
Briefly to summarise the observations described above, it
may be stated that in Amphioxus there is a series of
excretory tubules opening into the atrium, but not into the
ccelom, and provided at their blind internal ends with a large
number of solenocytes. These tubules are situated " morphologically" outside the ccelom, being covered with ccelomic epithelium ; the solenocytes alone push through into the
coeloinic cavity.
At each end of the pharynx the excretory organs dwindle
in size, as already pointed out by Boveri. The tubule in
these regions becomes shorter, the branches become reduced
in size, or are not developed at all, and the number of solenocytes becomes much less. This is also the case throughout
the pharyngeal region of small specimens. Fig. 3 represents a small portion of the kidney of a young Amphioxus
31 mm. long. Not only are the solenocytes not so crowded,
but the average length of the tubes is less than in fullgrown individuals (fig. 1).
That the segmental kidneys of Amphioxus really fulfil an
excretory function has been amply demonstrated by Weiss
;md Boveri; but the part played by the solenocytes themselves is less clear. Boveri, who remarked that their distribution over the wall of the cceleni coincides with that of a
network of blood-vessels, concluded that the "fadenzellen "
were concerned in the elimination of waste products from the
blood : " diese Zellen dem Chemismus der Excretion dieneu."
He could not find that they took up colouring matters—a
result which agrees with my own observations on the solenocytes of PolychEetes (5, Part II). It seems to me probable,
therefore, that, as I have already suggested for worms
(5, Part II), the solenocytes are concerned chiefly with the
elimination of fluid substances which can pass by osmosis
through the thin walls of the tube, well adapted for such a
498
NDWIN H. GOODftlCfl.
purpose. The flagellum would serve to propel the fluid into
the excretory canal and thence to the exterior. That a considerable amount of fluid could pass through the tubes becomes evident when we remember that in a full-grown
Amphioxus there are, roughly speaking, 100 kidneys on each
side, or some 200 in all. Now each of these has, on an average,
about 500 solenocytes—to take a low estimate,—making the
number of solenocytes in the whole animal roughly 100,000.
The average length of the solenocyte tube may be taken at
Y$ mm., or 50 fi. There are, therefore, about 5 metres of this
thin-walled tube in each full-grown individual, representing
no inconsiderable area for osmotic exchange in an animal of
such small bulk.
Conclusion.—I do not propose in this paper to enter
into a detailed discussion of the homology and taxonomic
importance of the segmental kidneys of Amphioxus, but
the extraordinary resemblance they bear to the nephridia I
have described in the Nephthyidas, G-lyceridse, and Phyllodocidee must be insisted upon. For the purpose of comparison, figures are given of the inner end of the nephridium
of Phyllodoce P a r e t t i (figs. 2 and 5), which, of all the
Polychsetes I have studied, most closely resembles Amphioxus
in the structure of its renal organ. The nephridium of this
beautiful Phyllodocid is large enough to be dissected out.
It is then seen to end in the ccelom in a bunch of blind
branches, which are provided with a number of solenocytes
arranged like the ribs of a fan. The tubes are in double
rows, while the cell-bodies of the two rows of solenocytes are
closely packed together, and wedged in alternately.1 In
fig. 5 I have given a diagrammatic representation of the
extremity of a branch of the nephridium, to compare with
the similar diagrammatic figure of a small portion of the
kidney of Amphioxus (fig. 4). These figures bring out
clearly the wonderful likeness of the two organs.
1
I estimate the number, of solenocytes in a Phyllodoce Paretti roughly
at 600,000, there be ing about 1500 to each nephridium, and some 200
segments.
STRUCTURE OF EXCRETORY ORGANS OF AMPHIOXUS. 490
It results from these observations, as I have already pointed
out in a preliminary paper (7), that in their segmental
arrangement, in their function, and in their histological s t r u c t u r e , t h e excretory o r g a n s of Amphioxus and the nephridia of Phyllodoce are in all
essentials identical.
Before committing ourselves to new theories, something
must be known of the development of these organs; but,
considering how remarkably close is the agreement between
the two, it seems more than probable that they are homologous
structures. If two such excretory organs as the solenocytebearing nephridia of Phyllodoce, and the solenocyte-bearing
kidneys of Amphioxus, could be shown to have been independently involved, we should have to give up structural
resemblance as a guide to homology.1 But there seems to be
no danger of our being driven to abandon the problem as
yet, and all we need assume is, not that the vertebrates have
been evolved from the Polychastes, but that the remote
common ancestor of these now highly differentiated phyla was
of more elaborate structure than most authors have been hitherto inclined to suppose. We must assume that it possessed not
only paired coelomic (genital) sacs and ccelomostomes (6 and
8), but also nephridia, whose blind internal end was provided
with solenocytes.2
We may conclude provisionally that
now, for the first time, true nephridia have been shown to
occur in the vertebrate phylum; and further, we may hope
to trace in the vertebrates the same two series of organs—
the nephridium and the ccelomostome—which I have elsewhere
1
The only case which seems to me at all comparable is that of the
nematocysts in Ccelenterates, Planarians, and Molluscs.
2
This is all the more easy to believe since I have found these cells at the
blind inner end of the nephridium of the larva of Phoronis (it will be remembered that Masterman observed cells similar to Boveri's " fadenzellen" in
Actinotrocha [9], and they have been described by Wagener [12]); and
"flame-cells" very like solenocytes have been described in Nemertines by
Burger (4), in Molluscs by Meisenheimer (10), and in .Rotifers by
Shephard (11). Also the "flame-cells" of Platyhelminths and Entoproctous
Polyzoa are probably of the same nature (6).
500
EDWIN S. GOODRICH.
endeavoured to prove exist in the majority of coelomates
(6, and 5, Part III).
It follows, from the conclusion provisionally adopted above,
that the many theories which have been built on the assumed
homology between the separate segmental excretory organs
of Amphioxus and the renal organs of coelomic origin of the
higher vertebrates must be allowed to drop for the present.
These latter organs (pronephros, niesonephros, and genital
ducts) have nothing to do with nephridia, and appear to
belong undoubtedly to the category of ccelomostoraes (5,
Part III, and 8). Their homologues in Amphioxus may be
sought in the opening of the larval " head cavities," in the
"brown funnels" described by Lankester, and in the segmental
genital sacs as already suggested by Boveri (3). It is not
impossible, however, that true nephridia may yet be found at
some stage of development amongst the craniate vertebrates,
and more especially in the Cyclostomes.1
L I S T OP R E F E E E N C E S .
1. BOVERI, T.—" Ueber die Niere des Amphioxus," 'Munch, med. Wochenschrift,' No. 26, 1890.
2. BOVEKI, T.—"Die Nierencanalchen des Ampliioxus," ' Zool. Jalnb.,'
vol. v, 1892.
3. BOVEKI, T.—"Ueber die Bilduugslate der Gesclikchtsdruseii, etc.,"
' Anat. Anzeig.,' vol. vii, 1892.
4. BuKGbB, O.—" Die Nemertinen," ' fauna und flora des Golfes von
Neapcl,' vol. xxii, 1895.
5. GOODBICH, E. S.—"On the Nephridia of the Polychseta," pt. i, 'Quart.
Journ. Micr. Sci.,' vol. xl, 1897; pt. ii, ibid., vol. xli, 1898; pt. iii,
ibid., vol. xliii, 1900.
6. GOODUICH, E. S.—" On the Ccelom, Genital Ducts, and Nephridia,"
'Quart. Journ. Micr. Sci.,' vol. xxxvii, 1895.
7. GOODRICH, E. S.—"On the Excretory Organs of Amphioxus," 'Proc.
Roy. Soc.,' 1902.
1
I fully expect that nephridia will some day be found in the Enteropneusta
and even in the Tunicata.
STBUPTUKE OF EXCRETORY ORGANS OP AMPHIOXUS. 501
8. L\NKESTER, E. RAY.—"The Enterocoela and Hie Coelomocoela," 'Treatise
on Zoology,' pt. 2, 1900.
9. MASTERMAN, A. T.—"On the Diplochorda," ' Quart. Journ. Micr. Sci.,'
vol. xl, 1897.
10. MEISENHEIMEII, J.—"Entwickl. von D reissensia poly morpha, Pall,"
' Zeit. f. wiss. Zool.,' vol. lxix, 1901.
11. SHEPHARD, J.—"On the Structure of the Vibratile Tags or Flame-cell
m Rotilera," ' Pioc. Roy. Soc. Victoria,' vol. xi, 1899.
12. WAGENER, K.—"Ueber den Bau der A c t i n o t r o c h a branchiata,"
• Archiv f. Anat. und Phys.,' 1847.
13. WEISS, E.—"Excretory Tubules in Amphioxus lanceolatus,"'O w uait.
Journ. Micr. Sci.,' vol. xxxi, 1890.
EXPLANATION OF PLATE 27,
Illustrating EDWIN S. GOODRICH'S paper " On the Structure
of the Excretory Organs of Amphioxus."
FIG. 1.—Enlarged view of an excretory organ of Amphioxus, drawn from
the living.
FIG. 2.—Enlarged view of the terminal tuft ot the nephridium of Phyllodoce P a r e t t i , drawn from the living.
FIG. 3.—A small portion of the excreloiy canal of a young Amphioxus,
with its solenocytes, from the living. Cam. T ^ oil immeision, oc. 8.
FIGS. 4 and 5.—Semi-diagrammatic views of portions of the excretory
organs of Amphioxus and Phyllodoce P a r e t t i , from living and preserved
specimens.