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M19 TRANSACTIONS
1290
rid eos OF THE
ROYAL SOCIETY OF EDINBURGH.
+ VOL. XXXV.—PART III.—(No. 19.)
ON THE DEVELOPMENT AND LIFE HISTORIES OF THE
» TELEOSTEAN FOOD- AND OTHER FISHES.
[Piates I. tro XXVIII. ] a at
BY
Proressor W. C. M‘INTOSH, F.R.S.; anp E. E. PRINCE, BA.,
ST ANDREWS MARINE LABORATORY.
EDINBURGH:
PUBLISHED BY ROBERT GRANT & SON, 107 PRINCES STREET,
AND WILLIAMS & NORGATE, 14 HENRIETTA STREET, COVENT GARDEN, LONDON.
5/2/90. MDCCOXC.
Price Two Guineas.
L We ee i =
MIS ot
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Fushe>
XIX.—On the Development and Life-Histories of the Teleostean Food- and other Fishes. /
By Professor W. C. M‘Intosu, F.R.S., and E. E. Prince, B.A., St Andrews Marine
Laboratory.* (Plates I. to XXVIII.)
(Read 18th June 1888.)
For Table of Contents see end of paper.
I. Generat REMARKS.
Until very recently existing information concerning the eggs and oviposition of
British fishes, and more especially marine fishes, was of the most fragmentary
character. In the standard works upon Ichthyology, such as Owen’s Anatomy of
Vertebrates (vol. i. Fishes), it is comprised in a few vague sentences ; while the original
papers published by British ichthyologists are not numerous, and refer, for the most
part, to fresh-water species. Within the last few years, however, attention has been
more systematically directed to the subject, and the enlightened views of the late Royal
Commission on Trawling, and more especially of its chairman, the late Earu or
Datnovstr, has given a fresh impetus to the study of the development and life-history
of our food-fishes, as preliminary to a thorough investigation of their habits, food, so-
called migrations, and general life-history.
The following paper comprises the first results of our recent work at the St Andrews
Marine Laboratory.
Though much has been done by foreign observers of late years in regard to the
development of marine fishes, yet the cod and herring only, amongst those conspicuous
by their economic value in this country, have been specially dealt with.
It was therefore necessary, even at the risk of repeating some observations already
known to science, to examine as thoroughly as possible the ovarian growth, oviposition,
hatching, and development of such of the important white fishes as could be obtained,
and to fill up the gaps in our knowledge of the period between the escape of the embryo
from the egg, and the young, though advanced, forms known to naturalists and fishermen.
* The authors have to acknowledge the courtesy of the Fishery Board for Scotland, under whose auspices the work
has been accomplished, and to whom all credit is given. Grants from the Royal Society (Government Grant) and
from the British Association have also been of great service in regard to assistance and apparatus. To Dr ScHarrr,
B.Sc., now of the Museum of the Royal College of Science, Dublin, for valued aid of various kinds in 1886, and to
Dr J. Witson of St Andrews, for help in making sections, our acknowledgments are also due. When cruising in the
Fishery Board tender “Garland,” Mr W. L. Canperwoop, B.Sc., and Mr H. E. Duruam, B.A., also kindly gave
assistance. It may further be stated that the first part of the paper, containing the development of the food-fishes and
their early larval condition, was mainly the work of Mr Prince; while the account of the post-larval stages, the
development of Anarrhichas and the salmon, was the work of Dr M‘Inrosa. Mr Prince added further notes on the
structure of the later stages of other forms.
VOL. XXXV. PART III, (NO. 19). eG
666 PROFESSOR W. C. M‘INTOSH AND MR E, E. PRINCE ON
The ova of about forty British fishes have been examined, and in most cases the
development of the young before and after leaving the egg, as far as possible, followed.
The period over which the special observations extended commenced with the work for
H.M. Trawling Commission in 1884, when the talented chairman (Lorp Datuouste) placed
every encouragement (personal and administrative), and all the facilities in his power
for pursuing the subject as thoroughly as time would permit. The experience of former
years at St Andrews and elsewhere has been made available, especially in regard to the
growth of marine fishes, and to the structural features in the later stages of the salmon.
The ova examined at St Andrews may be conveniently arranged in two divisions,
viz., Pelagic or floating eggs, and Non-Pelagic or demersal eggs.
Under the former head twenty-three species may be grouped, viz., Long-Rough Dab,
Turbot, Plaice, Lemon-Dab, Craig-Fluke, Common Dab, Common Flounder, Sole, Miiller’s
Topknot, Ling, Five-bearded Rockling, Cod, Haddock, Bib, Whiting, Poor Cod, Green
Cod, Pollack, Frog-fish, Skulpin, Lesser Weever, Sprat, and Grey Gurnard. Besides the
foregoing, the Common Eel and the Conger have been examined; but their pelagic or
demersal character has not been finally determined.
The non-pelagic ova include at least fourteen species, besides a few doubtful forms of
which the ovarian eggs alone have been under consideration. This (demersal) group
embraces the Herring, Smelt, Salmon, Trout, Bimaculated Sucker, Wolf-fish, Shanny,
Viviparous Blenny, Montagu’s Sucker, Lump-sucker, Goby, Armed Bullhead, Cottus,
Fifteen-spined and Three-spined Stickleback, Sea Bream, Gunnel, &c., besides the
Cyclostome—Myzxine. Amongst the doubtful eggs are those of Yarrell’s Blenny and the
Sand-Eel (Ammodytes tobianus).
Il. Tae Mature Ovum.
General Features.
The mature ovum of osseous fishes is generally of comparatively
small size, spherical in form, and more or less translucent. Two parts may be distin-
guished, viz., a protective external capsule (PI. I. figs. 1—4, 27"), and a contained vitelline
mass (y), the latter consisting of a globe of food-yolk, with interfused germinal matter.
Upon being placed in water, the ova of some species float near the surface and throughout
the water ; these, as already pointed out, form the pelagic group; while in other species the
eggs sink to the bottom, and form the second group, viz., the demersal or non-floating eggs.
The first group exhibit in a striking way the feature characteristic of pelagic structures,
viz., a colourless translucency ; while the second or demersal group are less delicate in
appearance, and often tinted ina marked manner. Thus the freshly extruded ova of
Cyclopterus lumpus are of a brilliant purplish rose, or a subdued green or yellow tint,
which soon, however, fades away, and the eggs become more translucent. The ova of
the salmon, by their rich orange colour, afford a familiar example of tinted demersal eggs ;
while those of many species of Stickleback (e.g., Gastrosteus spinachia) are of a trans-
parent amber-tint. Such coloration, as just noted, like the whitish opacity of the ovarian
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 667
ovum, may be transient and give place after extrusion to an imperfect transparency.
The ova of Ammodytes tobianus present a marked example of this, for while contained in
the ovary they are of a bright orange colour—the ovaries on this account forming a
bilobed orange-tinted mass in the abdomen of the nearly ripe female, but the eggs when
ready for extrusion, and indeed while passing to the oviducal aperture, would appear to
become colourless. Pelagic eggs usually float loosely together or singly, and do not
adhere to each other, save in certain noticeable instances, of which Lophius piscatorius is
an interesting example. Acassiz first described the floating eggs of this familiar fish as
adhering together in long bands near the surface (No. 1, p. 280), but even in this case
eggs may become detached and float free (No. 2, p. 16). Professor E. van BENEDEN
describes some minute isolated and agglutinated eggs which he was not able to deter-
mine, but believed that they belonged to a species of Lota, and he supposed that, after
being deposited in a mass, they “remain for some time adherent one to another, and
afterwards separate, and then float free from all adhesion, on the surface of the sea”
(No. 25, p. 41). This surmise is perhaps questionable, and VAN BENEDEN, indeed, himself
adds—* I never saw the eggs become detached from one another” (p. 42); and they prob-
ably, therefore, belonged to two different species. Eggs similar to those of E. van BENEDEN
were obtained by Haeckel on the coast of Corsica. They formed agglutinated masses of
various volume and form—the ova being in fact imbedded in a gelatinous substance.*
Pelagic ova, if ever adherent, possibly may soon become detached, but eggs deposited on
the sea-bottom, in masses, adhere together most strongly, though in an advanced stage
they are less firmly united, this loss of adherent property in such a form as Cyclopterus
lumpus taking place only after the lapse of a considerable interval, often many weeks,
when the capsule becomes softened, and changes occur in its pliysical character, probably
to facilitate the liberation of the contained embryo. Usually, however, these eggs cling
together if undisturbed (even when dead) for long periods. The adhesive character
which Von Baer was the first to notice in certain Cyprinoids* is due to a mucilaginous
ovarian secretion bathing the eggs, and acting as a lubricant during extrusion. On
exposure to water, it has the property of hardening, as in many similar instances both in
vertebrates and invertebrates ; and, in the case of adherent eggs, it acts as a cement, bind-
ing them together so firmly that they can be separated only with difficulty ; and the points
where the adjacent eggs were in contact show prominent scars or facets after separation
(Pl. I. figs. 2, 3, and 4, x).
A marked translucency of both capsule and egg-contents usually indicates the healthy
* Mr Rarrray has recently submitted to us examples of pelagic ova from the west coast of Africa, which are also
bound in masses by a connecting substance converted by reagents and alcohol into a thread-like meshwork. Threads
of a like character were noticed in some ova sent by M. Mrtier many years ago to the French Academy of Sciences.
They were evidently demersal eggs, for they were attached to a wooden barrel hoop by the elastic threads, the latter
forming a felted meshwork, which Miter supposed to be produced by the parent-fish (No. 110, p. 342). They were
procured in 14° 15’ N. lat. and 20° 30'W. long. The eggs Mr Rarrray kindly sent to St Andrews were obtained (in the
s.s. “ Buccaneer ” Expedition) in lat. 1° 17’ 6” N., long. 13° 54’ 4” W. Vide Remarks on these by Mr J. T. Cunntncuam,
Trans. Roy. Soc, Edin., xxxiii. i. p. 108, pl. vii. fig. 7.
+ Untersuchungen iiber die Entwickelungsgeschichte der Fische, Leipzig, 1835, p. 7.
665 PROFESSOR W. C., M‘INTOSH AND MR E. E. PRINCE ON
living egg, especially in the case of pelagic ova, and also to a certain extent in demersal
forms. ‘This translucency is due to the disappearance of the granules in the yolk of the
ovarian egg when ripe. Sometimes, however, eggs which are not perfectly mature, z.e.,
lack the translucency of the ripe ovum, may yet be fertilised, and their embryos in due
time liberated. This was frequently the case with imperfectly ripe eggs of T. gurnardus,
which, though presenting slight opacity, were successfully hatched. Occasionally eggs of
the species just named exhibit a remarkable pinkish or reddish coloration, the oil-globule
being of a dark tint (Pl. XVI. fig. 10). The cause or meaning of this abnormal appear-
ance is undecided; the eggs, of course, were not fertilised, and did not develop ; indeed,
this coloration has only been seen in dead eggs. Pelagic eggs, when dead or unhealthy,
show a great increase in the perivitelline space, and sink to the bottom of the tanks.
Sometimes living eggs, from various causes, such as a change in the specific gravity of
the water, sink, this being frequently the case with 7. gurnardus ; yet when the water
is violently stirred, or when removed from still water for examination, and then emptied
into the tanks, they again often assume their buoyancy. This may be due to the dis-
engagement of particles of foreign matter, such as sand, though this is not always
evident. The eggs of Molva vulgaris (PI. I. fig. 10) are less buoyant than some other
Gadoids, e.g., Gadus morrhua and G. aglefinus, and sometimes, though living, sink to
the bottom in quiescent water, yet successfully develop. The ova of the ling are indeed
more delicate, and more susceptible to unfavourable conditions than those of the cod and
haddock. The addition of spirit to a vessel containing them causes them to rush to the
side of the vessel, and cling to it with tenacity. The hardy character of certain pelagic
eggs and their vitality was shown in many cases at the Laboratory. No difficulty was
found in developing eggs fertilised at sea and conveyed long distances, in some cases after
travelling in earthenware jars for three or four days. Eggs of the cod contained in such
jars, three-fourths filled with sea-water, reached the Laboratory on the fourth day after
fertilisation, and though most of the eggs had sunk to the bottom, and the water was
offensive with putrid matter
Infusoria, Bacteria, and Spirilla being abundant, yet many
of the eggs still floated at the surface, and the hearts of the embryos pulsated regularly.
The effect of cold is to retard development, but is not detrimental unless extreme. In
one instance a series of the eggs of the haddock were floating buoyantly in the tanks at
6 p.M., but next morning the glass vessel was covered with a coating of ice, on breaking
which most of the eggs fell to the bottom, and in these the yolk and germinal area were
found to be much shrunken and corrugated, leaving a wide space round the vitelline
mass. A few only survived, these having apparently remained under the trickle of the
supply pipe.* That pelagic eggs float in sea water, while they sink in fresh water, or in
sea water having an admixture of fresh, Professor Barrp has shown to be due to the
fact that their specific gravity is about 1:020 or 1:025.t
* Vide Nature, June 1886.
+ Of this floating property, the oldest fishermen, Barrp adds, had not the slightest idea ; they thought “that the
females deposited their eggs on the rocks, where they were visited and impregnated by the males... .. . They had
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 669
Pexacic Ova.
General Remarks.—The pelagic nature of the ova of so large a number of valuable
food-fishes removes them altogether from many of the vicissitudes which befall demersal
egos, Their transparent glassy nature, minute size, and enormous abundance, sufficiently
provide for their safety and the increase of the species. Pelagic ova are by no means
common in the stomachs of fishes, while ova deposited on the bottom (e.g., those of
Cyclopterus, Cottus, and Clupea harengus) are eaten by many fishes with great avidity,
yet the numbers of one of these at least are, so far as can be made out, by no means
seriously affected. How much more surely, then, is the multiplication of those with
pelagic ova provided for? As a rule, they are deep enough to escape the vicissitudes of
the immediate surface, and in our country are seldom stranded on the beach in numbers
sufficient to attract attention.* The larvee which escape from them are also minute and
translucent, and thus are less prone to attract the notice of predatory marine forms ; more-
over, they soon become very active, while their purely pelagic life gives them a vast area
for their safe development.
The contrast between such types and the condition, for instance, in Cottus, is marked.
In the latter the ova are deposited between tide-marks in masses, and are often devoured
by other fishes, and it may be by predatory birds and mollusks. The comparatively large
young are conspicuous objects, and can only escape by keeping within reach of tangles
and other sea-weeds, a constant reduction of their numbers taking place, notwithstanding
their defensive armature, during the somewhat slow growth to the adult condition. It is
possible, indeed, that though the egg-capsules in Cottws are much denser, and the embryos
larger and more highly developed than in the cod, a much greater number of the latter
proportionally reach maturity than in the case of the former.
On the eastern shores pelagic ova begin to appear at the end of February, though
there is no reason why some should not be found earlier, as Dr J. Murray tells us they
are on the west coast (Clyde district), and a kind of succession of those of different species
oceurs throughout the spring, summer, and autumn. Amongst the earliest are the ova
of the plaice, Wotella, and the large egg with the spacious perivitelline space, the larval
form issuing from which is described subsequently. Those of the Gadoids, such as the cod,
haddock, and whiting, next appear, and also those of the flounder and dab, while towards
the end of the month the eggs of the gurnard are also captured. April is characterised
by the abundance of pelagic ova, the maximum perhaps being attained towards the latter
part of the month, when the ova of the spratt and other forms swell the list. As an
at times noticed the little transparent globular bodies in the water; but it never occurred to them that they were the
eggs of any fish. They may be found at the surface in common with the eggs of pollack, haddock, and probably other
species of the cod family, when the sea is smooth, but when the water becomes rough they are carried to a depth of
several fathoms by the current, though the tendency is to remain near the surface” (No. 8, p. 715).
* G. O. Sars found, however, that they were so at Lofoten.
+ HeEnseN first noticed the pelagic ova of the sprat, and his observation has been corroborated by J. T. Cunnino-
HAM and ourselves. Other Clupeoids, as shown by RaFFaxg xe, also have pelagic eggs.
670 PROFESSOR W. C. M'INTOSH AND MR E. E. PRINCE ON
example of the duration of a particular kind of ova in the bay, those of the gurnard may
be taken ; for, appearing in April, they continue throughout May, June, and even part of
July, being very abundant in June. It is clear, therefore, that with rapid growth, the
differences in size between the post-larval forms produced from the ova at the extremities
of the period must be considerable.
Distribution.—Nothing was more striking, in the investigations in connection with
H.M. Trawling Commission in 1884, than the abundance of the pelagic ova in the upper
regions of the water, and indeed throughout it. They are not usually found quite at the
surface, but as soon as the tow-net is sunk a fathom or two, they occur almost in every
haul on suitable ground. Though on the banks frequented by the cod, haddock, and
whiting, these pelagic ova are in greatest profusion at the breeding season, yet they are
met with during many months from January till late in autumn, a continuous discharge
of ova taking place from one or other group having this habit. Moreover, it is clear that
the provision by which only a portion of the ovary in most fishes with pelagic eggs becomes
ripe at a given time, greatly prolongs the spawning period, and tends to intensify the
feature just mentioned. It is possible indeed to form an estimate of the number of
spawning fishes in a given district by the abundance of pelagic ova, or the contrary. It
is only necessary to illustrate this by reference to the surface of Smith Bank, off the coast
of Caithness, where the ova and embryos were in vast numbers in the beginning of April,
so much so that the area resembled a vast hatching-pond, even the sea-birds feeding in
long lines on such as the currents swept to the surface. The same feature was shortly
afterwards noticed, along with Lorp Datnovustn, off the Island of May, though both eggs
and embryos were less numerous than in the former case.
Again, recent investigations with the trawl-like tow-net on the bottom show that a
vast number of pelagic ova, such as those of the cod, whiting, rockling, sole, flounder,
gurnard, sprat, and other forms, are to be found there—when the large mid-water net and
the surface-net are nearly devoid of them. Whether this aggregation of ova is due to
cold at the surface or to the effect of currents has not yet been determined, but it is a
feature of great interest.
Sizes of Ova.*—As an example of the variety of pelagic ova common to the sea
beyond the Firth of Forth in April, the following measurements from spirit-preparations
are interesting. The ova were collected by the tow-net (sunk a fathom or thereabout)
in the usual manner, and then placed in strong spirit, which caused considerable contraction,
probably from ‘1 to °15. A very few measured 0216 of an inch, others had a diameter
of 023, ‘03, 033 (probably Motella), -035, 0866, °04, ‘043, *045, ‘046, -05, the largest
number ranging over the area covered by the last five, which probably included cod,
haddock, ling, &e., 056, and a very few at ‘058 and ‘083 of an inch. A little variation
appears to occur in each species. The average in fresh specimens of the haddock is
‘056, the blastodise being °033; plaice, °0716; ling, ‘0916, and the oil-globule, -031;
* A table of sizes of ova from RarraEte is given by one of us, in a Report on the Pelagic Fauna of St Andrews
Bay, Seventh Annual Report, Fishery Board for Scotland, 1889.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 671
cod, °06; grey gurnard, 055, and oil-globule, ‘0116; lemon dab, 053; flounder, -038 ;
common dab, ‘033; skulpin, ‘025 to 030; sprat, ‘044 in long diameter, ‘039 in short
diameter ; sole, 045.
Tue Eac-CapsuLrk, WITH REMARKS ON THE REPRODUCTIVE ORGANS AND
PERIOD OF SPAWNING.
Few points in the constitution of the ovum afford more matter for controversy than
the origin and significance of the external protective membrane.
The twofold division of egg-membranes, due to Prof. E. van Brnepren (No. 24,
pp- 228-30), and founded upon their derivation, is both natural and convenient, viz., (1)
membranes differentiated from the cortex of the egg-mass itself; (2) membranes formed
ab extra by the cells of the ovarian follicle. It is generally agreed that the egg-capsule
of Teleostean ova belongs to the first division. CUNNINGHAM, however, does not adopt
this view, and the “ vitelline membrane” of his earlier papers he now considers to
be an extra-vitelline product—developed by the cells of the follicular epithelium
(No. 47). Other protective structures may lie outside the egg-capsule proper, such as
the mucous layer in Perca fluviatilis, the gelatinous matter surrounding the floating ova
of Lophius piscatorius, and others, but they are probably ovarian, oviducal, or other
secretions, and do not belong to the ovum proper. Further, it seems most in accord
variously
with present results to regard the external capsule as a single membrane
styled Eikapsel (MULiEr, His, &c.), Eihaut (Kuprrer), Chorion (LEREBOULLET), Ectosac
(OwEN), outer yelk-sac (Ransom), and zona radiata (WALDEYER). G. Brook, again,
describes in Trachinus a thin membrane (his vitelline membrane) outside the zona.
Such has not been seen in any of our pelagic eggs. It is generally hyaline, tough, and
slightly resilient, and varies in thickness in different species—thus approximately in
Anarrhichas lupus, it is 00143 to 00162 in. Gadus merlangus, it 1s 000310 in.
Gastrosteus spinachia, ,, “0015 4 Pleuronectes flesus, rh 000125 ,,
Gadus morrhua, y 000312 ,, | A limanda, ,, 000104 ,,
» eaeglefinus, “ 000440 |) = Trigla gurnardus, f 000333 |,
In pelagic ova it is so exceedingly thin and translucent that the developmental
changes in the germ are visible through the capsule,* yet in demersal ova it is not only
denser, but presents in many species marked structural features, such as projecting knobs,
filamentous processes, reticulations, and the like, all of which, however, must be looked
upon merely as modifications of the single capsular membrane—the zona radiata. It is
very thin and transparent in the sprat, the egg of which generally shrivels when put in
spirit. The zona usually presents laminze, which Sars observed and counted in Gadus
morrhua ; but such does not imply the existence of separate layers, for chitinous structures
of this kind often show a stratified condition. Ryprr could only make out the lamin
*In undeveloped and dying eggs the growing opacity of the vitelline mass is readily seen. This opacity of the
egg-contents ANDRE wrongly attributes to the capsule itself, which he says becomes opaque (No. 4, p. 197).
672 PROFESSOR W. C. M‘INTOSH AND MR E. E, PRINCE ON
in Gadus morrhua after treatment with osmic acid, but in both that and other species
they were observed at the St Andrews Laboratory without preparation. As the time
approaches for hatching, the capsule (¢.g., in Gadus aglefinus) often breaks up into
flakes like the translucent chitinous secretions (tubes) of Annelids, The continued action
of water and other causes seems to produce this physical change, so that the embryo is
more readily extruded.
We shall glance first at a few of the prominent features of demersal ova—the two
most obvious points as compared with pelagic eggs being (1) the greater density of the
zona radiata ; (2) the tendency to adhere together in masses by reason of the peculiar
secretion which issues from the oviduct along with the ova. One of us has pointed out,*
that in adhering together, eggs such as those of Cottus and Cyclopterus (vide Pl. 1.
figs. 1-4) do so by limited areas of their surface, z.e., by facets, and thus the mass of
ova is traversed by an intricate system of channels, which ensures more perfect aeration
in the circumstances in which they are placed, e.g., in rock-pools. In the slow-running
tanks of the Laboratory, however, these eggs develop less successfully than detached
and floating forms, since the decomposition of a few frequently causes the death of the
whole mass.
Considerable variations are presented by the external surface of the zona radiata.
Thus in Lepadogaster bimaculatus the capsule shows very evident punctures, and the
ova, instead of being fixed to each other, are attached separately to shells, stones, and
similar structures. Anarrhichas lupus, again, has the largest non-pelagic egg known
to us. During the investigations for H.M. Trawling Commission in 1884, one of us
had been familiar with the ovarian eggs of this form in their earlier stages, and in a
morbid ovary some of the fully developed eggs were retained so late as the month of
February, the spawning period apparently extending over the late autumnal or winter
season, probably from October or November to December. It was not until the 16th of
January 1886, however, that normal mature ova were obtained. A local trawler pro-
cured in comparatively shallow water (5 to 6 fathoms) a large mass of them. These ova
(Pl. XX. figs. 6, 7) are of a pale straw colour, with a slight opalescent hue. In shape
they are more or less spherical, and measure 5°5 or 6 mm. in diameter. The zona
radiata presents a comparatively smooth, though minutely punctured appearance
(Pl. XX. fig. 8), and is very tough, so that the eggs, which are fixed to each other in
the usual manner to facilitate aeration, can only be torn asunder with difficulty. In
section (PI. I. fig. 25) a stratum (a), marked by a deep heematoxylin-stain, separates an
outer thicker from an inner thinner portion of the zona radiata. Fine striations or pore-
canals are also seen traversing the entire thickness of the capsule. A single large oil-
globule 1°75 mm. in diameter occurs in each ovum. This, as usual, constantly passes to
the upper pole, just as the oil-globule does in pelagic eggs. Only a single unimpregnated
egg was available for the demonstration of the early condition. In some unhealthy
or dying eggs a number of very small oil-globules were seen clustering round the edge
* M‘Inrosu, Nature, June 1886.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 673
of the germ, the general size being about 3} inch. Towards the period of hatching
the chitinous zona radiata is more easily torn, and readily splits into lamellz, all of
which show minute punctures (Pl. XX. fig. 8), appearing like minute pale specks on
a dark ground. In some again the punctures are lost in a general granular area.
Whether these so-called punctures were actual canals, or only radiating striz, could not
be demonstrated.
This separability of the capsule into layers in the later stages does not conflict with
the view that it is really a single coat. Such chitinous formations in other forms show
the same tendency to split into filmy strata under certain circumstances, and, as explained,
a like tendency is exhibited in the extremely thin zona radiata of Gadus morrhua
and G. e@glefinus. In size the ovum of Anarrhichas* resembles that of the salmon
(Pl. XX. figs. 9, 10), though the punctures in the latter form (fig. 11) seem to be
somewhat larger.
LIiparis montagui.—The capsule presents externally a minutely areolate appearance
(Pl. I. fig. 4) due to slight elevations, resembling indeed the surface of grained morocco
leather, the elevations having a more or less marked linear disposition. In newly
deposited examples, or in ripe ovarian ova, the external configuration shows an almost
regular hexagonal character (PI. I. figs. 21, 22), the sutures being pale, while the central
regions are more opaque, probably from increased thickness. After exposure to water a
change seems to occur, the hexagonal facets becoming less marked, while a series of eleva-
tions become visible, ‘and are apparently due, therefore, to a later modification. In
oblique views the capsule shows undulating surface-markings (PI. I. fig. 22). As these
ova were not actually observed to be deposited by this species, however, it must be added
that a margin of doubt exists as to the feature described.
In this as in other species the zona radiata is at first soft and plant, hardening
subsequently, as in those deposited in the Laboratory. In the fresh condition minute
punctures are visible, though these are less distinctly seen after mounting in certain
media, ¢.g., Farraut’s solution, and on tearing the capsule the same dense series of laminze
can be separated as in Anarrhichas and Cottus. While in the ovary the eggs have a pale
straw colour, and measure about ‘043 inch, the oil-globule being 0083 or less, but those
just deposited in the tanks show a slight increase in size, viz., ‘045 inch in diameter,
and the oil-globule varies from ‘005 to 0116 of an inch. The eggs of this species are
very frequent on sea-weeds, zoophytes, and fragments of sticks and débris at the bottom, in
comparatively shallow water as well as in the deeper parts, and they show much variation
in colour, from pale straw to a light pink or flesh colour. They have often been mistaken
for the eggs of the herring, from which they differ in regard to the structure of the
zona radiata, and in the absence of the so-called vitelline membrane, which Mr Brook,
however, says is not present. The embryos again are sufficiently diagnostic, for the
* It is remarkable that the masses of the eggs of this species have hitherto escaped observation, fishermen being so
little acquainted with them that they were mistaken for those of the salmon. Some time afterwards the recently
hatched embryos (then unknown) were recognised by one of us in Edinburgh, having been forwarded to the Fishery
Board for Scotland by one of the steam trawlers of the General Fishing Company, Granton.
VOL. XXXV. PART III. (NO. 19). 5 R
674 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
elongated and somewhat feeble herring cannot be confounded with the shorter and more
vividly tinted larval sucker, which shoots into the surrounding water at once on issuing
from the egg. The ova usually referred to this species, however, require further study,
and the condition of the larva on emergence presents certain differences in the several
varieties. It is possible that several species have similar ova, but where absolute
certainty in regard to their determination was not possible, only those having the same
size and structure were grouped under the head of this species. The spawning period
ranges apparently from January to June.
Cyclopterus lumpus.—The ova of this species are very variable in colour, ranging
from a beautiful amethystine lustre through the various shades of straw-tint to greenish.
The zona radiata is thick, and minutely punctured, but presents no special thickenings
or superficial wrinkles, except where the facets of attachment are situated. The eggs are
fixed together in sponge-like masses, so as to permit free aeration, yet the hatching of
this species in confined tanks is somewhat difficult. The germ, as in pelagic forms, keeps
for the most part at the lower pole, the oil-globules ascending to the upper pole. Their
diameter is about ‘1 inch, while that of the large oil-globules is about ‘041 and less.
Ova, apparently of this species, were obtained in great quantity from the stomachs
of codling off Boarhills (Fifeshire), but, unless erroneously diagnosed, the gastric juice
had caused a diminution in diameter, as they measured only ‘083 of an inch, while
the large oil-globule in each measured ‘026, and one or two smaller globules were also
present. Though to a slight extent digested, this ovam showed much resemblance to
that of Cyclopterus, and formed masses of a yellowish green colour. In addition to the
ordinary punctate structure, the zona agrees with that of Cottus in presenting larger,
more evident dots at intervals (PI. I. fig. 24); indeed, this arrangement of larger punc-
tures in the midst of the smaller ones is more distinct than in Cottus. They resemble
large canals rather than radial strize, and they are finely dotted when viewed in profile, as
at the edge of a torn fragment. It is noteworthy that at the same period as the above
partially digested ova were obtained, a considerable quantity of similar eggs of a pale
straw colour were procured on the beach near the Laboratory. Their diameter was ‘0916
and that of the large oil-globule ‘031, and several smaller globules were also present.
The ordinary pores were larger than in Cottus, but the larger pores, scattered at intervals,
were similar. If these be the ova of Cyclopterus, which they closely resemble, consider-
able latitude must be given in regard to diameter. It has, however, to be borne in mind
that the condition of the ova (7.e., whether they had been subjected to dessication or other-
wise) was unknown. ‘The spawning period of Cyclopterus extends from February to the
end of May, and occasionally even a little later.
Agonus cataphractus.—The ovaries of a number of female specimens caught by the
sprat-nets in the estuary of the Tay were found to show nearly ripe eggs in December.
The eggs are large, and of a dull golden or dull yellow colour, their diameter being ‘07
inch and that of the oil-globule about ‘0216. The zonais minutely dotted with punctures
arranged in a linear series. The surface is also covered with well-marked areole. (PI. I.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 675
fic. 23). This species seems to spawn from January (or perhaps even from December)
to April.
Cottus scorpius (Pl. I. fig. 3).—The ova present various shades of red, inclining at
times to orange or yellow.. Their diameter averages ‘075 inch, and the large oil-globule
ranges from ‘015 inch in diameter downward. The zona is smooth, except where the facets
for attachment to adjacent ova occur. Minute dots are visible under a high power, and
these have a more regular linear arrangement, as a rule, than in Cyclopterus. Moreover,
larger dots occur at intervals all over the surface, recalling those noted in Cyclopterus
taken from the stomach of young cod. In the Report to H.M. Trawling Commission,*
one of us has alluded to the error of Professor ALEXANDER AGaAssIz in considering the
ova of Cottus pelagic, a fact overlooked by Mr Cunnincuam.t
Ammodytes tobianus, L.—G. O. Sars states that the comparatively large ova of this
species are not pelagic, but are laid in loose sand, where they go through their
development. Covcn, again (No. 44, ill. p. 138), considered that it sheds its ova
in this country as it dashes through the sand in December; while Day (No. 51, i.
p- 333) found the reproductive organs in both male and female, at St Ives, far
advanced in August and September. On the other hand, THompson states that in
Ireland they were nearly ripe at the end of July. The organs, however, were found
to be small in November at St Andrews. Early in May some specimens (none more
than 6 inches in length) showed ripe spermatozoa, though the testes were comparatively
small; while in the females the ovaries were not much developed, and contained
very minute eggs. These eggs were transparent and granular, with a large germinal
vesicle. Some larger eggs, five or six times the diameter of the remainder, showed
a coarsely granular yolk, with many small oil-globules, and a very thin external
capsule, which is finely reticulated, and provided with minute punctures as in other forms.
In the ovary the eggs appear to have a somewhat whorled arrangement. Later, about the
beginning of June, the reproductive organs in about twenty examples showed an irregular
state of advancement, some having fairly advanced ovaries, while others were rudimen-
tary. In those best developed the ova were of a rich orange colour, “reddish yellow,” as
Sars said, and they were just visible to the naked eye as minute grains ;); of an inch in
diameter. The germinal vesicle was still very evident, measuring 3}9 inch. Most of
the larger ova were of this size, though others were much smaller, the smallest being in
fact less than the nucleus of the largest eggs, and their nuclei showed many nucleoli. The
zona is distinctly dotted at this stage. The sperms in the male fishes showed a distinct
head, but no motion was visible at this time. So far as could be observed at St Andrews,
the spawning period of this species would seem to be late, indeed so late as to bring it
within a reasonable distance of the pelagic larval forms described in a subsequent
chapter.{ In some examples, however, examined in the middle of December, the genital
* 1884, + Op. cit., p. 103.
t Section xi. Investigations, at present being carried out by Mr W. L. CatpEerwoop at the St Andrews Labora-
tory, may clear up the subject.
676 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
organs were so little developed as to form two rounded cords. From the fact that no
definite series of pelagic ova has been found previous to the appearance of the larval
forms, the ova would appear to be demersal.
Gobius ruthensparri.—In a female specimen about 3 inches long, obtained on 25th
January 1886, the ovaries were found to be small, though the ova were sufficiently
developed to be visible to the naked eye. Under the microscope, ova of various stages
were seen, the largest being about a line in diameter. A germinal vesicle was present,
and the central region of the egg was filled with well-marked globules (yolk).
Centronotus gunnellus.—Like Zoarces viviparus, this species is characterised by the
presence of a single unpaired reproductive mass in the form of a median band between
the intestine and the abdominal roof. Unlike Zoarces, however, the male organ of the
gunnel is also unpaired. In Day’s recent work on British Fishes the following note upon
the spawning of this species occurs (No. 51, vol. i. p. 210) :—‘‘ Nirsson states that its
spawn is deposited in November. Mr Pracu, however, in June believed he discovered
the spawn of this fish in Fowey, in Cornwall.” At St Andrews, where it is abundant,
frequent examination of the reproductive organs supports Nrisson’s observations. In the
earlier part of the year (February) the ovaries of the female are very slightly developed,
minute ova at various stages occurring in the follicles. In May the male elements are
less prominent than the female, for the ovary is the larger organ. In many the structure
is in a state of degeneration, large fatty globules and other granules taking the place
of the sexual elements. The ova at this time still show great variation in size, the
germinal vesicle being also present and unaltered. Towards the end of November
females, though of small size, present a large, clavate ovary, tapering from the liver in
front to a point behind the anus. The ova are now readily seen by the naked eye, and
those on the surface are of nearly uniform size, viz., about ‘043 in diameter. Several
oil-globules (‘012 in diameter) occur in the larger ova, and the yolk is opaque on
account of the abundant straw-coloured, almost opaline, yolk-spherules. Outside the
ovary is a transparent membrane, apparently continuous with the interstitial connective
tissue, and not readily removed from the surface. The smaller ova are finely granular,
and in some (the larger) small oil-globules are present.
The ova of this species after deposition seem to have been first observed by Mr
Anperson SmirH,* a member of the Fishery Board for Scotland. He found them,
probably on the west coast, from February to April. At St Andrews they have hitherto
been obtained amongst the rocks in March, masses about the size of a walnut (as Mr Surra
states) occurring in the holes of Pholas, the adults in each case being coiled beside
them. The ova adhere together like those of Cottus or Clupea harengus, and have
a diameter of ‘076 inch, while the oil-globule measures 0166 to ‘016 inch. In
those nearly ready to hatch the zona radiata is somewhat tender, and presents the
usual laminated appearance. It is also most finely and regularly punctate, after the
fashion of wire-cloth of great tenuity. The ragged margins especially exhibit the
* Quoted by Mr Cunnineuay, op. cit., p. 125.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 677
appearance of finely crossed fibres, partly due in all probability to the breaking up of
the tissue.
Blennius pholis—In May a large male, 6} inches long, was procured at the East
Rocks, St Andrews. The testes were highly developed, and almost reptilian or
amphibian in appearance. They form two large flattened organs, or rather are rounded
anteriorly, and flattened on the inner side—the two bodies, in fact, being precisely
like the two separated halves of along bean. The blood-vessels run along the flat sur-
face, and give off branches which spring as it were from a midrib. In colour they are of
a faint pinkish white. The outer or convex region is of a firmer texture and more
translucent than other parts of the testis, being composed apparently of tubules contain-
ing spermatozoa in full activity and abundant sperm-cells. The whiter opaque region
consists of aggregated sperm-sacs. The spermatic duct leading to the genital aperture
is exceedingly wide, and on one side shows a spermathecal enlargement, which, at
first sight, resembles an additional urinary bladder. The ducts open by an aperture
on a prominent papilla behind the large corrugated anal orifice. This strong papilli-
form protuberance approaches that in fishes which are known to copulate, but there
is no account of such in this species. A little later (viz., on the 23rd June) an adult
female, 5 inches long, had the ovaries much enlarged—containing a mass of large
bluish-grey ova, and smaller ones of a slightly orange hue. The minute structure of these
somewhat peculiar ova has been carefully described by Dr Scuarrr.* The ova (which
were not quite mature) measured about ‘0415 of an inch in diameter.
The above facts show that this species deposits its eggs apparently during the early
summer; PARNELL, indeed, names the month of June, while Dunn considers that it
spawns in spring. Covcn states that it deposits the ova on the roof of small caverns in
rocks near shore (Zool., 1846, p. 1419); and Day, who quotes the above authors, adds
that he found minute fry at Penzance in August. At St Andrews young specimens,
about an inch long, and which had acquired the features of the adult, are abundant
in the pools of the East Rocks about the middle of September.
Blenniops ascanit.—On 14th June 1886 a fine male, procured in a crab-pot off the
Buddo Rock, Fife, showed testes only partially developed. The stomach was distended
by eggs of Cyclopterus, wpon which it had been feeding largely.
A female in August exhibited only traces of ova—the ovaries being apparently
atrophied, but on the 16th September both organs were very large, the individual ova
reaching about y'; inch in diameter.
Motella mustela—On 17th July 1885, a female rockling, 6 inches long, was
examined, and the ovaries were found to be connate posteriorly, and contained ova of
some size, so that the species must pair very early in winter, and the spawning period
would seem to be very lengthened. In May the tanks in the Laboratory were found to
be full of the floating ova of this species, and during March, April, and May the ripe eggs
appear usually to be ready for extrusion, so that the ova of the female above referred
* Proc. Roy. Soc., vol. xli. (1886) p. 449 ; and Quart. Jour. Mier. Sci., Aug. 1887.
678 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
to, in which the unripe ova were of variable size, large and small, would probably have
been retained until the end of winter or beginning of the year. The pelagic ova of this
species are amongst the most abundant forms in and beyond the bay in March, April,
and May.
We have already spoken of the capsule as a zona radiata—a protective membrane of
general occurrence in the ova of most diverse groups of Vertebrates. Thus in the Aves
a zona radiata is present, though it does not persist; but at an early stage it dis-
appears, and the egg leaves the ovarian follicle enveloped by another membrane which
is distinguished as the vitellme membrane. This second membrane is exceedingly
attenuate, so that it is difficult to distinguish it from the outermost layer of yolk-cells
from which it is derived. The Leptilia possess also two membranes; but, unlike the
birds, they are not both of vitelline origin, the outer, which is very thin, Ermer (No. 53,
p. 418) declares to be a product of the follicular epithelium, and therefore chorionic ; but
the inner is thicker, and vitelline in origin; and Ermer regards this as the zona radiata
(his zona pellucida). The capsule in the Amphibia (Rana) is a remarkable structure,
and would appear to be really a chorio-vitelline membrane, for the inner cells of the
ovarian follicle form a layer very closely applied to the true vitelline membrane,
and as the latter becomes continuously thinner the two layers are really inseparable,
and form one layer, of which the outer stratum is chorionic, and the inner one is
vitelline.
In the Elasmobranchs a double layer is present, the outer being first formed, and
regarded by Batrour as vitelline; while the inner one, equally of vitelline origin, he
distinguished as the zona radiata. Both, however, atrophy as a rule before the egg
leaves the follicle. In Cyclostomes (Petromyzon) two layers are described, an outer
imperforate, and an inner perforated layer. The outer layer on contact with water
swells up and forms a gelatinous coating by which the eggs adhere to external objects.
In Myzxine, according to J. T. CunnincHAm’s researches, the thick capsule is a chorion,
being developed along with its solid projecting processes from the follicular cells.
Possibly a delicate vitelline membrane may be developed internal to the outer homo-
geneous capsule, but this Mr CunnineHaAm was not able to decide (No. 46, p. 600).
Notwithstanding that a double egg-membrane is so common, as indeed KOLLIKER long ago
pointed out (No. 80, p. 84), yet in the Teleostei the recognition of a single layer of vitel-
line origin accords best with the character of the capsule in general, in the mature ovum.*
Certainly LEREBOULLET’s designation “ chorion” (No. 93, p. 459) is inappropriate ;+ nor
does Kuprrer’s view, that the capsule in certain osseous fishes is double, like the
Elasmobranchs, seem better justified. Kuprrer holds that, in the ease of Clupea
* Dr Martin Barry affirmed that one membrane only envelops the ovum in fishes, no layer being formed
external to the vitelline membrane (No. 21, p. 309). SotcEr also came to the same conclusion from an examination of
Leuciscus rutilus (Arch. f. Mik. Anat., 1885).
the primitive vitelline membrane separated from the vitellus ” (No. 93, p. 507).
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 679
harengus, two separate layers, an outer vitelline membrane, and an inner zona radiata,
may be distinguished (No. 87, p. 178); but Horrman does not think the distinction
justifiable—one membrane alone being present, which, however, presents an inner less-
defined part, probably more recently formed, or in course of formation, from the vitelline
cortex ; and G. Brook supports this interpretation (No. 34a, p. 201).* Ifthe outer con-
centrically-laminated stratum be regarded as a layer separate from the inner stratum
which shows radial striations, then with Kuprrer we must consider the former as of
exceptional occurrence amongst Teleosteans (No. 87, p. 178). Brock, again, figures two
Teleostean ova with double capsules, the outer layer being striated in one case and
unstriated in the other (No. 29, Taf. xxviii. fig. 7, fi; Taf. xxix. fig. 6, b, e). The
interpretation as a single layer, we repeat, seems, however, better founded, for if the ovum
of Callionymus lyra be examined, we find external to the zona radiata, which has the
usual structure, “a series, for the most part, of hexagonal reticulations like those of a
honeycomb,” not unlike the reticulation of the early ovum of Ammodytes tobianus.
“These spaces are not quite uniform in size, but many are. Some again have four, six,
or seven sides; . . . . the septa bounding the reticulations stand out very distinctly, and
their edges show minute striz ” (No. 106, p. 481, also Pl. xiii. figs. 1,2, 3,4). The ripe ova
of this species have been examined at the Marine Laboratory, and the reticulation in
both cases is external, and is evidently inseparable from the zona radiata. The same
condition would appear to be present in the pelagic ova of Crenilabrus tinca, recently
described by J. H. List, the outer part of the zona consisting of regular six-sided
areas, and the inner only of fine parallel striations.t Such elaborate modifications
of this single layer are probably illustrated by the ovum of Cyprinus dolbula, with
its radially directed rod-like processes; of Perca fluviatilis (No. 111, p. 186), with
its prominent hollow cylindrical appendages, which interlace, and, with the mucous
envelope, hold the eggs together in “élégants réseaux,” as LEREBOULLET describes
(No. 93, p. 471); but they do not serve, as the same author states, for absorption
like the minute canals, though both structures penetrate the capsule. In such forms also as
Blennius, Gobius, and pelagic eggs like Heliasis and Belone, long filaments occur near the
micropyle, and are pronounced by Horrman, who describes them, as simply excrescences
of the zona radiata. If we regard the capsule in Teleosteans as essentially a single layer,
then the dissimilarity of the elaborately modified capsules of the foregoing species
—of the less complex capsule in Clupea harengus (No. 87, p. 178), and in sow Lucius
(No. 93, p. 465); and of the extremely simple membrane in the ova of Gadoids, Pleuro-
nectide, and others, wholly disappears. The species in which various layers, not to
say distinct membranes, have been described, find their place in the same category as the
ova of the cod and like forms with simple layers. That the capsule can undergo elaborate
modification is easily understood, when it is noted that in its early condition it is always
* See also LeREBOULLET's description of a similar inner layer closely applied to the yolk in the pike, the outer
stratum being alone striated (No. 93, p. 465).
+ Zeitsch. f. wiss. Zool., Ba, xlv. (1887) p. 596, tig. 1, a, b.
680 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
soft and pliant, and may remain so even after deposition, as we find to be the case,
notably in the thick capsules of Gastrosteus spinachia and Cottus. These ova, for some
time after deposition, are soft and yielding, possessing, as Prof. ALLEN THomson (No. 153)
states, in the fresh-water congener of the former, “so little elasticity that it usually
retains dimples or impressions made upon it from without.” In this connection it may
be mentioned that the so-called outer layer in Clupea harengus is slightly facetted (No.
87, p. 177), this being due, doubtless, to the impress of the follicle-cells before the egg is
extruded—a suggestion which may also be applied to the similar appearance in the case
of Perca (No. 111, p. 187). The zona radiata, as its name implies, has a characteristic
radiate structure in many Teleosteans, The real nature of the striation so visible in section
has been much disputed, and there is little unanimity of opinion in regard to it. In
many species this feature has not yet been made out, eg., in a number of familiar
Gadoids, viz., G. merlangus, G. eglefinus, G. luscus, Molva vulgaris, and some of the
Pleuronectidee, such as P. jflesus and P. limanda. The capsule in the familiar
Pleuronectid, Pleuronectes platessa, again, is very distinctly punctured (Pl. I. fig. 20).
CUNNINGHAM has recently mentioned that the zona radiata of the cod usually described as
not punctured (vide Ryprr, No. 141, p. 457), exhibits pore-canals, but he does not describe
them in the ovum of Zrigla gurnardus; yet the latter, so far as our experience goes,
shows them much more distinctly than those of the cod; indeed, we have not yet
satisfied ourselves concerning the latter. In the ovum of Trigla one of us has demon-
strated that the whole surface of the capsule is minutely and faintly dotted (PL. I. fig.
19). This punctate appearance is especially distinct after the escape of the embryo.
The capsule of this form in the unimpregnated condition shows numerous wrinkles—the
yolk occupying a comparatively small area, so that a large perivitelline space exists,
which, however, diminishes after fertilisation, until the vitelline globe almost fills the
capsule, which at the same time becomes less distinctly wrinkled. The corrugation of the
zona radiata is, however, a characteristic feature, and exists in all the egos of this species.
The zona is firm and elastic to a remarkable degree for a pelagic form, and its unevenness
causes some obscurity—only a faint line of dots being as a rule visible along the ridge
which happens to come into focus under the microscope. In one instance the zona
presented a series of scale-like markings or areolx (Pl. I. fig. 16), probably due to an
unusual or morbid condition in connection with the follicular epithelium. The normal
wrinkles (seen best in 7. gurnardus) also occur in the lemon-dab (PI. I. fig. 18); and
Ryper speaks of these in G. morrhua as fine lines crossing each other at definite angles.
Such lines, however, are less visible in eggs which are healthy and perfectly mature.
The typical zona radiata exhibits, as Von Barr discovered in Cyprinoids, fine striations
perpendicular to the superficies of the yolk, and Cart Voer described at greater length
the same feature in the Salmonidee (No. 155, p. 7); while Rercnerr noted it in the ova
of Tinca vulgaris and Leuciscus erythrophthalmus, and Leypic in Gobius fluviatilis.
Are these striz really canals, or merely fine fibrillations, such as we find in the
transient zona radiata of the fowl under a high power? In either case a punctured or
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 681
dotted appearance would be produced superficially, as im a large number of Teleostean
egos, especially in the comparatively dense capsules-of fresh-water forms. These
punctures may be comparatively large and distinct, as described by MULLER in Perca
(No. 111, p. 187-8), and by Levekartr in Hsox; or they may be of smaller size, as in Salmo
fario (No. 153, p. 101, and fig. 68, c, p), Gastrosteus spinachia; or of extremely minute
size, as in certain pelagic forms, eg., Trigla gurnardus and P. platessa. Frequently
the striations are observed to pass only partially through the capsule, and the outer
stratum is then imperforate, instances of this condition being the capsule of Clupea
(No. 87, p. 177), and Esow (Aubert), Gastrosteus spinachia, and probably Trigla
gurnardus, In other ova they traverse the whole thickness of the capsule, as is the case
in Salmo fario (No. 4, p. 198), and in Perca fluviatilis, according to the experiments
of J. Miter (No. 111, p. 188). The distinguished observer just named was convinced
that, when he placed the eggs of the perch under pressure, oily matter from the interior
of the egg could be squeezed through the canals of the zona radiata, and the canalicular
structure of this membrane would appear to be demonstrated in this instance. Other
observers, however, strenuously deny this, and, like ANDRE, pronounce the so-called
canals to be nothing more than rectilinear striations directed radially from the inner
to the outer surface of the capsule (No. 4, p. 202), precisely like the radial fibrillations
in the zona of the fowl’s ovum. It is only necessary to observe the effect of desiccation
on the egg of the cod, and then the action of water, to prove that a ready interchange
occurs through the zona either by pores or by ordinary endosmose.
Little can be said here as to the origin and growth of the zona radiata, for its
development is already complete when the ovum reaches maturity. That it is a true
vitelline membrane admits of little doubt ; and Horrman’s opinion, that it is secreted
by the vitelline mass as a superficial layer during the intra-ovarian period, and is not
separated until it shows an appreciable density and firmness, is probably well founded.*
Ransom holds that, after it is defined as an external membrane, it continues to grow
interstitially up to a certain stage, when growth ceases, and it performs a solely
protective function (No. 127, p. 494). Other layers are formed later upon the surface
of the yolk after the zona radiata has become detached as an elastic protective capsule,
and these may claim to be called vitelline membranes, as indeed they have been styled
by various authors. Thus, OkLLAcHER, when speaking of the vitelline membrane in the
trout (No. 113), really means the stratum of germinal protoplasm, the polar segregation of
which forms the blastodise; while LerEBouLLET uses the same term for the layer
of protoplasm which ventrally limits the intestinal tract of the embryonic fish at a
comparatively late stage (No. 93, p. 612). Such uses of the term “ vitelline membrane”
for very different layers (though all of vitelline origin) are not to be approved, and the
name zona radiata is at once distinctive and appropriate for that vitelline membrane
* The development of the vitelline membrane in Triton has been shown in an interesting manner by Mr Iwakawa,
and his descriptions and admirable figures (see No. 75, p. 274, and pl. xxiv. figs. 24-26) will apply in the case of the
Teleostean capsule,
VOL. XXXV. PART III, (NO. 19). a8
682 PROFESSOR W. C. MINTOSH AND MR E. E. PRINCE ON
which forms the external capsule, and subserves a protective function. When the
embryo is sufficiently mature the capsule is burst,—the rupture being due, no doubt,
to the vigorous motions of the young fish, which in the case of Pleuronectes flesus
generally emerges from the capsule by pushing out its tail.
The Micropyle.—The zona radiata is pierced by the micropyle (PI. II. fig. 19, mic.),
an aperture probably universally present in Teleostean eggs, and in these it varies
very little in structure and appearance. Thus in the salmon, trout, pike, ruff, perch,
bullhead, gudgeon, minnow, chub, and various species of Gastrosteus, Ransom’s descrip-
tion accords almost perfectly with the micropyle, as seen in the cod, haddock, ling,
whiting, bib, flounder, dab, plaice, gurnard, and others. At a certain point the capsule
is distinctly thickened, and an internal conical elevation is formed, which, as BALFouR
says (No. 10, p. 51), corresponds with an external funnel-like depression, while a
cylindrical canal connects the bottom of the funnel with the apex of the inner papilla.*
The thickened appearance of the capsule in the micropylar region is not produced simply
by the protruding hillock, and due to the crateriform depression outside; but as ANDRE
(No. 4, p. 201) ascertained, and as may be easily demonstrated in the delicate translucent
ova of the Gadide or Pleuronectidee, the capsule is actually thicker at this point
(Pl. X. fig. 9). Lisr shows the same feature in Crenilabrus tinca.t Viewed from
above, three parts may be distinguished—a large outer annulus and a smaller inner
ring, with a central pore which is the opening of a cylindrical tube. In the trout
these measure, according to ANDRE, ‘015 mm., ‘008 mm., and 005 mm. in diameter
respectively. The first-named ring is the rim of the external crater; the inner ring
marks the narrower, deeper portion ; while the central aperture is the essential part, the
true microlpyar canal, which is not, however, perfectly cylindrical, but midway along its
course distinctly enlarges, and then narrows again. This sinuosity observable in the canal
proper, ANpr& thinks, is produced by the ends of the pore-canals or radial striae which jut,
out slightly into the lumen of the micropyle (No. 4, p. 201). That the micropyle is really
a depression, and not simply a puncture, is shown by the fact that the striations of the zona
radiata present an inclination towards the micropyle, which is increased as the aperture is
approached, and still more so down the walls of the crater, their outer ends being directed
towards the cavity of the depression, and forming projections into it as just stated.
This inclination of the striz is shown by Ransom and others; but His does not
indicate it in his figures of the ovum of Salmo fario and S. salar (vide No. 67, Taf. i.
figs. 7, 8, 9, and 10); and the same may be said of List in his recent paper. Connected
with the depression and thickening of the capsule around the micropyle, is the striking
appearance external to the larger annulus seen in the marine and fresh-water species of
Gastrosteus, where bold radiating strize pass away from the margin of the external crater
(vide Nos. 153 and 67, Taf. i. fig. 15), a feature less marked in the chub, in which the margin
* Ransom speaks in Gastrosteus of the micropyle as projecting actually into the protoplasmic dise, and of a subse-
quent shortening of its funnel after fertilisation (No. 127, p. 450).
t Op. cit., p. 597, fig. 2, a.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 683
is crenate and the sides are furrowed. In the pike Ransom describes the micropyle as
trumpet-shaped, and projecting slightly from the surface of the capsule (No. 127, pl. xvi.
fig. 25, a); while in the minnow, too, the margin is raised around the outer opening of
the funnel (/bid., p. 456). Stria are occasionally seen in certain pelagic forms, e.g., in
Trigla gurnardus and Gadus eglefinus, but the margin of the crater is usually sharply
marked, and the aperture itself very clearly defined without radial markings. When viewed
in “ full face,” the funnel seems larger than it really is on account of the torsion, so to
speak, of the zona radiata, which appears as if bent in to form the orifice, a feature ANDRE
particularly points out (No. 4, p. 199), and to which we have made reference above.
The micropyle thus varies in appearance. Usually the external opening is the larger ;
but in some cases this is reversed, a large gaping internal opening being present (vide
fic. of ovum of G. eglefinus, Pl. I. fig. 14), while the external orifice is small. The
striations above mentioned are also visible in this case—the whole peri-micropylar region
being granular, while the granules have a tendency to range themselves in radial lines.
Near the micropyle in some examples an accessory structure is present, due apparently
to a granular protrusion of the zona (Pl. I. figs. 11 and 15). In this and other cases
the micropyle was distant from the germinal area. Fertilisation in pelagic eggs does not
produce any marked change in the micropyle, certainly none like that described by
Ransom, and just mentioned. In one instance, beside the micropyle proper, was a
depression plugged by an ovoid granular structure, while a large group of “ oleaginous”
spheres lay upon the yolk near the micropyle (PL. I. fig. 17).
Origin, Position, and Function of the Micropyle-—The mode of origin of the
Teleostean micropyle is unknown. When first observed in the mature ovum it presents
the features maintained throughout the subsequent history of the egg. Lrypie describes
(No. 97, p. 376, fig. 6) the earliest ovarian egg of Trigla hirundo as somewhat pyriform
and stipitate, recalling, in fact, the stalked ovum of Unio, in which the micropyle marks
‘the pedicular point of attachment by which the egg adheres to the ovarian capsule, as
Carus was the first to note. Such an interpretation of the micropyle, as the cicatricule
left by a pedicle, cannot in the case of the osseous fishes be adopted, and we are still
left in doubt as to the way in which the aperture arises.
It is interesting to observe that in many forms the position of the micropyle is
constant, and corresponds to the germinal pole, where the embryonic area is formed,
as, indeed, Ransom found in Gastrosteus. In Perca, however, the aperture is turned
towards the inside of the ege-tube—the ova being fixed in a cylindrical mass, so that the
possibility of the micropyle being blocked up by adjacent ova is obviated (No. 127, p. 456).
GeRBE similarly says, “that the micropyle plays an important part, as the dise always
collects near the place oceupied by it” (No. 57, p. 330). Neither Ransom nor GrrBe
examined pelagic ova; but from the later observations of Ewart and Brook, it would
appear that in floating eggs the micropyle is always found in the lower hemisphere
(No. 55, p. 55). This position is, of course, the reverse of that in stationary demersal ova,
in which a preformed dise is commonly found in the upper (animal) segment ; whereas in
684 PROFESSOR W. C. M‘SINTOSH AND MR E. E. PRINCE ON
pelagic eggs the blastodise formed after fertilisation is also theoretically constant, but in
the reverse segment—the animal pole being underneath, and in calm water the germ
is usually found at this lower pole.*
As to the function of the micropyle, most authorities are agreed that it is connected
with the fertilisation of the ovum, affording means, in fact, for the entrance of the
spermatozoa. Kuprrer, however, calls this generally adopted view into question, and
doubts whether it has any essential part to play in fecundation (No. 87, p. 179). In the
ova of lower forms the function named has been universally admitted from the time
Merssner first described the aperture in crustaceans and insects (No. 102, p. 272),
and Levckart laboriously worked at the structure and function of this aperture in a
large variety of insects. The latter, in his elaborate paper, states that he beheld sperms
not only adhering to the outside of the egg, but entering the micropyle ; and indeed figures
this phenomenon in the ovum of Melophagus ovinus, a crowd of spermatozoa being
collected at the external opening, though not more than three or four find entrance.
In Teleosteans its function appears to be solely that of affording ingress for the fertilising
element, though Frrp. Keser (No. 77) conceives not only this to be the case, but that
through it there is an actual outflow of the contents of the ege—the purpose of this
outflow being to lubricate the canal and favour the entrance of sperms, as well as to
increase the vacant space within for the reception of the spermatozoa,
MerssNer, who first described the micropyle in the ovum of the rabbit, thought that
the aperture only penetrated the vitelline membrane, and that it was effectually closed
over by the chorion outside (No. 103). A modified view has been put forward by
Ransom, who was probably the earliest to discern and rightly interpret this aperture in
osseous fishes.t He was of opinion that a delicate film covered the micropyle, which
was only ruptured by the entrance of sperms; and more recently Borck, in connection
with his remarkable theory of osmotic fertilisation, to which we shall refer shortly,
conjectures that a clear membrane, in the case of Clupea harengus, closes the aperture of
the micropyle (No. 23, pp. 5, 6). Besides admitting sperms, a small quantity of water
may also enter, which (water) mingles with certain organic particles, and fills up the space
between the vitellus and the zona radiata in the extruded ovum.
THe DrutorLtasm or Foop-Youk.
Within the egg-capsule is the ovum proper, a spherical translucent mass, largely
composed of fluid food-yolk. With the food-yolk, which serves for nutrition, there is
interfused active protoplasm, and this, at an early stage, collects as a delicate film over
the surface of the yolk-ball; indeed the mature ovum of Teleosteans, before fertilisation,
exhibits a distinct superficial layer of clear protoplasm, in which minute vesicles and oil-
* According to RyprEr, the germ is lateral in Alosa.
+ Brucu independently discovered the micropyle in the eggs of the trout and salmon (No. 35, p. 172).
eS Se rr
EEE EE EE
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 685
spheres are embedded.* During the first hour after fertilisation these translucent vesicles
are readily seen under a moderate power (450). Occasionally granular protoplasm is
observed at certain parts of the contour of the vitellus in the haddock. A similar appear-
ance occurs in the cod, in ova which are abnormal though still translucent. Amongst
these vesicles are others extremely minute and very numerous, which in refracted light
have the appearance of punctures.
To distinguish the albuminoid matrix, which forms the greater part of the bulk of the
ego, from the active germinal protoplasm, the name “ deutoplasm,” conferred by Prof.
E. van BeneDEN, is both appropriate and convenient. This deutoplasm rarely has the
appearance of yolk-segments contained in a sponge-like network; but is composed in
many pelagic eggs of minute yolk-particles aggregated in a matrix apparently homo-
geneous, highly refractive, and coagulating on the addition of water. The latter feature
has long been known, for LerespouLLer found coagulation to take place in the ovum of
Salmo fario, just as Voer had noted in Coregonus palewa (No. 155, p. 11).t Broadly
speaking, we may say of the yolk in the Teleostean ovum that it possesses special features
of its own, which separate it from the nutritive matter of other vertebrates ; whereas the
yolk of the Elasmobranchii resembles in a very marked manner that in the Avian egg.
There is apparently little difference in the specific gravity in various parts of the deuto-
plasmic matrix, as it retains any position in which it is placed before the aggregation of a
polar disc; but Ransom questions whether its specific gravity is equal throughout, and
thought that nearer the surface it is of a more fluid consistency, or, as he says, “ I had
some reason to think a little less dense than the centre, as it ran more freely ; but all parts
flowed from a rupture like very thick syrup ” (No. 127, p. 436). The greater density of the
deeper deutoplasm can be readily explained by the movement of the interfused protoplasm
surface-wards, so that the central part of the yolk-globe becomes more purely yolk-
matter, while with the more superficial strata a larger, though constantly diminishing,
quantity of germinal protoplasm will still be intermingled. KowaLewsky considers that a
protoplasmic network must exist in the yolk (Carassius, Polyacanthus, and Gobius), since
after hardening the latter presents polygonal partitions (Zeitsch. f. w. Zool., vol. xliii., 1886).
He also terms the yolk the entoblast, in contradistinction to the germinal disc or ectoblast.
The freedom with which the so-called oil-globules in various forms (e.g., the gurmard
and ling) move through the deutoplasmic globe not only proves its very fluid consistency,
probably corresponding with that of thick cream, but shows the absence of a definite
* LEREBOULLET inclines to the opinion that the yolk is active in the formation of germinal protoplasm ; “at any
rate,” he says, “in the Lizard and Bird we find it before the germinal vesicle is ruptured ” (No. 95, p. 11).
+ The behaviour of the deutoplasm under various conditions was made the subject of some interesting observations
by Dr Davy in the ovum of the charr (Salmo wmbla), and he found that while contact with water in quantity coagu-
lated it, the careful application of water in minute portions did not do so. Again, when heated even so high as 212° F.,
it did not coagulate, nor did it under the influence of steam ; whereas boiling water at once effected the change, owing,
it was inferred, not to the heat, but to the admixture of water. While acids, salts, and alkalies had no coagulating
influence, except when dilute, nitric acid, corrosive sublimate, and alcohol produced the change immediately. Davy
came to the conclusion, as a result of his researches, that the deutoplasm of the charr and other Salmonoids has pro-
perties distinct from the albumen of the Avian yolk (No. 50, p. 436). Results similar to those of Davy were obtained
by Ransom in the various Teleostean eggs which he studied (No. 127, p. 436).
686 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
protoplasmic network, such as the reptilian ovum presents, or as Dr Scuuttz demonstrated
(No. 144) in the Selachians.
Little or no food-yolk makes its way into the germinal area, so that, as LEREBOULLET
observes (No. 93, p. 485), it takes no part in the segmentation of the germ. Indeed, all
evidence tends to prove that the deutoplasm is in an inert or quiescent state, and only
passively contributes to embryonic development, being slowly incorporated by the active
protoplasm of the blastodise in a mode which RypeR compares to the process of ingestion
and assimilation in Amaba (No. 141, p. 557).
When the eggs of Gadus morrhua are partially dried, the surface of the yolk shows
a series of clear reticulations, which on re-immersion in water run together and disappear
in the course of eight or ten minutes; such reticulations have, however, no connection
with the later protoplasmic reticulation of the vitellus after epibolic extension of the
blastoderm, and which is very noticeable in the cod, common dab (PI. V. figs. 3, 11),
and others. HarckEL regards it as so much passive matter contained in a gastrula-
cavity (No. 62); but in Teleosteans it plays a more important réle in later stages than
that of supplying crude pabulum to the germ. Indeed, the germinal protoplasm
Baprant holds to be solely transformed yolk—not a mere segregation of interfused
germinal matter. The germ, he says, is formed “by endogenous development of cells at
the expense of the yolk or primordial protoplasm;” but he repeats the error of Costr
that the germinal area is never formed until after fecundation (No. 9).
J. T. CUNNINGHAM, in a highly suggestive paper, observes that the yolk and germ are
equally concerned in the processes of cleavage; segmentation in Teleosteans (as in
Amphibians), dividing the ovum at the first stage of cleavage not equatorially, as E.
vAN BrnebEN holds (No. 25), but meridionally into two similar halves, each with a cap of
protoplasm and a mass of subjacent food-matter (No. 48). This view, however, gives
to the crude deutoplasm an importance which cannot be accorded to it, even though
cleavage as regards the yolk be merely potential and never fully achieved.
The separation of the deutoplasmic mass into a segmenting blastoderm (Pl. XXII.
fig. 1, bd), and an appended ball of pabulum (Jbid., y), is more complete in osseous fishes
than in Elasmobranchs, and imparts to the yolk rather an accessory character than that
of an active participator in the whole process of cleavage.
That it contributes to the growing organism, and even buds off cells to build up part
of the enteric tract, does not conflict with this view, which is supported by the fact that
the yolk persists as a bulky appendage on the ventral surface of the young fish (PI. XIX.
figs. 5, 7), until a late embryonic stage, being enclosed by the body-wall, and finally
absorbed when the post-larval stage is reached. The passive réle attributed to the yolk
Ryper would confine to the early stages, while later its function, he holds, is more
important, since it becomes through the medium of the intermediary layer an active part
of the ovum (No. 141, p. 569).
But this view is not inconsistent with that here maintained, for if it serves as pabulum,
this is really a part secondary to actual participation in blastodermic cleavage, and while
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 687
the transformed substance of the cortex is difficult, if not impossible, to separate from the
protoplasm of the germ proper, yet the yolk in the main is neither concerned in the
cleavage of the germ proper, nor actively contributes to. the increase of the embryonic
tissues. In the Gadoids and other forms no vitelline circulation is established, and the
absorption of the yolk is a slow and circuitous process.*
Oleaginous and other Globules—One of us has already published an account of
these bodies, which form a striking feature in the yolk of many Teleostean ova
(No. 125). The following remarks refer mainly to 7. gurnardus, and they still further
explain certain statements in the paper referred to.
In the ripe ovum of the gurnard the globule (PI. V. fig. 5, og) is of a dull pinkish
hue under a lens, while by transmitted light it exhibits a brownish yellow or pale salmon-
tint. It is enveloped by a protoplasmic pellicle which sometimes appears incomplete,
and forms an equatorial line, with pale pinkish vesicles studded along its border.
Unlike those forms in which the globule is imbedded in a definite pocket (e.g., Motella),
the globule in the gurnard, as also in Cyclopterus and Cottus (Pl. I. figs. 2, 3), is most
mobile, and can be made to pass under the disc when the latter is uppermost. On
rolling the egg the globule emerges from beneath the disc, and is liberated with a bound
at the edge of the rim. Moreover, in passing round it flattens out, and again contracts
its diameter, or rather resumes its more spherical form. At times the globule appears to
ascend directly through the yolk, though this may be a deceptive appearance, for
Ransom found in the very mobile globules of Gastrosteus, that while they passed freely
through the yolk, they could not be made to go “through its centre to get to the
uppermost segments when the egg is rolled round ; in doing so the drops often separate
to unite again” (No. 127, p. 436). Ransom accounted for this by the greater density of the
central yolk-substance. The passage of the globule under the rim is well seen in the egg
of the gurnard when the germ has extended as far as the equator. In certain morbid con-
ditions the exact relations of the globule during its movements can be readily determined.
Thus the globule is often firmly fixed in the dead egg between the opaque blastoderm and
the yolk, or the globule is seen at the side, and cannot be made to pass beneath the dise,
possibly on account of the doubling of the edge of the disc, or because the investment of
the globule and the periblast have become dense and rigid. During the earlier morbid
stages, however, the globule is observed to pass beneath the somewhat opaque disc, and in
certain abnormal cases, from pathological change, the globule rolls external to the dise.
From the above observations it is evident that Mr CunnincHaw’s view (No. 48, p. 6;
also Pl. II. fig. 19) that the globule moves in the perivitelline space—that is, between the
yolk and the zona radiata
passes between the disc and the yolk, and never passes through the protoplasmic cortex
of the latter, save in rare morbid examples. In those eggs in which the rim has still a
short distance to traverse the globule continues freely movable, and its surface next
the yolk often presents a series of small globules and a single large central one. The
is not borne out, since in experiments, such as the above, it
* Vide “Significance of the Yolk in the Eggs of Osseous Fishes,” E. E. Prince, Ann, Nat. Hist., July 1887.
688 PROFESSOR W. C. M‘INTOSH AND MR E, E. PRINCE ON
globule passes in later stages under the embryo, and for some time moves freely; but
about the fifth day, when the blastopore closes, it becomes fixed, generally at the point
coinciding with the vegetal pole. It now exhibits a thick layer of protoplasm, which
becomes vacuolated in a complex manner, and gives origin to numerous nuclear structures
as well as pigment-spots (PI. XI. figs. 12, 13). In certain cases (gurnard) the peri-
blast was observed to bend in from the blastodermic layers, and carry the oil-globule
with it at its margin.*
PERIVITELLINE SPACE.
This space is generally very distinct, and contains a transparent fluid, usually said to be
water, which enters the ovum after fertilisation. In an undetermined species the space
is enormously enlarged (PI. XIII. fig. 3). RercHerr, however, very lately observed that
under the action of nitric acid it exhibited whitish flakes (No. 134, p. 463), Ransom again
states that when the funnel of the micropyle is withdrawn from the discus proligerus (in
Gastrosteus), water enters “to fill the breathing chamber.” This view was questioned by
one of us in a short paper read at the British Association in 1885 (No. 122), the following
statement being made :—‘‘ That a certain amount of water finds access to this space is
possible, but in stained sections the fluid filling the chamber often appears coagulated and
faintly stained, thus indicating the presence of minute protoplasmic particles. 1t would
appear to be, therefore, a dilute plasma.” Rarraxce has recently stated that the fluid
is albuminous (No. 125a). In the gurnard various granular bodies, probably portions of
protoplasm of a circular form, have been seen. It is possible that these agree with the
segmenting corpuscles of RypER and the expulsive bodies of RarraEtz.t
Ill. Exrruston AND DEPOSITION.
The ova when ripe either pass directly into the body-cavity from the ovaries and out
by an external pore, as in the Salmonidz and Anguilla, or they pass to the posterior end
of the ovary as they become mature, and thence by an oviducal aperture to the exterior.
The latter is the more prevalent mode, and it presents two types according as the act of
deposition is very rapid, as in the Cottoids, Discoboli, and certain Blennies; or it is slower,
as in the Gadide, and may be even prolonged, as appears to be the case with T’rigla.
The difficulty of ascertaining the real facts in regard to oviposition is apparent when
it is remembered that, about even so familiar a form as the salmon, opinion has been
up till comparatively recent times divided; the fishermen being of opinion that the
process is gradual, and may occupy many days, whereas there is much evidence to show
that the ova are discharged all at once, or very rapidly. In stripping a ripe female the
* J. A. Ryper (Amer. Nat., vol. xx. p. 987) states that the periblast is hypoblastic, and that the only source of
the nuclei in the pigment-cells of the oil-drop must be periblast; therefore these cells are hypoblastic in origin.
Kinosiry and Conn severally observe (op. cit., p. 188) that possibly the ova of all the Gadide have one or more
conspicuous oil-globules in the deutoplasm.
+ Op cit., p. 16. He also thinks the perivitelline space has a phylogenetic significance.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 689
egos run out with little or no pressure, and the ovaries may often be thus emptied in a
few moments. Now if the ovaries of a female Cyclopterus lumpus, exemplifying rapid
deposition, be examined, we find, when in a ripe condition, that the contained ova
apparently become mature simultaneously.* In such a case great distension of the
abdomen occurs, and the eggs are deposited in a single large mass in a very short time.
In a female Cottus scorpius under observation, and likewise distended with ripe ova,
oviposition occupied only a few seconds.
A very different condition obtains in other forms, such as Molva vulgaris or Pleuro-
nectes flesus, in which a large proportion of the ova ripen together, yet the act of extrusion
is more deliberate and slow; while in Gadus morrhua, or more distinctly in Trigla gur-
nardus, the eggs reach maturity by successive strata, a comparatively small proportion of
them being ripe and translucent. The latter generally pass posteriorly, and collect near
the genital opening—ready for extrusion.t Isolated ripe ova, however, are scattered
throughout the evaries, and in such forms the extrusion of all the eggs in a single female
must extend over a prolonged period.
While the ova remain in the body of the fish they are bathed in a mucilaginous fluid,
so that they easily glide over each other, and thus their egress is facilitated. This ovarian
mucus seems to have different properties in different species of Teleosteans, either dis-
appearing on mixing with water, as we see especially in the non-adhesive floating eggs of
the cod, haddock, whiting, ling, gurnard, skulpin, flat-fishes, and also in the demersal eggs
of the Salmonidz, or remaining glutinous and adhesive for some hours—the eggs clinging
strongly together and forming irregular spongy masses, as in British Cottoids, Discoboli,
various species of G'astrosteus, as well as the recently discovered ova of Anarrhichas. In
Lepadogaster,{ however, the ova are fixed singly to shells, sticks, sea-weeds, and other
structures,
After submergence in sea water such ova become so strongly cemented that some
force is required to separate them, and the egg-masses of forms like Cyclopterus adhere so
firmly that many of the ova are usually injured in dislodging them. Whether the
mucilaginous nexus which binds ova like those of Lophius piscatorius together im
considerable masses, or forms a thick, tenacious layer outside the zona radiata in eggs
such as those of Perca fluviatilis, be really an excessive secretion of the mucus spoken of
above or not is undetermined.
Demersal ova appear to be deposited by the female on the very sites where the whole
course of development, up to the time of hatching, will be undergone. With pelagic ova
the case is very different; during development they may wander far from the place of
deposition.
It must be noted, however, in the case of the cod, and other food-fishes, that the
grounds upon which the adults congregate are those where the surface specially abounds
with their pelagic ova, as Sars first noted at Lofoten.
Upon extrusion the buoyancy of pelagic ova is strikingly shown, for, if ripe, they at
* Vide Nature, June 1886. + Vide No. 104, p. 363, &e. I Vide No. 106, p. 434.
VOL, XXXV. PART ITI. (NO. 19) oT
690 PROFESSOR W. C. M‘SINTOSH AND MR E. E. PRINCE ON
once ascend like minute crystalline globes of oil, and before fertilisation, as well as after,
they swim freely in the water (No. 11, p. 36, and No. 65, p. 450). Not only are these
pelagic ova found at and near the surface of the sea, but, in many areas, throughout the
greater part of its depth. Moreover, they occur in great numbers near the bottom. In
calm regions they congregate near the surface in scattered groups, and show no tendency
to adhere together, save in such exceptional instances as those before mentioned. The
slightest agitation scatters them, and they are carried to and fro by the currents in the
surrounding medium.* In very still water in tanks they often form layers extending over
a considerable area, the lower strata sustaining by their buoyancy the superimposed
layers, which are even and regular to a remarkable degree (Pl. I. fig. 10). Their
buoyancy is readily affected by a variety of conditions, especially by adulteration of the
sea water in which they float. In impure sea water+t and in fresh water they sink, as
they also do in alcohol, in which fluid they rapidly become opaque. Dead eggs never
float, and dying eggs, though remaining translucent, lose their buoyancy. Healthy eggs
are rapidly affected by unhealthy or putrid ova in their vicinity, a fact showing that the
zona radiata is pervious, and that endosmosis and exosmosis readily take place, as indeed the
absorption of water by the partially desiccated ova of the cod (vide p. 681) clearly shows.
In demersal and pelagic ova unhealthy or dying eggs are readily recognised by the
opacity of their contents ; and an offensive odour, if the eggs are in masses, indicates that
they are dead. Small groups of demersal ova, such as those of Cottus and Cyclopterus,
when dead, may be kept for many weeks in still water in a flat vessel without undergoing
much change in outline, though of course opacity is complete.
Fertilisation.—With very few exceptions (eg., Gambusia patruelis,t Sebastes
norvegicus, and Zoarces viviparus) the ova of Teleosteans are fertilised after expulsion
by the shedding of the milt, on the part of the male, in their neighbourhood. The rapid
diffusion of the milt in water by the serpentine movements of the spermatozoa is very
striking—they spread through a large area, and in tanks used for artificial fertilisation and
rearing it is difficult to keep ova in an unfertilised condition if sperms can by any
possibility find access through the supply-tank.§
In demersal ova deposited on the sea-bottom, on zoophytes or shells, or (in littoral
forms) beneath shelving rocks, in hidden nooks of tidal pools, and in some cases in
nests constructed by the male fish, fertilisation is usually ensured by the proximity of the
male, which may even carefully guard the ova during development, as is notably the case
in Cyclopterus lumpus (vide No. 107, pp. 81, 82); but even in this species masses of eggs
occasionally are found whose fertilisation has not been accomplished. This may some-
times happen in the case of pelagic ova, though experiments at the Laboratory have
shown that eggs of haddock may remain for a considerable time unfertilised, and yet be
* See HensEn’s observations proving that pelagic ova are widely scattered in the sea (No. 65, p. 449).
+ Vide No. 104. t No. 141, p. 461.
§ As occurred to Professor Ewart and Mr Brook at the Rothesay Aquarium, and also with Motella in the St
Andrews Laboratory.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 691
successfully fecundated—a series of ova of the species named being fertilised sixteen
hours after oviposition; and in the case of the ova of the herring from the deck of a
fishing boat, G. Brook states that forty-eight hours have been allowed to elapse, yet fertil-
isation was found to be successful.
More uncertainty probably exists in the case of pelagic ova, which after expulsion are
never quiescent, but may travel over large areas, so that at times their fertilisation must
be a matter of chance. The fishes at the spawning season congregate, it is true, in vast
numbers, males and females thus herding together; but ripe females may occasionally
shed their ova where it is problematical whether sperms will ever reach them, and in this
way we can account for the quantity of dead eggs of plaice and cod which Hensen found
while dredging in the inner bay of Kiel (No. 65, p. 429), though changes in the nature of
the water have also to be taken into account. If no spermatozoa reach them within a
limited time after extrusion, pelagic eggs lose their glassy transparency, and descending to
the bottom assume the white opacity and wrinkled appearance of dead ova. In demersal
forms, with a denser capsule, the unhealthy or dying condition is not so readily seen;
but opacity of the contents, and especially an increasingly offensive odour, if in masses,
are unmistakable indications of loss of vitality.*
The relation of the micropyle to effective fertilisation has been already treated of ;
and many authors regard its position as of the highest importance. GeERBE, indeed,
satisfied himself in the case of the trout that this position is always superior, and
he took pains to secure this condition when performing artificial fertilisation (No. 57,
p- 330). In the uppermost segment he found after fertilisation that a granular layer is
formed by a process of thickening, so that a “ nuage vague ” condenses as a circular area
always in relation to the micropyle. GERBE would extend the observations he noted in
the trout to the ova of Teleosteans in general, and certainly in many demersal forms the
blastodise concentrates in the uppermost segment, and the micropyle is stated to be
uppermost ; yet in pelagic eggs the disc would appear always to be formed at the inferior
pole, and in such eggs if the constancy of the position of the micropyle be well founded,
it must be no longer uppermost, but on the under side of the egg, and such is affirmed to
be the case, though there are difficulties in the way of such an affirmation, and many
reasons for holding that the position is not necessarily constant.
Demersal ova do not show a uniformity in the situation of the micropyle, for in the
ega-tubes of Perca it is not uppermost, but directed to one side, so that it opens into
the lumen of the cylinder; and Grrpe found that it occupies a like position after
fertilisation in Salmo furio, the capsule he says, moving through a quadrant, so that the
micropyle is no longer uppermost; “this change simply alters the respective positions of
the cicatricula and the micropyle, and when accomplished the phenomenon to all intents
and purposes is ended” (No. 57, p. 331).
* The ova of Osmerus eperlanus would seem to become opaque very rapidly, for CUNNINGHAM notes that the
unfertilised eggs sank to the bottom, remained unattached and free, and became opaque-white shortly after expulsion,
though at first they were of a translucent yellow (No. 49, p. 293).
692 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
The artificial fertilisation of the eggs of osseous fishes is easily performed, it being
only necessary to apply ripe spermatozoa (PI. I. fig. 9) from the male to mature ova
placed in water. If ova and the male element be placed in the same vessel of water, the
process is accomplished in a few moments. The exact mode by which it was really
accomplished remained unknown until Ransom not only saw and truly interpreted the
micropylar opening, but watched spermatozoa make their way into the aperture.* “TJ
saw,” he says (No. 127, p. 461), ‘an active spermatozooid enter the apex of the funnel,
and disappear as if inwards ; a quarter of a minute more had not elapsed before the bright
circle which marks the aperture became indistinct from shortening of the funnel; during
the next two minutes I saw three more spermatozooids enter the apex and vanish
apparently inwards.” Notwithstanding the clear and unmistakable observations pub-
lished by Ransom, the process of fertilisation is one about which much discussion has
taken place. Kuprrer, as already mentioned, has even doubted that the micropyle
plays any essential part in fertilisation (No. 87, p. 179); and Borck has advanced a
theory of endosmosis which is somewhat like the explanation Newport put forward in one
of his earlier treatises, when, having failed to detect in the ovum of Rana any perforation
or fissure by which sperms could find access to the egg-contents, he said that mere contact
with the external envelope must suftice for fertilisation, as he never found spermatozoa in
contact with the yelk-membrane, or even within the substance of the external envelope
(No. 112, p. 203). This endosmotic theory Newport afterwards abandoned, and adopted
the opinion which Dr Martin Barry had put forward—in accordance with the views of
LEEUWENHOEK, and Prevost and Dumas (No. 121), that the spermatozoa penetrate bodily
into the ovum (No. 21, p. 309). Ransom’s explicit account decides the matter, the situa-
tion and structure of the micropyle clearly indicating its purpose, viz., the admission of
the spermatozoa to the germinal elements within the ovum (No. 127, p. 462). G. Brook,
again, has recently affirmed that in Clwpea spermatozoa enter on all sides. The interesting
question remains as to whether one or more spermatic bodies are concerned in the normal
fecundation of a single ovum. The presumption that one spermatozoon suffices is
strong, but there are peculiar difficulties in the case of the Teleostean ovum in actually
observing the fact. The entrance of these bodies has been watched in many Inverte-
brates, and one spermatozoon is usually found competent to effect fertilisation, though
SELENKA found (in Towopneustes variegatus) that while one usually enters, several may
find access, and normal development still follow. Three or four indeed sometimes enter,
as Herrwie and Fou observed in the same species, and the separate pronuclei formed by
each usually fuse with the single female pronucleus; but they found that subsequent
cleavage was irregular (No. 66). In Petromyzon CauBeria’s investigations show that
one sperm only enters, the enlarged head-portion separating at the outer micropyle from
the tail which is left behind, while the head penetrates the yolk or rather passes along a
protoplasmic process, which penetrates the yolk and reaches the female pronucleus at the
inner extremity (No, 38, p.464). Kuprrer and Beyeck®, again, found that several sperms
* Doyére had previously seen the micropyle in Syngnathus,
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 693
may enter in this form (No. 89). In osseous fishes a similar condition would appear to
obtain, one spermatozoon being suflicient ; but as this does not plug up the micropyle,
others may also enter, indeed, Ransom observed this in Gastrosteus. “I watched closely
one egg,” he says, “‘ which was placed with the micropyle in full face, so that the aperture
at its apex was well seen. Spermatozoa approached and entered the funnel, and
one was watched till it disappeared, apparently in the direction of the interior of the
egg, Just at the moment when it seemed to occupy the aperture at the apex of the
micropyle. Immediately after the depth of the funnel began to diminish, and a
breathing chamber commenced to form; two or three more spermatozoa were, less
distinctly, seen playing about in the apex of the funnel as it was shortening; one of
them appeared to become still before it vanished apparently inwards” (No. 127, p. 461).
The exaggerated length of the micropylar funnel, which Ransom describes in Grastrosteus
as enabling it to dip into the granular discus proligerus, has not been described in other
Teleosteans. Neither ANDRE nor GERBE mention it in the trout, nor does His show it
in the trout or salmon; while in pelagic eggs the micropylar eminence, though distinct,
is not by any means prominent (PI. I. figs. 11-14). A lengthened micropyle is indeed
unnecessary, the mere presence of the spermatozoon within the ovum being the
essential point. The actual entrance of sperms has been seen in very few Tele-
osteans. Ransom, as already noted, saw them occupying the external orifice of the
micropyle, and ANDR# speaks of observing a sperm apparently entangled, in the micro-
pylar canal, by the jutting ends of the radial strize, which appeared to him to serve
for securing the sperm after its entrance (No. 4, p. 201); but there seems to be no
column of protoplasm facilitating the passage of the sperm from the micropyle to the
female pronucleus, such as CaLBERLA describes in Petromyzon planeri. The head of
the sperm in this form separates from its flagellum, and passes along the proto-
plasmic column, which withdraws from the micropyle (CALBERLAa’s dussere Mikropyle),
and the sperm proceeds through the neck of the column (distinguished as the inner
micropyle) to the enlarged central termination, where the “eikern” or female pro-
nucleus is seated. Here conjugation of the two pronuclei is effected (No. 38, p. 458,
Taf. xvii. figs. 5, 6, 7, and 8). Possibly the preformed discus proligerus may repre-
sent this column; and in those Teleosteans in which no dise is formed, the distance
between the inner orifice of the micropyle and the protoplasmic cortex of the vitellus
is insignificant. The spermatozoa of Teleosteans seem to be of the ordinary type,
and show, so far as observations go, little difference in structure—the usual head
or enlarged portion being distinguishable from the hair-like tail or flagellum (PI. 1.
fig. 9).
Polar Globules.—The details of the phenomena of fertilisation in osseous fishes are
probably not unlike those in forms more fully known. Horrman has deseribed the
formation of the pronucleus and ejection of a polar globule in Scorpena, Julis, and
Crenilabrus, and he states that the globule closes up the orifice of the micropyle,
and prevents the admission of other sperms after that of the single sperm which
694 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
accomplishes fertilisation.* He, however, states that the extrusion of polar bodies, the
disappearance of the nuclear spindle, and the aggregation of the germinal area may
take place independently of impregnation. Kriycstey and Connt describe and figure
a polar globule in the egg of the cunner apparently after maturation. The globule
appeared in the centre of the aster, and passed through the micropyle. List recently
does the same in Crenilabrus pavo, the body being globular at seven minutes and rod-
like at thirty minutes.t Ryper noted in the ovum of Gadus morrhua a minute
granular papilla projecting from the early germ, and looked upon this as representing the
polar cells derived from the germinal vesicle (No. 141, p. 477). In Trigla gurnardus,
twenty-five minutes after the addition of sperms, a somewhat cylindrical nuclear body
has been observed in the superficial protoplasm (Pl. I. fig. 17, a). It exhibited very
slow amceboid movements, and five minutes after it was first noted it had shortened
and contracted in the mid-portion as if dividing into two—a wide granular border
extending round it (Pl. L. fig. 17, 6). Three minutes later the two separating parts
closely approached, and the body became still more contracted and compact—the
granular margin also becoming less (PI. I. fig. 17, c); but the median cincture was still
plainly marked ten minutes later (PI. I. fig. 17, d). A side view of a similar structure
in another ovum exhibited two spherical nuclear bodies enveloped in a vase-shaped mass
of protoplasm, and from the centre of its wide upper surface radial striations diverged
(Pl. I. fig. 17, e). No similar appearance has been observed in other pelagic ova seen by
us. Mr CunnincHam was more fortunate with the ovum of Pleuronectes cynoglossus,
and he describes a polar globule in this species.§
The more obvious features in the living ovum after fertilisation are—(1) The
meridional streaming of the cortical protoplasm to the animal pole. (2) The formation,
or, in certain forms, the visible increase in the size of the blastodise, and its assumption of
a more definite contour. (3) The disappearance of the minute clear vesicles which stud
the entire cortex of the vitellus, probably as a consequence of the transference of the
protoplasm to one pole—by which they are carried to the region of the disc. In many
forms a change in the optical appearance of the yolk is seen. Ransom noticed this, and
says that the increased clearness and translucency of the yolk is in part due to distention
and greater transparency of the enveloping layer (No. 127, p. 458); indeed, the whole
ovum after fertilisation assumes a brighter and more tense appearance. Finally (4), a
space slowly becomes apparent between the vitelline globe and the inner surface of the
zona radiata, so that the egg-contents are no longer closely applied to the capsule, as in
the unfertilised ovum.
Probably the foregoing features mark the fertilised condition in all Teleostean ova ;
but there are many forms in which, for various reasons, they cannot readily be discerned.
* This closure of the micropyle is perhaps incomplete, as the subsequent formation of a perivitelline space is
due to the entrance of water in the main through the micropyle, though it may also enter by the general surface.
+ Loe. cit., footnote, p. 190. t Op. cit., p. 597, fig. ii. d.
§ Op. cit., p. 131,
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 695
Especially is this the case in ova which show a preformed discus proligerus. In the pike,
for instance, LEREBOULLET states that both are alike, save in the formation of a “ disque
huileux” which collects in the fertilised egg, as GeRBr also describes in the egg of the
trout, two hours after fertilisation, the circular germinal area appearing as if enclosed
in a “crown of oil-globules” (No. 57, p. 330); yet even this feature may appear in the
unimpregnated egg, and it cannot therefore, as LEREBOULLET confesses, be traced to the
action of the sperm (vide No. 93, p. 478). The fertilised ovum in pelagic forms (e.g., cod
and gurnard) is more readily distinguished, as the segregation of the protoplasm is plainly
visible within an hour or two after fertilisation; but the transference is not to the upper
pole, as in a large number of demersal forms, but to the lower pole, where the patera or
flattened disc is formed of clear, straw-tinted protoplasm containing minute spherules,
which are especially numerous at the base and periphery. During the process of segrega-
tion the contour of the vitellus becomes very distinctly corrugated—an appearance pro-
duced by the streaming of the protoplasm along definite meridional lines; and pelagic
forms are especially favourable for observing this polar transference. Ransom, in common
with other observers, wholly failed to detect this movement (No. 127, p. 458), though he
says that the granules often form radial lines round the margin of the concentrating dise
(Ibid., p. 459). Besides passing along the superficial areas, much protoplasm probably
also glides in the deeper strata of the vitellus to the base of the germ during the first
hour after entrance of the sperm. Such streaming of the protoplasm towards the disc has
been noted by many observers, and recently Kowatewsky has described it in Carassius,
Polyacanthus, and Gobius (No. 86). In two hours or more, according to the temperature
and other conditions, a plano-convex disc is formed, composed of an almost homogeneous
matrix. The dise in the fertilised ovum is always well defined and prominent, and
continues to receive additions of protoplasm, so that it increases in size, and becomes more
pronounced; whereas in the unfertilised ovum, when a disc is formed, it becomes “ vague,
irregular in outline, and loses coherency” (No. 57, p. 330). The primary segmentation-
nucleus has rarely been detected in the blastodise before cleavage, granules and colourless
vesicles alone appearing in its matrix. The breathing chamber gradually becomes more
distinct; but this may also happen in the unfertilised condition, as Ransom found that such
ova may, after being in contact with water for an hour, show this marked interspace. Its
formation, as well as the concentration of the disc, Ransom holds to be only indirectly
due to the spermatozoa, which may render more easy and rapid the influx of the
surrounding medium into the egg (No. 127, p. 463). The same observer carefully studied
the formation of this space in Gastrosteus, and states that it first appears close to the
micropyle, whence it “ gradually extends over the rest of the yolk-ball, being complete in
three to five minutes after the spermatozooids have been applied” (Jbid., p. 457); but ina
note at the foot of the page he says that water may enter more freely, and the chamber
arise simultaneously in the ova of other fishes. Newport, who was the first to signalise
this perivitelline space, speaks of it as “ respiratory,” and being in Rana “‘at first but a
small area” (No. 112, p. 187), a view coinciding with Ransom’s upon the same ovum, for
696 PROFESSOR W. C. MINTOSH AND MR E. E. PRINCE ON
he believed he saw it arise, just as in Gastrosteus, near the micropyle. Most recent
observers, including List, describe this perivitelline space in Teleostean eggs. To
what is the formation of this chamber due? Does the vitellus, which before fecundation
fills up the intra-capsular area, diminish, or does the external capsule really enlarge? On
the one hand, RaNsom maintains that the yolk-sac or capsule enlarges (No. 127, p. 457);
while, on the other hand, Gerse believes that, by the contraction of the vitellus, this
“zone of separation ” is produced (No. 57, p. 330). Keser has further surmised that part
of the contents of the egg may flow out through the micropyle (No. 77), and the egg-
mass would thus decrease. Kuprrer considers that both the first mentioned phenomena
happen, for he says that in Clupea not only does the yolk contract, but the capsule
enlarges by as much as one-quarter of its diameter (No. 87, p. 185). A still more
marked increase in size LEREBOULLET noted in the egg of Perca, which, he says, by
absorption of water through the radial tubes acquires a volume twice that which it had
before extrusion (No. 93, p. 471). Usually, however, the enlargement of the Teleostean
ovum is so small as not to be readily noticed.
Movements of the Yolk.—The curious movements of the vitelline mass, which have
been described by many observers, and are stated by Ransom to be “the most striking
phenomena which follow on the entrance of the spermatozooids into the egg” (No. 127,
p. 463), are not visible in all Teleostean ova. At any rate, if performed at all, they are
obscure, or so imperceptible as to have escaped notice in pelagic ova, while in demersal
ova they are occasionally not exhibited—LeEresouL.er indeed affirming that in Perca
fluviatilis the egg-contents remain unmoved, and at no time show the intra-capsular move-
ments so remarkably distinct in Hsox (No. 93, p. 503). He further says—‘ TI have not
seen it (the rotatory movement) in the white fishes, of which I have observed many species,
and M. Voer has not noticed it in Coregonus.” In addition to the undulations, or
“ oscillations ” as Ransom terms them, which usually pass like a wave of contraction from
one pole * to the opposite pole, and occasionally along the equatorial line, producing a
dumb-bell outline in the latter case, there are rotations of the vitellus en masse. RANsoM
did not observe any rotation in Gastrosteus, which exhibits the oscillations very distinctly,
nor did he in other ova, though he admits that such movements on the polar axis were
not improbable. LEREBOULLET again speaks of another movement, in fact, a simultaneous
double movement: the vitellus, he says, “ exeree un mouvement de rotation sur son axe et
un mouvement de translation autour de la coque” (No. 93, p. 497). These motions seem
to continue during the early progress of cleavage, but cease,according to LEREBOULLET, when
three-quarters of the yolk-surface are enveloped. He describes at this later stage, in
Esow, an alteration in the form of the vitellus; it elongates and becomes pear-shaped, the
narrowest diameter circumscribing the part of the yolk not yet covered by the extending
blastoderm. BamBrke, in Leuciscus (2), described the same change of shape, and speaks
of the opening (the blastopore, or trow vitellaire of C. Voer) as resembling the mouth of
* Ransom says the pole at which the movements commence is that resting on, 7.c., in contact with, the capsule ; but
this can hardly be so.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 697
a balloon (No. 20a). The change of outline BAMBEKE attributes to epiboly, the blastoderm
squeezing the fluid yolk out of shape; and this is not improbable, for in various pelagic
ova the naked yolk, v.e., that part not yet covered, projects boldly from the blastopore
like a plug pressed out from the diminishing aperture. The change in shape
might be attributed to the contractility of the yolk—an inherent property according to
Reicuert (No. 134); but there is much reason for holding that the active agent is the
ameeboid protoplasmic cortex, or the blastoderm itself external to that layer. A most
remarkable phenomenon was observed by LereBouLter in the ovum of Hsow at the stage
just referred to, when the usual rotation is perceptibly diminishing, for he states that
the blastoderm seemed to continue its rotation “as if disconnected from the yolk, and
the latter continued to turn from right to left as though inside a loose sac” (No. 93,
p. 491).
What the significance of these varied movements really is cannot be definitely stated;
but that they are connected with the separation of the germinal matter from the food-
yolk proper, as RANSOM surmises, seems very probable. Ransom, indeed, would go further,
and regard them as a form of contractile movement, not remotely connected with seg-
mentation (No. 127, p. 495); and it is noteworthy that these movements cease when the
germinal matter has, for the most part, separated from the trophic element in the
vitellus. The yolk alters its form soon after fertilisation, as LEREBOULLET observed in the
pike; and he refers to a movement of the constituent elements of the egg—the marked
flattening of the spherical yolk, which now becomes elliptical (see No. 127, pl. i. fig. 17),
while the blastodise projects prominently from its surface.
Whether the yolk-matter itself, or the protoplasmic envelope outside, really produces
the rhythmic contractions referred to, the phenomena depend, as Ransom found, upon the
presence of oxygen in the surrounding medium, while carbonic acid produces total cessa-
tion or a marked repression of these movements (No. 128, p. 237). They seem to demand
less oxygen than cleavage proper (No. 127, p. 495), though the amount of oxygen used is
small; and Ransom did not succeed in obtaining chemical evidence as to the products
of the oxidation which undoubtedly goes on.
The conclusion that all the movements collectively known as yolk-contractions are
connected with the polar segregation of the germinal protoplasm, is probably near the
truth. That their existence, or at any rate their vividness, is correlated to peculiarities in
the early development of the germ there is no proof, and Ransom’s conclusion is very
much at variance, indeed, wholly opposed to the facts, when he says that such movements
in Esox and Gastrosteus are connected with rapidity of development (No. 127, p. 495).
These forms, instead of hatching in a shorter time than those with slow or indistinct con-
tractions, have an embryonic development unusually prolonged, so that the reverse of the
above conclusion is really true, viz., that the ova in which these movements are not
merely indistinct but imperceptible, are of all forms the most rapid in development,
and of such rapidly developing eggs those of the Gadidz and Pleuronectide are marked
types.
VOL. XXXV. PART III. (NO. 19). 5 u
698 PROFESSOR W. C. M‘INTOSH AND MR FE. E. PRINCE ON
IV. SEGMENTATION.
At the time segmentation begins (always within a few hours after fertilisation)
the process of segregation is to a great extent completed, and the germinal disc is
defined as a thickened patera of clear protoplasm lying upon the yolk in those forms
whose upper segment is the animal pole, or depending from the yolk in those ova
with an inferior animal pole, and separated by an intermediate stratum, which differs
both from the yolk and the germinal matrix. Thus ova of the haddock, fertilised at
2 p.m. on 23rd March 1886, showed at 8.50 P.M. a uniform prominent mass or cap of
protoplasm without trace of segmentation. At the margin were numerous protoplasmic
processes, rising in some cases on the surface of the yolk into globules. On the second
day the rim of some of the granular spheres projected beyond the dise at the lower pole.
Whether the separate cells, seen during development, in the perivitelline space are
due to these projections is unknown. In the cod, again (see Pl. X. fig. 9), the spheres,
which differ in size, show minute granules. The nuclei of the spheres are not always
easily seen in the living egg, but with due care can generally be made out.
Ryper is right in saying that the cleavage does not at first go quite through the dise,
the contrary being stated by Kiycstey and Conn. The latter authors noticed marked
amceboid movements at the 4- and 8-celled stages, processes being sent out by the spheres.
In the early stage of segmentation the Teleostean egg shows external larger spheres
and internal smaller ones (PI. IX. fig. 8), just as Janostk* found in Crenilabrus and
Tinea, the internal dividing more quickly than the external. This, likewise, is observed
in the Elasmobranch ege.
We have seen that all the features of the fertilised ovum may appear to some extent
in the unfecundated egg, and though seomentation is usually an indication that fertilisa-
tion has taken place, it is not infallibly so. OxrtiacuEr found cleavage-lines passing
across the germ in an unimpregnated egg of the fowl (No. 113),+ and in Teleostean ova
the dise may break up into segments by an irregular kind of cleavage. Its abnormal
character is soon revealed, resembling as it does the cleavage of unhealthy and dying
eggs, the cells always showing great irregularity, and the protoplasm composing them
assuming a more or less marked opacity or a granular appearance. Both in size and
shape LerEBouLLer found that these abnormal cleavage-segments differed from the
normal (No. 93, p. 485).
The Cortical Protoplasm.—tThe blastodise is formed by the segregation at one pole of
protoplasm, which, moreover, constitutes a superficial and tenacious layer around the
vitellus. This layer is itself derived by centrifugal transference from the scattered proto-
plasm mingled with the general matrix of the yolk, a phenomenon which recalls the
formation of the periblastula in the crustacean ovum, such as that of Astacus. In this ovum
* Archiv f. Mikr. Anat., vol. xxiv.
+ BiscHorr (Ann. d. Sci. Nat., iii. sér., Zool., t. ii.), Hensen (Centralblatt f. die Med. Wiss., 1869), Kipp (Quart.
Jour, Micr. Sci., xvii., 1877), and others have confirmed OrLLacueEr’s observation in other forms, especially Mammals.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 699
the protoplasm interfused with the yolk also collects at the surface, though it is not
visibly separated by a line of demarcation, and can only be recognised by its texture and
property of readily staining. Ere long it completely separates from the granular deuto-
plasm, and forms a superficial blastodermic layer enveloping the yolk.* In the same
manner a protoplasmic cortex, like the periblastula just mentioned, forms an equal layer
over the yolk in fishes’ eggs, but is not at first sharply defined, though later it is so.
Batrour observes that in Elasmobranchs the dise is merely a part of the ovum in which
the protoplasm is more concentrated, and the yolk-spherules smaller than elsewhere.
In the ova of the haddock on the second day the blastodise shows small “ oil-globules ”
amongst the protoplasm between the spheres, and the dise presents a pale salmon-tint by
transmitted light. Usually it appears to consist of homogeneous protoplasm, with numerous
small spheres of oil or indifferent fluid and scattered granules. In Clupea harengus no
cortical layer is present before segmentation, according to Kuprrer (No. 87, p. 179), nor
is a blastodise preformed, this latter feature being shown also by Gadoid and other
pelagic ova, though in these eggs a cortical layer is well defined before fertilisation.
Notwithstanding that the cortex seems thus sharply marked off from the yolk, there is
good reason to believe that the centrifugal movement of the deeper interfused protoplasm
does not cease when the layer is formed, and Kier refers to this process as the feeding
of the cortex upon the yolk for purposes of growth (No. 79). Batrour also speaks of
certain nutritive elements of the yolk as being converted into protoplasm (No. 11, note
at foot of p. 679), and Kuprrer (No. 88, p. 214) and Rrengck (No. 137) have adopted a
similar view, as also more recently has G. Brook (No. 30).
No nuclei can be detected in the cortex; but clear structureless spheres occur in
small groups, or singly over its surface, and these coalesce later, and form larger spheres,
which are found at the base of the blastodisc during segmentation. RypEr has
determined their composition to be that merely of an indifferent fluid (No. 141, p. 467).
Outside this cortical protoplasm Ransom distinguishes a delicate homogeneous layer, his
“inner yolk sac,” which is not possessed by the more immature eggs. In “ the smallest
intra-ovarian ova” examined in saliva, he says “the yolk is granular and irregular, not
smoothly defined as it would be were an inner sac present” (No. 127, p. 442); and in ova
two-thirds their full size, also, he failed to perceive it. When intact it seems able to
resist osmotic currents in Salmo salar, and it varies in bulk, being unusually thick in the
ruffe (Acerina) (Ihid., p. 453).
Such an inner-sac would appear to be absent in Gadoid and similar pelagic ova,
and indeed in the forms studied by Ransom the precise nature of the so-called inner-sac
is a subject for further investigation. He regards it as a membrane, as performing
contractile movements, and as folded in along the lines of blastodermic cleavage
(No. 127, p. 479).
It is difficult, however, to conceive a structure, meriting the name membrane, envelop-
ing yolk and germinal dise so closely as to be almost inseparable, and involved in the
* Vide Reronennacn, “ Die Embryonalanlage und erste Entwickelung des Flusskrebses,” Zeit, 7. w. Z., xxix., 1877.
700 PROFESSOR W. CO. M‘INTOSH AND MR E. E. PRINCE ON
cleavage-process. The view that it is simply the cortical protoplasm, and not a definite
membrane (vide No. 122, p. 445), is supported by certain facts which Ransom mentions, for
he speaks of the inner face of the yolk-sac as ill-defined and closely connected with the
formative yolk (No. 127, p. 433), and that on rupture the shreds change their form
(Ihid., p. 478) and are frequently drawn out into thread-like prolongations (p. 468) ;
while he further describes it as continuous with the blastoderm (p. 467), and admits
that, as it ultimately shares in the cleavage process, it ‘‘ may to that extent be considered
a part of the formative yolk” (p. 433) or germinal protoplasm. ‘The presence of a
like membrane investing the germ has been maintained by ScHENK in the ovum. of
Elasmobranchs (No. 142), but other observers, including Leypiec and Batrour, have
denied its existence. The yolk-sac described in the hardly mature ovum of Rana by
Cramer (No. 45, p. 33) as a distinct membrane before cleavage begins, is merely the
more consistent superficies of the yolk-ball, and not a separable structure. The fact
seems to be that what Ransom regards as a distinct membrane is the cuticular stratum
of the protoplasmic cortex, and is therefore less of the nature of a sac than that of an
external layer, slightly more consistent than the protoplasm underneath. Ransom
admits that in a sense it may be so regarded (No. 127, p. 433); and it is adherent to
the blastodise, over the outer surface of which it passes, and probably constitutes the
clear matrix, as distinct from the granules of the dise. It forms folds at the margin of
the clefts during segmentation, “ reminding one,” he says, “of the ‘ Faltenkranz,—
described by RetcHErT and by Scautrze in the frog’s egg,”—these folds being in fact
the familiar corrugations produced by the cleavage and separation of the blastomeres.
Sections through the dise at this time show no investing membrane, though it is true
that the cortex takes a slightly deeper stain than the underlying matrix of the
blastomeres, but the one insensibly passes into the other. Barour also found, in the
ova of Elasmobranchs, that the surface was very susceptible to stains, and that the sides
of the furrows took a deep colour ; but such appearances did not suffice, in his view, to
demonstrate a separate membrane, so that in Teleosteans, also, we must, with LEREROULLET,
affirm “labsence de membrane propre” (No. 95, p. 13) outside the blastoderm. That
Ransom’s layer is simply the cortical protoplasm is shown by the fact that on rupturing
it no coherent layer beneath held in the contents, but the food-yolk immediately flowed
out (No. 127, p. 465). Ransom himself also speaks of the formative yolk as a layer invest-
ing the yolk-ball. We cannot, therefore, recognise an inner yolk-sac as such, for the
somewhat viscid and coherent layer, which alone appears to envelop the yolk, would
behave precisely as Ransom’s yolk-sac did, when in contact on its inner side with the
semi-fluid yolk, and on its outer side with the watery perivitelline fluid. The whole
of this cortical protoplasm, however, does not enter the blastodise and undergo seg-
mentation ; a considerable part never reaches the animal pole, but permanently clothes
the yolk-globe, and part of it may temporarily form a supplementary disc at the
vegetal pole, as Kuprrer saw in Clupea (No. 87, p. 185); while a portion remains as a
sub-blastodermic stratum, and becomes thickened as a peripheral wall, the nuclear zone,
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 701
or periblast proper, around the margin of the disc. A thin stratum may also be
distinguished creeping over the segmenting blastoderm as an external pellicle, referred
to before as probably homologous with Ransom’s inner sac, and this layer sends down
processes which fill up the interspaces between the large primary blastomeres
(Pl. HU. fig. 1, p). This appearance, which is distinctly seen in sections of the early
blastoderm, may, it is true, be really the dilute plasma, or perivitelline fluid, penetrating
the inter-blastomeric fissures, though more probably it is periblastie protoplasm, forming
an intermediary substance, such as LEREBOULLET distinctly recognised (No. 93, p. 493),
and as E. vAN BENEDEN figures (No. 25, pl. iv. fig. 7, &c.).
To sum up briefly, we may say that the protoplasm interfused with the food-yolk
continues from a late intra-ovarian stage to collect superficially as a cortical layer, and
forms—
(1) The blastodise at the animal pole, and in rare cases a transient pseudo-dise at
the vegetal pole (Pl. IL. fig. 1, bdm).
(2) The intermediary, or sub-blastodermic layer (Pl. II. fig. 1, p').
(3) The thickened marginal wall or periblast-ring (PI. II. fig. 1, per).
(4) The superficial envelope and inter-blastomeric substance of the segmented dise
(PL te nel; 7’).
(5) The sole intra-capsular envelope of the deutoplasmic globe or yolk, prior to the
epibolic extension of the blastoderm (PI. II. fig. 1, p’).
The Subgerminal or Nutritive Disc.—Reference has been made to the layer of proto-
plasm beneath the blastoderm proper (PI. II. figs. 1 and 15, a, b, c, d, e—ep), and it has
been distinguished from the periblast proper, 7.e., the thickened peripheral wall, and the
nuclear zone round the margin of the disc, by various names, such as ‘‘ intermediary layer”
(BaMBEKe), “ disque huileux” (LEREBOULLET), “ Rindenschicht” (Hrs), “ median lens or
lentille ” (E. van BrnepEN); while other observers, e.g., HAECKEL and Ransom, have not
recognised it, the latter indeed saying of the blastodermie surface in contiguity to the
yolk, that it seems to be merely “ the corpuscles resulting from segmentation in contact
with the fluid-yolk” (No. 127, p. 467). It appears to arise like the rest of the protoplasmic
envelope of the yolk by superficial segregation, though BAMBEKE attributes its formation
to a centripetal extension of the peripheral annulus; but LeREBoULLET’s statement
probably represents the origin of this sub-blastodermic stratum more truly, when
he says that in Hsow and Perca it arises simultaneously with the disc, these nutritive
elements, as he calls them, following the plastic element in their migration to the
animal pole (No. 93, p. 11), and at the earliest stages may, as Kuprrer supposes, give
nutriment to the germinal dise (No. 87, p. 194). Ransom did not distinguish a stratum,
however, but speaks of “a collection of dark oil-granules distinct from the large drops
which float in the yolk.” He saw granules and globules of oil below the disc, and as
these are consumed during the development of the germ-mass, it is probable that a
kind of yolk-digestion goes on,
702 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
LEREBOULLET, Kuprrer, Rreneck, and OELLACHER all noticed the accumulation of
globules under the dise in impregnated ova ; and BAMBEKE (who quotes them) says these
indicate food-particles for nourishing the germ. GERBE figures a crown of oil-globules
around the periphery of the disc (No. 57, p. 330, pl. xii. figs. 3 and 4, b); while
OELLACHER speaks of his lenticular germinal mass as including a lower layer which
imprisons many oil-spheres, and at times is seen to be separated by a distinct contour
from the disc. OELLACHER regards it as part of the blastodisc, and BAMBEKE likens
it to his intermediary layer, though the subgerminal disc has been distinguished
as a separate structure, neither to be confounded with the lower part of the germinal
dise nor with the intermediary layer. LrrEBouLLEer indeed distinctly affirms that
his mucous layer underlies, as a definite membrane, the blastoderm, while it rests
upon the nutritive disc. BaMBexe erroneously likens his intermediary layer to this
stratum beneath LEREBOULLET?’s mucous layer in the trout (No. 20a). In LereBouLLet’s
view, three distinct strata must be recognised at the animal pole—(1) the germinal
dise proper, (2) the mucous or intermediary layer, and (3) the “disque huileux” or
nutritive layer. The separation of the stratum underneath the disc into two layers has
caused some confusion, and the distinction is perhaps unnecessary. It is readily seen
that the lower portion of the intermediary layer will be more fully charged with oily
spherules and granules from the yolk than the portion in apposition to the base of the
disc, but it is needless to separate it as a distinct oily stratum. A subgerminal stratum
is probably not absent in any Teleostean ovum, though less prominently seen in some
(e.g., Gadoids and Pleuronectids) than in others (sow and Gastrosteus), but the
presence of a layer beneath the subgerminal stratum has been noted by very few
observers. We cannot indeed regard LerEBout.et’s lowest (third) layer as separate from
his mucous layer, which has been so generally recognised in Teleosteans. This single
subgerminal layer, in whose lowest stratum oily spheres and granules are numerous, is the
granular layer which Batrour speaks of, though in Elasmobranchs it consists chiefly of
small yolk-spherules, and it is also G6rre’s floor of the germinal cavity (the
“ Dotterzellen”). In Teleosteans it is continuous with the peripheral wall of protoplasm
(His's “ Keimwall”) and the thin periblast beyond, originating in the same way, and
persisting probably by continual renovation, the blastoderm thus feeding upon this
finely granular layer. Kowatewsky regards the intermediary layer as a provisional organ
(op. cit., 1886). We call by the name “subgerminal or nutritive disc” the disc-like
stratum beneath the germ, and it embraces LEREBoULLET’s two layers—the mucous and
the oily stratum; it is the thin central part of BAmprKe’s intermediary layer; it is
OELLACHER’s inner layer, holding many oil-globules, of the “ Rindenschicht ;” and although
OELLACHER speaks of it as more coarsely granular than the dise or layer above, yet
it is derived from it. OxtiacnEr rightly compares his lower layer to LEREBOULLET’S
mucous layer; while BamBerKe also correctly says that both are really his intermediary
layer.
We can therefore distinguish (with BamBexe) at the animal pole only two strata—
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 703
(1) the blastodise, or true segmenting mass; (2) a granular layer, or subgerminal dise not
segmenting, and probably nutritive, and interposed between No. 1 and the vitellus.
V. Tue BLastopERM.
Within one or two hours after the entrance of the spermatozoa, the thickened cap
of protoplasm, either preformed as a discus proligerus, or segregated as a blastodise
proper, undergoes segmentation. The blastodise is readily distinguished with the
naked eye in the more transparent ova as a spot of lighter colour than the yolk
on which it is placed; while under a lower power it is seen protruding as a discoid
prominence at either the upper or the lower pole, according to the particular form.
In certain Salmonide, for instance, the germ always floats uppermost, as it also does in
the sterlet, according to SALENSKY, and in the trout; this being due, according to Ransom,
to the oil attached to the disc, which compels it to float in the upper segment (No. 127,
p- 450).* Ina number of pelagic ova, possibly in all, the dise lies underneath the yolk,
the animal pole being inferior ; but whether superior or inferior, the position is constant
for the species, and there is no actual reversal, such as occurs in Cephalopods, where the
germ and the yolk-pole exchange places at a certain stage. As the vitelline mass revolves
freely in the perivitelline fluid, the germ may often be brought to the upper side by
agitation in the water; but it usually seeks the lower pole at once, and remains there
when the egg is at rest.
Baxrour views the disc merely as a part of the ovum, which is characterised by the
presence of more protoplasm than the rest of the vitellus (No. 10, p. 106); but while
this is so in the Elasmobranch and Amphibian ovum, in the Teleostei the germ is so well
marked and distinct, and, with the exception of some colourless vesicles and a few granules,
so destitute of yolk-matter (apparently consisting of pure protoplasm) that the yolk
becomes rather an appendix than an essential part of the germ.
The same author supposed that the Teleostean yolk at some later stage must be almost
entirely deprived of the protoplasm so abundantly interfused during the early stages,
and this undoubtedly is so, the yolk-matrix before it wholly disappears increasing ‘in
density and coherency.t That the disc owes its origin to fecundation in all Teleosteans,
we have seen to be an error; and the view of Cosrr, which LEREBOULLET adopts (No. 93,
p. 33), is not more tenable—viz., that the dise is derived solely from the divided and
scattered germinal vesicle—for, in some species, the discus proligerus is formed and this
vesicle is seated in its midst. As the segregation of the disc proceeds, and its mass
increases, its colour likewise becomes deeper ; and Ransom believes that it undergoes a
physical change, “ being more solid” than in its earlier condition.
The dise then is the essential part of the ovum, and the yolk is merely supplementary,
* His figures the germ disc of Zsox as uppermost (No. 67, Taf. i. fig. 13); but LEREBOULLET says, “ Sa position est
oblique ou, si l’on vent inclinée & l’équator” (No. 93, p. 481).
+ In a form like Anarrhichas the embryo remains long (several months) within the ovum, and when treated with
alcohol the yolk becomes extremely hard, and apparently consists of a purely albuminoid matrix. This likewise is the
case with the ovum of Salmo salar. Sea water also hardens the yolk of the latter species (vide No. 104a, p. 153).
704 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
though the view is held by many authorities (VAN Benepen, No. 25, pp. 52,53; Horrman)
that segregation is equivalent to cleavage, and that when the disc is defined the ovum
consists of two cells—one being the germ, and the other the yolk. The behaviour
and undoubted function of the deutoplasmic globe is opposed to this view, the separation
of the germinal matter from the inert yolk being protracted and undefined, and wholly
unlike cleavage. Nor in the syncytial yolk has a nucleus been discovered equivalent to
the segmentation-nucleus formed from the fusion of the male and female pronuclei in the
germ. Dr Martin Barry, half a century ago (No. 21, p. 313), noted in the ovum of
Rana a nuclear body, which he described as elliptical, well defined in contour, apparently
granular, and placed within the membrana vitelli (vide Barry’s figure, No. 21, pl. vi. fig.
28, d), but no such additional nucleus is apparently present in the 'Teleostean yolk.* The
emphatically passive and inert character of the Teleostean yolk has already been indicated,
and the real distinction of the active germ from its trophic appendage insisted on.
We have referred to the relation of the early blastomeres and the potential yolk-segments
CuNnNINGHAM speaks of; but however plausible that view may appear during the first
stages of cleavage, it is difficult to maintain such a relation of blastomeres and yolk
when the morula is reached. The disc indeed becomes disengaged from the yolk (GERBE
says it completely separates, No. 57, p. 330), and a series of independent phenomena begin
which concern it alone. We do not now allude to the formation of a true cavity beneath
the disc, as this phenomenon falls to be considered later, but to the embryological
separation between the germ and yolk, when their physical relations are most intimate.
CunnincHam (No, 48), referring to the statement made by AGassiz and WHITMAN
(No. 2) that this separation dates from the 16-cell stage, observes, with greater accuracy
than the two authorities named, that this separation by a cavity is not seen in living
ova at the centre of the disc, and sections prove CunniINGHAM to be right. In sections
the line of demarcation is broken by knob-like processes which project from the
blastoderm into the yolk (Pl. II. fig. 1), and these appear to be masses of protoplasm
in the act of entering the dise, though another interpretation remains, viz., that they are
pseudopodial protuberances.t During segregation and early segmentation remarkable
changes of form are seen in the Teleostean blastodisc—similar to the phenomena SCHENK
noted in Elasmobranchs, and confirmed by Atex. Scuuttz (see Batrour, No. 10, p. 410),
consisting of an alternate rhythmical pullulation and subsequent flattening or subsidence—
a movement which involves the entire mass of the unsegmented disc (so that it seems
to draw together and become compact and prominent). This is shared by the individual
blastomeres in the segmented disc, as the separate cells appear at one time prominent
rounded bodies standing boldly out upon the yolk, at another time as conical or irregular
mounds (PI, X. figs. 9, 10), or again flattened structures, crescentiform in section, their
outline in the last case being less definite, and the entire disc exhibiting a diffuse and
* See Baprant, Comptes rendus, 1864, tome lviii.
+ KowAtewsky noted these transition-elements, and says that all stages can be seen amongst the entoblastic (yolk-
mass) cells forming below the blastoderm—from those which are still in the yolk to those which had entered the
blastodermic elements, and were only at one point of their bases united to the protoplasmic network of the yolk.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 705
expanded appearance. These changes of external form, which are often combined with
an apparent dehiscence of the blastoderm and puckering of the under surface (PI. LI.
fig. 14), are probably due to the inherent mobility of the protoplasm; but are also
connected doubtless with the transference of the cortical matter which has not yet ceased.
They are especially noticeable when fresh cleavage is about to commence, as RANsoM
seems to have observed (No. 24, p. 466).
The primary segmentation-nucleus is rarely visible in the germinal dise,* though
Kuprrer noted it as a clear homogeneous vesicle, fifteen or twenty minutes after fertilisation,
situated in the basal stratum of the blastodise of Clupea (No. 87, p. 206). In the section of
the blastoderm of Gadus eylefinus, at the 5th hour, when two blastomeres are completed,
we see that the nucleus (m) occupies a position slightly above the basal stratum,and presents
surrounding radial structures, apparently prolongations of the nuclear substance itself
(PL IL. fig. 18). When this nucleus has divided into two, each is seen to occupy a central
position in the pair of newly-formed blastomeres. The two blastomeres (Pl. XXVIII. fig. 4)
often show disparity in size, with a more or less distinct reniform outline when viewed from
above. This disparity may be due to unequal segregation of protoplasm, or to more obscure
causes, but the shape of the earliest blastomeres appears also to depend upon the direction
of the first plane of cleavage; for, when this is in the shorter axis of the blastodise, the two
cells are rudely discoidal, and are in contact by their flattened margin; or if in the longer
direction, the result, as in the gurnard, is the production of a pair of reniform cells—the
hilum, so to speak, of each coinciding with the proximal margin. The nucleus in each blasto-
mere is not spherical, but slightly elliptical and flattened, showing indeed as a transparent
almond-shaped body, when viewed in profile, and of a paler hue than the surrounding matrix.
In the living ovum the nuclei are usually very difficult to detect during the earlier stages,
and Ransom failed to make them out (No. 127, p. 467); but, when not diaphanous, the nuclei
may appear, ¢.g., in the 2-cell stage of Gustrosteus spinachia and Trigla gurnardus,
as minute irregular vesicles, like clear vacuolations distributed in each blastomere. The
protoplasm around the central nucleus of each blastomere exhibits a radial disposition
like the figure of the “lines of force” around a magnet (PI. II. fig. 18), but the more
detailed features of nuclear and blastomeric cleavage are of the complex nature charac-
teristic of karyokinesis. Each cleavage begins as a superficial indentation, which in the
case of the first furrow commences in the centre of the straw-tinted pullulation or
granular blastodise, within an hour or more from the first appearance of the dise, and
extends outwards, its course being preceded by puckerings, as though the two masses
were drawing apart, and producing the beaded structure described by Batrour
(No. 11, p. 391). The diverging course of the cleavage-plane is not opposed to the
“Joi centripete” of M. Serres, for the plane penetrates (centripetally) the disc. The
vacuolations which produce the beaded appearance, while most numerous at the margin of
* Ransom failed to make out the primary segmentation-nucleus, and indeed the blastomeric nuclei. Possibly
various species may differ in regard to the visibility of the nuclei, for LeREBouLLer found the nucleus in Perea with
difficulty, whereas in Hsox it was well seen (No. 93, p. 513).
VOL. XXXV. PART. III. (NO. 19). oX
706 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
the cleavage-plane, occur sparsely over the disc, and especially in its basal portion (Pl. I.
fig. 18). They probably have an important relation to the cleavage-process, as BaLrour
thought. In sections they occur as clear rounded vacuolations, but are without doubt
filled with indifferent fluid, and probably are no other bodies than the clear vesicles
scattered over the cortical protoplasm in the ripe unfertilised egg. The vesicles disappear,
as we have seen, with the polar segregation of the disc ; but they really persist, and are
transferred to the disc, where they accumulate (Pl. II. fig. 18), often coalescing and
forming larger vesicles, but not to be confounded with the oily extra-embryonic spheres,
though LeREBOULLET does so, saying—I have seen large transparent spaces like those
M. Voer shows in his figs. 113 and 114 (Embr. of Salmon) produced by oil” (No. 93,
p. 486). It is possible that these vesicles, or rather their clear fluid contents, may render
mechanical aid during cleavage, filling up with their less consistent matter the furrows
formed by the dehiscence of the segmenting blastomeres. After the first furrow, which
is perpendicular to the basal plane of the disc, has produced the first pair of blastomeres,
the pullulation of the protoplasm is marked, each cell becoming increasingly definite,
a feature which Kuprrer regards as indicating the appearance of an equatorial furrow
(No. 87, p. 196, Taf. ii. fig. 15, &e.). Such an equatorial furrow, according to Horrman,
appears before the first perpendicular furrow, and thus the dise would be separated
from the marginal protoplasm as well as from the yolk at the first stage in cleavage.
A complete discontinuity of yolk and germ produced by cleavage does not accord well
with the actual condition in the ovum, and the first furrow would appear to be the
primary perpendicular one. When this furrow has penetrated almost to the base,
for it does not perfectly bisect the disc, as LEREBOULLET long ago noticed (No. 93, p. 481;
see his fig. 18, pl. i.), small furrows directed towards the centre of the disc, appear at
right angles to the first cleavage-lines, followed by the appearance, along the course
marked by them, of a second cleavage-furrow, which divides the two primary blastomeres
into four almost equal segments. Each of the newly-formed blastomeres has a rudely
square outline, its two free outer sides being rounded, while the two inner sides are more
nearly straight lines, and mark the perpendicular planes which are in apposition to the
similar surfaces of the two neighbouring blastomeres. In each blastomere a large nucleus
can be made out, though often with difticulty, as LEREBOULLET noted; but not ill-defined,
as the same author further stated (No. 93, p. 483), for the nuclei appear as homogeneous
hyaline vesicles with a smooth and distinct contour, the bright contents of which are
termed by AvrrBacH the “ ground substance” * (PI. II. fig. 4, a). Nuclear division is
not easy to follow in the living ovum, though blastomeric cleavage is readily observed.
The ovum of sox seems well adapted for nuclear observations, as LEREBOULLET found out
when he contrasted this species with Perca, for in the latter the nuclei had greater
transparency and were thus less readily seen (No. 93, p. 513). In this species (sox)
Kurrrer followed the division of the primary nucleus, and watched the first furrow pass
down between the two newly formed nuclei (No. 87, p. 207).
* Organologische Studien, Breslau, 1873-4.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 707
Around the cleaving nucleus a radial disposition of granules is seen,* the centres of
the radii being the nuclear apices, for the nucleus itself becomes biconical and shows
longitudinal striz prior to the division which soon takes place across its middle or shorter
axis, this transverse separation being followed by the division of the surrounding blas-
tomere. The process indeed accords perfectly with Baurour’s account of the Elas-
mobranch ovum (No. 15, pp. 394-5). Occasionally a blastomere is seen to contain
two distinct nuclei, illustrating indeed the stage of the process figured in PI. II. fig. 2,
a stage which LEREBOULLET also clearly observed, for he says—‘‘ Dans un de ces lobes j'ai
trouvé une cellule qui avait deux noyeaux distincts rapprochés l'un de lautre”
(No. 93, p. 484), and Baxrour similarly speaks of a double nuclear condition (No. 11,
p- 396). Though usually very distinct and centrally situated, the nucleus sometimes
becomes diaphanous, and appears to be absent. Such an enuclear condition is hardly
possible, though Professor Ray LANKEsTER, it is true, speaking of the blastoderm of
Cephalopods, says—‘‘I have most fully satisfied myself that temporarily many of the
segmentation-products are devoid of nucleus” (No. 90, p. 39); and LereBouLLer, when
noting the fact that all through cleavage each blastomere contains a nuclear body, adds
that “often it may be absent” (No. 93, p. 484); while Bampeke could find no trace
of nuclei in Leuciscus rutilus, but accounts for it by the similar refrangibility of the
nucleus and the matrix in which it is situated (No. 20a). This disappearance of the nuclei
is not an uncommon phenomenon in cell-division. Very often (Pl. IL. fig. 1) a body
apparently of the nature of a clear vesicle occupies the place of the deeply-stained nucleus
in sections, or such a vesicle occurs only partly occupied by a nuclear remnant (PI. I.
fig. 1). These unstained bodies were noticed by Batrour, and he felt uncertain whether
they were nuclei imperfectly stained, or nuclei in course of being formed (No. 11, p. 395).
In the living egg the phenomena of segmentation are followed without much difficulty,
especially in pelagic forms. The two primary cleavage-planes are seen to cut each other
at right angles; but the third cleft is parallel to the second (Pl. X. fig. 4). On the
completion of the third cleft the blastoderm consists of six cells, of which the central
pair are larger than the others. At this stage the blastoderm is rudely rectangular, an
outline altered by the next cleft, which passes once more parallel to the second and third
clefts, through the large central cells (Pl. XIV. fig. 8). The size of the blasto-
meres is far from uniform after the 8-cell stage. The 16-cell stage is completed by a
separate furrow traversing each cell and bisecting it, so that the total number of
blastomeres is thus doubled at about the fourth or, it may be, the sixth hour after
fertilisation. It would appear that in the Teleostean ovum, as also in the fowl and
Selachian, the two primary furrows alone are really regular, the succeeding furrows being
in varying degree irregular, so that the blastomeres are not seen to increase with the
* OELLACHER observed the concentration of yolk-spherules round one or two centres in the segmentation-spheres,
but this is not the phenomenon he described, though BALFour understood OrLLacuer to refer to the behaviour of the
ordinary nuclei during segmentation. Ryper also speaks of numerous fine granules aggregated round two centres in
the first cleavage-stage.
708 PROFESSOR W. C. M‘'INTOSH AND MR E. E. PRINCE ON
regularity of geometrical progression. The size of the blastomeres is likewise far from
uniform after the 8-cell stage, and in the 14- to 16-cell stage especially, they vary
very much in size and shape, the outer being large and somewhat rectangular, while those
more central are smaller and ellipsoidal. This distinction between the more external and
the inner cells Batrour noted in Elasmobranchs (No. 11, p. 392), and compared
it to the horizontal furrow which separates the smaller pigmented spheres from the
larger spheres of the vegetal pole in Rana (cf. figs. 3, 4, and 5, pl. xv. No. 11, and our
Pl. IX. fig. 8). The form of the dise varies, changing from the circular outline of the
early blastodise (Pl. XXII. fig. 1) to a more or less regular quadrate figure (PI. X. fig. 9),
and reassuming the circular form when the multicelled stage (morula) is reached (PI. II.
fig. 13, a). The first furrow parallel to the base of the disc passes across the median
horizontal plane at about the 50-cell stage (PI. II. fig. 14), and the subsequent cleavage
becomes very complicated. Owing to the increasing pressure of adjacent cells, the
rounded form of each cell (PI. X. fig. 10) becomes altered, and the polygonal shape is
assumed (PI. II. fig. 19). The size of the blastomeres shows much variability, though
the variation is now within narrower limits. In profile the disc up to this stage has
maintained the plano-convex outline, which is often retained until the 180-cell
stage or later (Pl. X. fig. 10); but when the cells are so subdivided as to appear
almost of one size, a marked bi-convexity is assumed, and upon the yolk a depres-
sion is formed in which the blastoderm rests (PI. II. fig. 2), as it does permanently
in Salmonoids (Leresouier, No. 93, p. 485; OELLACHER, KiErN); but later it spreads
out in Gadoids and other forms, and appears as a flattened plaque in which several
layers of similar cells can be distinguished (Pl. Il. figs. 3 and 15, e). There is
no marked difference in the cells of the various strata, and the blastodermic layers
are not readily distinguished, as they are in Elasmobranchs.* Batrour and other in-
vestigators have made allusion to this similarity in the size and contour of the cells
of the Teleostean blastoderm (vide Batrour, No. 11, p. 551; and LeReBouLLET,
op. cit.).
It is true, as already pointed out, that in very early cleavage the marginal cells are
distinguished from the inner cells by a marked difference in size (Pl. IX. fig. 8);
nor is the distinction lost with the appearance of the horizontal furrows, though it
cannot be due, as is undoubtedly the case in Elasmobranchs and Amphibia, to the
greater proportion of yolk-matter present in the outer germinal protoplasm, for there
does not appear to be any conspicuous difference in their physical character.
In the Elasmobranch blastoderm of about one hundred cells, the ectoderm is readily
distinguished from the endoderm or “ lower layer ” cells by their smaller size, and marked
columnar character. Rreneck + observes that the upper cells of the germ give rise to
a two-layered sensory lamina (or leaf), and that some of the lower cells fall to the bottom
* Ryper, however, speaks definitely of three layers in the multicelled stage of the Teleostean germ ; but this does
not agree with other descriptions by the same author.
+ Archiv f. Mikr, Anat., vol. v., 1869.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 709
of the cavity (germinal cavity). Soon after also the larger cells fall off, and we now get
complete analogy with the Amphibian egg, viz., above the cavity the sensory layer
composed of smaller cells, and below the large cells for the body of the embryo.* This is
not the case, however, in osseous fishes, for on the completion of segmentation, an
epiblastic layer can barely be distinguished: it is not by any means well marked.t
Germinal Cavity.—With the completion of segmentation the blastoderm undergoes
a change of the most striking character. It lengthens out (Pl. I. fig. 17) and soon
becomes elevated from the yolk, so that a chamber ge. (Pl. II. fig. 15, a-d), not
coincident with the centre of the disc, is formed between its under surface and the
vitellus (y) below.t Hitherto the whole of the inferior face of the blastoderm has rested
immediately upon the yolk (y) (see Pl. Il. figs. 1-8) or rather upon a portion of the
yolk-cortex ; but now the inner surface being raised it rests only by its periphery, and
the eccentrically situated cavity intervenes between it and the vitelline mass. In
Trigla gurnardus the sub-blastodermic cavity is plainly visible on the second day,
when the germ covers barely a third of the surface of the yolk.
A cavity has been observed in some Teleostean ova at a much earlier stage; but it is
probably a precocious dehiscence and of minor significance. Such a cavity in the
gurnard may be formed even before the first cleavage is accomplished, and is probably
due to the cleavage-process, as we find to be the case in Amphioxus at the 4-cell
stage. Acassiz and Wurman found a similar cavity in Ctenolabrus at the 16-cell:
stage, while His describes one at the 8-cell stage.§ Such cavities, of a transitory
nature, have been noticed in very many ova; in Acipenser sturio, for example, at
the 6- to 8-cell stage, according to KowaLEwsky, OwsJANNIKow, and WAGNER ;
while Rauber saw it in the Avian ovum at the 4-cell stage (No. 132, p. 6). The last
named observer distinctly affirms that the early cavity he saw is not the homologue of
the later embryonic chamber, generally distinguished as the “ Keimhéhle ;”|| and as this
is a point of no little importance, it is desirable to dwell upon the distinction here
implied. The very existence of a cavity, either “segmentation” or “germinal,” has
been denied by some investigators. It has been pronounced by Donrrz amongst others
(No. 52, p. 600) to be merely an artificial product ; and Kuprrer suggests something of
the same kind, though unwilling to lay stress upon his results, which were negative
(No. 87, pp. 214-16). That the somewhat complex methods now adopted in
laboratory work are calculated to produce occasionally artificial changes in embryonic
* Rreneck also considered that the embryo originated in one point of the peripheral thickening which occurs at
the point of contact between the yolk and the germ.
+ Goetre affirms that there is no distinct differentiation of any of the germinal layers in the multicelled condition
of the dise if we except the outer “ epithelial” (Archiv f. Mikr. Anat., iv., 1868).
t Rreneck, op. cit., observed the central part of the germ lifted off its underlying part.
g It is this cleavage-cavity which Ryper considers as probably homologous with the cavity of the false amnion
(Amer. Nat., xix., 1885, and Jour. Roy. Mier. Soc., Feb. 1886, p. 45).
|| This later cavity BaLrour, in common with most observers, names the segmentation-cavity, though he says it
is not a well-defined chamber, and remarks that “it may even be doubted whether a true segmentation cavity ... .
is present.”
710 PROFESSOR W. C. M‘INTOSH AND MR E. E, PRINCE ON
structures is very probable ; but the recognition of a cavity in the Teleostean blastoderm
has been so general that it cannot be placed in such a category.
We speak of it as a “ germinal cavity,” and do so advisedly, for it is not “the cavity
of Von Barr,” better known as the blastoccel or segmentation-cavity. This latter, which
exists in all segmented germs forming a blastosphere, as in Cylostomes and Amphioxus,
is, we believe, never formed in such pelagic ova as are referred to here, nor indeed has it
been clearly recognised in any other Teleostean ova, with the exception of Leuciscus
rutilus. In this last named ovum VAN BAMBEKE fully describes a true “segmentation
cavity,” though his results are not in accordance with those of embryologists generally.
Van BambexeE himself doubts the existence of his cavity in the germ of the Salmonoids
and carps, though closely allied to the form he investigated, and declares it to be
homologous with the chamber in the ovum of Petromyzon, Acipenser, the Selachians, and
Amphibians. It is true he quotes LerEBOULLET in support of his view, and the latter
undoubtedly does speak of the germ at the close of segmentation as having “
granuleux et la forme d’une sphere aplatie qui repose sur le vitellus” (No. 93, p. 503) ;
but neither his fig. 27, pl. i. nor fig. 3, pl. iii. necessarily imply BamBekr’s results,
nor exclude the existence of the germinal cavity which most authors have seen. The
segmentation-cavity of BamBeKkr, the homologue of Batrour’s cavity (No. 13, pl. xxi.
fig. 1, sc), arises as a space in the midst of the blastodermic mass (No. 20«), at
un aspect
what period he cannot say, though his figure would indicate an early stage,
probably when the blastoderm covers a quadrant, that is at the same time as the
“germinal” cavity, which it also resembles in its non-central position, for it is slightly
eccentric in position, and in front of the embryonic area proper. It is surrounded by
blastomeres—the roof, walls, and floor being composed of cells produced by the
seementation of the disc. The germ, in which it originates, is essentially a blasto-
sphere, for though the floor-cells largely disappear, so that the yolk may seem
partially to form the floor, there is probably never a stage, as BaLrour is careful to note
(No. 11, p. 519), “in which the floor of the cavity is without cells.” BaLrour, it is true,
regards the Teleostean germinal cavity as homologous with the segmentation-cavity
(cavity of Von Barr) in Elasmobranchs and Amphibians (No. 10, i. p. 70); but the
subsequent fate of each of these cavities tells against this homology, for the former is
persistent, whereas the latter chamber is transitory. If the Teleostean germ after
segmentation be a morula, which flattens out, and becomes lifted up, and separated by a
chamber from the appended trophic mass,* resembling in a remarkable manner the
condition in certain Urochordates (e.g., the cauducichordate Pyrosoma), in which no
centrally placed segmentation-cavity occurs (vide Huxiey, No. 738, and KowALEwsky,
No. 86, p. 609), then the presence of such a cavity, and the occurrence of a blastospherical
stage in Teleosteans, must be regarded as problematical.
* That the blastoderm is actually raised up seems to be demonstrated by the fact that separation may for some time
be incomplete, connecting strands of protoplasm being frequently distinguishable in the living ovum and in sections
(PI. II. fig. 15, c), and Ryprr is probably in error when he supposes the cavity to arise as a direct result of cleavage
(No. 141, p. 492).
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 76) bi
BatFour at one time held the view that the floor of the cavity in Selachians was
not truly blastodermic, the floor-cells arising as concretions around yolk-nuclei at the
base of the dise (No. 11), and such a cavity would be a germinal, not a segmen-
tation-cavity like VAN Bameekr’s; but later, BaLFour relinquished this view, a com-
plete floor being established, he states (No. 11, p. 43), by the growth inward of lower
layer cells along with cells formed in the periblast. The cells which OELLAcHER
describes on the floor of the ‘‘ Keimhéhle,” he says fall from the roof of the cavity, sink
into the yolk, and multiply (Zeitsch. f: w. Zool., xxiii. pp. 12, 18). The real nature of the
blastodermic vesicle of LEREBOULLET is by no means clear, for though BAaMBEKE regards
LEREBOULLET’S cavity as no other than his own, yet it must be remembered that
LEREBOULLET’S mucous layer is not necessarily a blastodermic layer in the strict sense ;
and Van BamsBeke himself admits this possibility when he points out the likeness
of this layer with his intermediary layer (No. 20a, p. 4), a point E. van BenepEN
also insists upon. That LeREBOULLET himself regarded his ‘ feuillet muqueux” or
“ véoétatif” as extra embryonic, is clear from his denying that it is formed of blastomeres
—‘ in fishes and Crustacea (the crayfish) the mucous layer,” he says, “is not of the same
origin as the serous layer” (No. 95, p. 14), the one being the true or animal blastoderm,
and the other the nutritive blastoderm.* It is not necessary here to decide the real
nature of the mucous layer, whether it be truly hypoblastic, or hypoblast and mesoblast,
or neither ; it is sufficient to note that the floor of the cavity, according to LEREBOULLET,
has a different origin from the roof, and is not composed of cleavage-products, so that his
cavity would not seem to be a segmentation cavity at all, and though he considered
himself justified in stating that the blastoderm is “creuse et forme unevéritable vésicule
.... dont les parois sont plus ou moins rapproches l'une de l'autre” (No. 93, p. 487),
yet it must not be regarded as the segmentation-chamber of a blastosphere, but the
germinal-cavity underlying a morula. If OrLuacuer be right, that only cells resulting
from cleavage form the blastoderm, then a cavity, if not floored by such cells, is not
a segmentation-chamber according to the accepted view regarding that cavity. The
nature of the floor of any cavity appearing in an early blastoderm is all important, while the
nature of the roof is not so, being, indeed, subject to variation in very closely allied forms
like Rana and Triton, one layer of cells forming the roof in the latter (No. 147, p. 453),
whereas in Rana the roof is two or more cells thick. The lamprey has a multicelled
roof, which thins out to a single layer, as Surpiey has found, in agreement with
CALBERLA, and as opposed to M. Scuurrze; whereas in Elasmobranchs, as also in
Ganoids (Acipenser), the ectodermic roof is thickened by endodermie cells which creep up
the walls of the cavity and pass along the roof. The roof of the germinal cavity in Teleos-
teans is formed by the whole of that portion of the blastoderm which is raised to form it
(Pl. IL. fig. 15), bdm). It therefore includes epiblast (or ectoderm) and lower layer or
* That LeREBOULLET's upper layer cannot be the epiblast, and his second layer the entoderm or “lower layer cells,”
is shown by the fact that he speaks of the lower as a single layer (No. 93, p. 492), and the upper as of many regular
layers of smaller cells, so that our interpretation holds best.
712 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
endodermic cells. When at its maximum it is a slightly flattened dome-like cavity
(Pl. II. fig. 155, ge); but with the extension of the blastoderm its roof is depressed,
and it thus appears subsequently as a mere fissure. Now LrREBOULLET figures his
cavity as a narrow fissure extending almost from margin to margin of the blastoderm ;
whereas BAMBEKE’S is a compact, but loftier and more spacious chamber.* It is
noteworthy that BamBeKE was struck by this dissimilarity, and after examining the
segmentation-cavity in the roach was prompted to seek for a germinal cavity underneath
the blastoderm, and found one, as he indicates in his figs. 4 and 6 (vide No. 20a);
but he adds that “a comparative examination of preparations forces me to regard it as a
simple accident and artificial, for the prominences and depressions of roof and floor
coincide.” There is much reason to suppose, therefore, from the shape and nature of
the floor, that LEREBOULLET’s cavity is not a segmentation-cavity, such as BAMBEKE
supposes, and, if this be so, then LeresoutLer likewise discovered this flattened
germinal cavity, as E. van BrNEpEN says (No. 25, p. 47), though this author is wrong
in according the discovery also to VAN BamBexe. If, on the other hand, LerEBouLLEt’s
be really Von Barr’s (and Van Bampexkr’s) cavity, then H. Raruxe first signalised the
germinal cavity in Zoarces ; and he was followed by SrrickEr. It is therefore not correct
to speak of a cavity of LerEBOULLET with Van BeNEDEN but rather of a (sub-blastodermic)
germinal cavity, which is persistent through all embryonic life, as distinct from the (intra-
blastodermic) segmentation-cavity which wholly disappears.t
What then is the significance of the germinal cavity thus distinguished? By the
fact that its floor is formed of yolk, or rather the protoplasmic cortical film (or inter-
mediary layer), and that it is roofed over by endoderm (lower layer) and epiblast-cells, it
is comparable to the ‘ Keimhéhle” in the fowl’s ovum.{ At a later stage the hypoblast-
cells which intrude from the periphery to form the blastodermie rim (bv) and shield
(Pl. IL. figs. 15, a-e, and 17) do not pass across the floor of the cavity, but creep
up the sides and partially arch it over, forming in fact a gastrula which would open ex-
ternally by the blastopore, were not this aperture plugged up by the mass of yolk (really
Ecker’s plug), which is so large that the invaginated lip is compelled to pass round, and
epibolically envelop it. The germinal cavity, arched over as it is by the thick blastodermie
roof, bdm (Pl. IL. fig. 15, a-e), is never truly open in the sense indicated; but potentially it
is so, the removal of the concentrated trophic matter (y) which does not segment would leave
the blastoderm a simple gastrula—indeed, as RypER remarks in regard to Alosa, that
“the yelk might be removed at any stage without taking away any essential part of the
embryo except the floor of the cavity” (No. 141, p. 569). Van BaMBEKe does not hesitate
to regard his chamber as a gastrula-cavity, and finds in it therefore great phylogenetic
* A glance at LEREBOULLET's figure (No. 93, pl. iii. fig. 3) and BamprKke’s (No. 20a) sufliciently shows this.
t+ See a paper “On the Significance of the Yolk in the Eggs of Osseous Fishes,” by E. E. Prrxce, Ann. Nat. Hist.,
July 1887.
+ It is interesting to observe that, with the appearance of the germinal cavity, the thick periblast-floor in some forms
becomes thinner, The Keimhdhle or germinal cavity is often called the segmentation-cavity in the fowl’s ovum.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES, 713
significance; but OELLACHER, Donrrz, Ryper, and others agree that it is merely an arti-
ficial product, and due to the action of reagents. It is difficult to accept the latter view,
after the careful observations of VAN Bamprxkr, who admits that in the trout and carp
it is absent, as seems to be also the case in a large number of Teleosteans at St Andrews;
yet since a cavity of this nature, remarkable for its deep situation and transient nature,
has been seen in other blastoderms (e.g., Aves and Ganoids), it may justifiably be
regarded as a normal structure, and perhaps due rather to the exigencies of the cleavage-
process than to ancestral causes. If, as Warrman holds (No. 159, p. 296), “the case of
Ascidia (Kowalewsky), of Sycandra (Schultze), of Anodonta and Unio (Flemming), of
Clepsine and Euawes, and numerous cases like the latter, show that the blastoccel arises
by the cells being pushed asunder in the process of cleavage,” then the segmentation-
cavity when it is present can have no profound ancestral meaning, such as Van Bam-
BEKE urges ; but is of interest merely in connection with modifications in the ovum, by
which the area embraced in segmentation is greatly reduced. This reduction impli-
cates a mechanical difficulty, resulting in the formation of a chamber, which is appro-
priately named a segmentation-cavity or blastoccel. Probably every instance of a
blastoccel may be explained in this manner, and it may thus co-exist along with the
germinal cavity. The former, it is generally admitted, becomes obliterated, whereas the
latter persists, and must be regarded as the remnant of the primitive enteron. Its
persistence in the embryo is of importance, for it is an essential point in the gastrula
that “it should directly or indirectly give rise to the archenteron” (No. 10, p. 457).
That in forms so various as Gallus, Rana, Acipenser (No. 82), and Balanoglossus
the segmentation-cavity is transient, and has no relation to the blastopore, is proof
that it cannot be regarded as enteric, for the archenteron has always relation to the
blastopore. In speaking of the cavity in the Teleostean ovum as germinal, we merely
do so to distinguish it from the segmentation-cavity (blastoceel), which is wholly
another structure, though the name does not necessarily imply any ulterior meaning.
Nor is this course discordant with the conclusions of Teleostean embryologists in general;
for OELLACHER distinctly affirms that the germinal cavity produced by the lifting up*of
the germinal mass is the sole cavity observed by him in Salmo fario, and he failed to
find a central segmentation-cavity, as was the case also with Van Bampeke in the ova
of this species, and of Cyprinus; and Kuen, though he speaks of a segmentation-
cavity, formed by the lifting up of the blastoderm, really means the germinal cavity
(No. 79, p. 197, and pl. xvii. figs. 11 and 12), this latter cavity being also recognised
by Rreneck (No. 137, p. 356), Grrr, Henneauy, Owssannikow, and Wem. JANosik
observed a cavity in the germ, and an earlier one between the yolk and the lower layer
cells, and he termed the former “ segmentation-cavity.’* It is not a little curious that
Ryper, while holding that the germinal disc of Teleosteans is equivalent to the entire
Amphibian ovum, yet regards the cavity outside the dise (germinal cavity) in the former
as homologous with the deeply placed chamber (segmentation-cavity) in Rana and the
* Archiv f. Mikr. Anat., vol. xxiv.
VOL. XXXV. PART III. (NO. 19). 5Y
714 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
Elasmobranchs, and somewhat inconsistently maintains that in Teleosts the origin of the
cavity is directly due to cleavage; whereas, on phylogenetic grounds, it must arise in
connection with the peripheral invagination and the formation of the blastopore. If, as
Ryper holds (No. 141, p. 492), the Teleostean germ is equivalent to the whole ovum of
Rana, then we must look for a segmentation-cavity deeply placed in the former blasto-
derm, a fact which BaMBEKE, as we have seen, considers established for Leuciscus.
Ryper, too, adopts a questionable view of the germinal cavity, when he says that it is
“simply a space filled with fluid, which facilitates the gliding of the blastoderm over the
yelk during growth,” and constituting the fissure between the outer (embryonic) layer
and the inner envelope of the yolk, and further as the representative of a “ primal
nutritive space,” a lymph-cavity. He also considers that the body-cavity is continuous
with the segmentation-cavity, and maintains that it does not disappear in Gadus
morrhua, Cybium, Coregonus, and Alosa,
While there are many points, therefore, which support the view that the segmentation-
and germinal cavities are not one, but may indeed co-exist, or may appear successively
in the same ovum, there is a possibility that the difference between the deep-seated cavity,
seen, for example,in Elasmobranchs, and the sub-blastodermic chamber in Teleosts, may, with
extension of our knowledge of the early blastoderm in the latter, disappear, and this would
be so if it could be shown that the germinal cavity arises, not by the lifting up of the
dise, but by intracellular dehiscence, and the disappearance of the lower (separate)
stratum, 7.e., the blastomeric floor.* At present the germinal cavity must be distinguished
as such, the characteristic features being its situation superficial to the yolk, the absence
of blastoderm-cells separating it from the granular yolk-cortex, and its persistence even
into the later embryonic period. Other minor features justify us in emphasising the
distinction of this cavity from the blastoccel or segmentation-cavity proper.
VI. Prertetast or Nuciear ZONE.
From the way in which the protoplasm of the ovum collects at the animal pole, it
is readily seen that the continuity of the disc and the cortical protoplasm beyond does
not cease for some time, and that even when the blastoderm by cleavage has become
defined in the form of a cellular prominence, its connection with the unsegmented
protoplasm external to it is most intimate. The process of superficial transference still
proceeds after cleavage has commenced.t
* The fact that during a considerable interval the segmentation-cavity in Elasmobranchs is greatly deficient in its
cellular floor, and the yolk limits it below (No. 11, p. 518), is interesting, though BaLrour doubts if ever the yolk alone
forms the floor (p. 519). G6rrr’s observations would demonstrate the existence of such a floor of cells in the Tele-
osteans, though it is always incomplete.
+ Granular yolk is also transferred in the Elasmobranch, both OkLLAcHErR and Batrour agreeing that yolk is
assimilated by the germinal area during segmentation. The cessation of the transference and of the yolk cell-gemma-
tion accounts in a great measure, according to BaLrour, for the comparative distinctness of the dise and the yolk at the
end of segmentation.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 715
So long as the yolk-ball can be distinguished even in advanced embryonic stages
(see Pl. VII. figs. 1, 9, &e., ep), it is provided with an envelope of unsegmented proto-
plasm especially noticeable round the margin of the dise (per, PI. II. fig. 12), and forming
in the early stages of cleavage a thickened peripheral belt. This envelope is the “ feuillet
végétatif ou muqueux” of LEREBOULLET (No. 93, p. 771); the “trophic or glandular layer”
of Remak (No. 135, p. 342); the “parablast” of Kier (No. 79, p. 116) and His (No.
67); the ‘‘ Korner-zone” of Kuprrer (No. 88, p. 217, fig. 1); the “lamina mycogastralis”
of Harcxen (No. 62); and the yolk-hypoblast of Ryprr (No. 141); but appropriately
distinguished as the “ periblast”” by many authors.
We may speak of the periblast as early as the stage of first cleavage, the two primary
blastomeres constituting the germ proper as distinct from the protoplasmic layer beyond.*
The distinction, it is true, is more apparent than real, for the protoplasm at the margin
of the disc is in a state of continual transition, passing into the germ probably during the
whole cleavage-process, the disc being indeed only a thickened portion of the proto-
plasmic cortex of the ege,—‘‘a lenticular enlargement of the Rindenschicht,” as
OELLACHER expresses it (No. 113). In thus regarding the periblast as an aggregation of
protoplasm which lies outside the germ proper, because it has reached the animal pole too
late to enter the dise and take part in cleavage, we adopt a theory of its origin which has
been questioned by some observers, notably by Acassiz and Wurrman (No. 2). These
observers suggest that the periblast is really a product of the blastoderm ; that, instead of
being, as we have expressed it, too late to enter the disc, it has already formed part of
that structure, and has been protruded as a germinal outgrowth all round the margin
during segmentation. Van Bamseke, as if by anticipation, expressly opposes such a
view, and says—“ It cannot originate from the dise ; it is coarsely granular, like the cortex
(le manteau protoplasmique);” but he goes on to state that the cortex wholly disappears
when the intermediary layer is formed, whereas the cortex persists very much longer,
though so thin that, as he says, “it is difficult to detect” (No. 20a).
It is not easy to controvert a view which denies the independent origin of the
periblast, for its apparent extension outwards from the margin of the disc and the
continuity of both would seem to favour it. But, if it be correct, then at one stage all
the superficial protoplasm of the ovum must be collected into the germ-mass; and no
such complete segregation has been observed—a stratum of cortical protoplasm continuous
with the germ is always discernible up to the stage when the periblast can be distinctly
recognised asa nucleated layer. Its extension beneath the disc is implied in the view here
adopted, for the superficial protoplasm collects beneath the disc as elsewhere, and this
can be observed by the behaviour of the oleaginous sphere in such an ovum as that of f.
gurnardus, inasmuch as it passes along beneath the floor of the germinal cavity evidently
prevented by the layer of continuous protoplasm from entering the chamber. Van
BAMBEKE, it is true, questions this latter point, saying that at one time no trace of a
* Krnester and Conn, in mentioning that complete furrows in segmentation pass downward to the vitelline
globe, except the intermediary layer and peripheral cushion of Van BAMBEKE. We agree with this view.
716 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
central lamella can be seen, and that it is ‘most probably formed by extension under
the disc from the bevelled ring outside.” Like AGassiz and WuirmMan, LEREBOULLET
holds that this layer is formed later than the disc, observing that, “ at the close of seg-
mentation, no trace of the mucous layer is seen, though dispersed vitelline globules are
visible out of which this layer is formed” (No. 93, p. 495).
Three theories of the origin of the periblast are thus held—(1) that it is simply a
separation, a superficial segregation of protoplasm interfused in the yolk, and reaching
the animal pole too late to enter the disc; (2) that it does form part of the disc, but
afterwards issues from it all round the margin, extending as an extra-germinal layer; (3)
that it is not a mechanical transference, but an actual transformation of yolk-particles.
The second and third views, just stated, involve processes less simple than the first, and
if a process of simple transference, the segregation of interfused germinal matter, suftice,
it is needless to resort to any explanation more complex. The superficial segregation of
protoplasm implies that a sub-blastodermic stratum is never wanting, and that, from the
first, the blastomeres “‘do not rest” (in E. van BeNnepEN’s words) “immediately on the
vitellus ; they are separated from it by a layer of substance which is finely granular”
(No. 25, pp. 44, 45).
For some time the periblast remains homogeneous, devoid of nuclei, and not separable
from the yolk-cortex beyond, save by its slightly greater thickness (per, Pl. I. fig. 14),
and by the occurrence of scattered granules in it, which are distinctly seen at the end of
the first day in G. morrhua. Further, the occasional presence of protoplasmic filaments
over the area of the periblast seems to indicate its tenacious character (PI. II. fig. 7).
It forms in some ova, as LEREBOULLET and E. vAN BENEDEN noted, a considerable
thickening below the centre of the germ. ‘This thickened central lamella disappears
later, and it is doubtful whether in many species it is ever present. The peripheral
thickening is usually well marked * as a prism-shaped ring (per, Pl. II. figs. 1-3), which
is triangular in cross-section, the dise resting upon one side, the lowest side being in
contact with the yolk, while the third is external and free. When segmentation is
far advanced and the biconvex form has been assumed, large nuclei begin to appear in
close proximity to the margin of the germ (Pl. [X. fig. 10, v). Though irregularly disposed,
two or three rows may be distinguished (PI. IX. figs. 9 and 10, n; and PI. IL. fig. 4a),
and they rapidly extend outwards over a variable area, which is known as the nuclear
zone. The nuclei are large clear vesicles, having a slightly pinkish hue in certain lights
(transmitted), well-defined and rounded in form, often slightly elliptical, and showing
in some cases granules or nucleoli (Pl. Il. figs. 6, 8, »; and Pl. IX. fig. 9). At first
they are crowded together, but as they extend towards the equator they show a
tendency to a regularity of disposition which is very remarkable when they are five
or six deep. Kuprrer describes these bodies in certain species of Gastrosteus as
larger than the nuclei of the germ, separated by regular intervals three times the
diameter of each nucleus, and arranged in rows duly alternating, the row nearest to the
* LEREBOULLET descants upon its unusual thickness in the trout (No. 95, p. 14).
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 717
dise being the first to appear, the rest following in succession (No. 88, p. 217). At the
12th hour, in the gurnard, the nuclear zone forms a conspicuous spotted belt round the
disc, and the yolk in certain views seems to be distinctly pitted by them (PI. II. fig. 5).
A little later they are less distinct. When the blastoderm has extended over one-third
of the yolk-surface, traces of the nuclei are still to be seen (PI. XIV. fig. 7, np). Thus,
at the 25th hour, in the gurnard the blastoderm is surrounded by a continuous belt
of protoplasm, beyond which few or no granules exist. Those previously seen have been
overlapped by it, but are visible underneath towards the rim. In the surrounding
protoplasm no large nuclei appear, and only a few of the granules of the previous stage.
Often, during the early period of the nuclear zone, the nuclei appear in groups as if
multiplying by division, this being well marked in the ova of Gadus morrhua; but on
the second day the nuclei are invisible, and only a granular ring surrounds the disc.
How do these nuclei arise? Three possible geneses are suggested,—they may be
derived from the nuclei of the blastoderm, as ScHuLrze, OELLACHER, WHITMAN, and
WeNcKEBACH (No. 158)* hold ; or they originate directly or indirectly from a primary yolk-
nucleus (Horrman, E. van BreNnepen); or lastly, they may be endogenously formed as
independent segregations of active protoplasmic particles (Kuprrer), either from the
marginal cells, or from the cells which fall from the lower surface of the “ segmenta-
tion-cavity,” or rather germinal cavity, and which fuse with the periblast. WENCKEBACH
asserts that no nuclei or cells arise either in the periblast or in the yolk, and that the
nuclei of the periblast, after their separation from the blastoderm, degenerate and take no
part in the formation of the embryo.t The appearance of the extra-embryonic nuclei later
than the nuclei of the germ—further, their first manifestation close to the margin, and
their increase centrifugally from the blastoderm, point, it cannot be denied, to a blasto-
dermic origin. Their derivation from an original single yolk-nucleus has not been
demonstrated by any observations, nor does it appear to be supported by the manner in
which the nuclei become visible, though it accords best with the theory that the multi-
nucleate condition is less primitive than, and derived from, the uninucleate. This con-
tention Burscuit has devised, and he adduces the case of certain Infusorians in which not
only is the multinucleate condition prior, but actually gives rise to the uninucleate con-
dition—many nuclei coalescing before nuclear cleavage takes place (No. 36, pp. 212-13).
It must be observed, on the other hand, that ENGLEMANN (No. 54, pp. 576-7) and ZELLER
(No. 161, p. 360) have shown that in Opalina the multinucleate is unmistakably derived
from a primary uninucleate condition. The existence of a primary yolk-nucleus in
Teleosteans still remains to be demonstrated. If, by segmentation of this nucleus, the
periblast-nuclei are produced, appearances in the living ovum afford little evidence of
it; but if the nucleus dissipates, and later, becomes aggregated again at numerous
superficial centres, then this view is not without support.
Kurrrer, Kier, and other authors regard the nuclei we are considering as free
* Ryper recently adheres to this view (U. S. Com. Report for 1885 (1887), p. 490).
+ No. 158, and Jour. Roy. Micr. Soc., Feb. 1887, p. 43.
718 PROFESSOR W. C. MSINTOSH AND MR E. E. PRINCE ON
nuclei, originating as independent segregations of active protoplasm, like the nuclei which
arise endogenously in the Molluscan ovum, as Professor Ray LANKESTER was the first to
recognise. In Crustacean ova such nuclei have long been known, though in Onzseus
it is noteworthy that Bosrerzsky affirms their blastodermic origin and subsequent
migration ; but this view is not generally accepted. WEISSMAN, too, imagined that in
the ova of Dipterous insects such structures arise de novo, and without genetic relation
to nuclei already existing ; but later researches lend little countenance to this opinion,
and WerssMAN has abandoned his contention. KowaLewsky has described in the yolk-
matrix of the Annelidan ovum scattered nuclei, endogenously formed and afterwards
collecting superficially, especially beneath the blastoderm ; they are at first few in num-
ber, but show rapid increase, and are especially abundant about the time of exclusion.
He regards the nuclei of the “intermediary layer” in the Teleosteans as originating from
those of the entoblastice (yolk-) cells. The appearance of free nuclei in the region outside
the embryonic area in the chick, as described by RauBer (No. 133, p. 570), is a further
instance of such extra-embryonic nuclear bodies, and the nuclei in the Teleostean
periblast may have a like origin.* The fact that they differ in shape from the
spherical nuclei of the dise—being generally more or less elliptical, and often of
larger size (PI. II. fig. 6, )—points to a non-blastodermic origin. Kuprrer speaks of
their differentiation, and of delicate contours which appear round them resembling hexa-
gonal figures, in Clupea (No. 87, p. 205). Lrresounzer observes that they are large and
granular in Hsow, and along with the matrix in which they lie, they “come from an-
other source” than the protoplasm and nuclei of the disc (No. 93, p. 494). Ba Four, again,
comes to the conclusion, while leaving their origin an open question, that there is no
evidence of their derivation from pre-existing nuclei in the blastoderm (No. 10, p. 109).
In the living Teleostean ovum it is difficult to watch the actual formation of these
nuclei ; but Kuprrer describes with some detail the appearance in Clupea of clear spots
of protoplasm which grow from a speck-like particle to a body 5-6 m in diameter (op.
cit., p. 201), and E. van Brnepent is no less decided in affirming that these nuclei
arise ‘‘par voie endogene” simultaneously in the periblast. We have noted that in
the egg of the cod, towards the end of the first day, the periblast shows only minute
granules scattered through its translucent protoplasm. The nuclei{ are few at first,
and close to the edge of the disc, as if some of them had escaped by “hernia.” At other
parts of the periblast clear vesicles and minute granules occur. Observations do not
strongly support the view that the nuclei of the periblast migrate from the archiblast,
but probably they arise in the periblast itself, and it may be that the activity in the dise
proper stimulates similar activity in the periblast, just as a limited area of irritation in
* Ryper regards the “ nuclear zone” as homologous with this germinal wall in the chick, and it is certainly note-
worthy that the nuclei in the latter (the “ white yolk nuclei”) are most abundant below the thickened periphery of the
blastoderm, and become the nuclei of cells which enter the germ. + Belg. Acad. Sc., No. 6, June 1876, p. 1202.
~ Kiyastery and Conn (op. cit., p. 199) observed in the cunner the formation of cells round these nuclei on the
surface of the yolk; but it seems, aceording to Mr G. Brook, that Mr Kinastry has since altered this view (Trans, Roy.
Soc. Edin., 1887, p. 224).
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 719
ordinary vertebrate tissues has a tendency to stir up a like condition in surrounding parts.
So early as the 82-cell stage in 7. gurnardus, numerous nuclei, precisely like those after-
wards present in the periblast, were observed, irregularly scattered beneath the blastoderm.
Some of these nuclei, which were in close proximity to each other, coalesced and formed
large irregular structures.
On one occasion careful focussing brought out beneath the cells of the blastoderm (in
an ovum of the species just referred to, of which the yolk was about half enveloped) the
faint outlines of periblastic nuclei, while, in an oblique view of the invaginated rim its
under surface was somewhat regularly nodulated by the nuclear projections which thus
protrude into it from below (PI. II. fig. 5).
The blastoderm of Gastrosteus spinachia at a certain stage shows, scattered through-
out its extent (Pl. II. fig. 9, x), large bright nuclei, often showing many nucleoli. These
nuclei, as suggested elsewhere (No. 124, p. 493), are probably periblastic, and they
persist for some time after the closure of the blastopore.
After their appearance close to the margin of the disc, they extend outwards, while
at the same time they also pass inwards, and form a nucleated stratum beneath the
blastoderm. They progress centripetally, and eventually stud the periblast-floor of the
germinal cavity, and are visible through the roof formed by the translucent blastoderm ;
but whether they increase by cleavage or spontaneous endogeny is not clear. Barour
states that they increase by division (No. 10, p. 109), and nuclei frequently show a
transverse line coinciding with the short diameter (Pl. LX. fig. 10), but the further
constriction and “ direct” division of an example of such nuclei into two daughter-nuclei
was not made out,* and it is probably true that they arise and multiply precisely like the
nuclei named ‘“‘autoplasts” by Professor LankesTER in the ovum of Cephalopods—arising
and multiplying not by cleavage, but originating de novo as independent segregations.t
The behaviour of the nuclei outside the dise in Teleostei is similar to that in Elasmo-
branchs, as Baurour clearly states that whatever influence the nucleus may have in
ordinary cases of cell-division, it may yet undergo precisely similar changes without
exerting any influence on the surrounding protoplasm. In Elasmobranchs the nuclei of
the disc are rounded and regular in form, while those in the yolk are irregular in shape,
and provided with knob-like processes. The cone-like nuclei are only found in the earlier
stages, and they possess no distinct membrane.
OxELLACHER, who refers more especially to the nuclear zone as described by Kuprrer,
says there isno need to resort to free-cell formation, inasmuch as its protoplasm is the
same as the rest of the archiblast, hence, in each, the segmentation-process is the same.
BaMBEKE ingeniously suggests that an endogenously-formed yolk-nucleus may give
origin to these nuclei, and that the cells of which they are the centres are segmented
more slowly than the cells of the disc (No. 20a, p. 4); but, as previously noted,
* The failure to observe “direct” division will not, of course, appear strange to those who accept karyokinesis or
indirect division as the sole process of nuclear multiplication, but all visible forms of division are here included.
+ LAaNKESTER is also of opinion that the cells of the perimorula in Gammarus locusta arise as isolated structures
like the autoplasts of Cephalopods (No. 92, p. 63).
720 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
neither a primary nor a later endogenously-formed yolk-nucleus has been made out in
the vitellus of the Teleostei. Upon this vexed question centres the interpretation of
the trophic part of the ovum.
That the periblast-nuclei are really autoplastic, would seem to be the conclusion most
agreeable to the facts of the case,* and if the yolk were ancestrally divided into separate
nucleated masses or cells, as was most probably the case, then upon the breaking down of
these yolk-segments, to form the existing syncytium of the Teleostean ovum, the nuclear
matter would likewise become diffuse. It is possible, therefore, to look upon the peri-
blastic nuclei as the revival (segregation) of the primary nuclear bodies. The vitellus in
one species (Zemnodon saltator), described by AGassiz and Warrman (No. 2, p. 14),
still shows the division into large yolk-segments without nuclei, though the segmenta-
tion is not total, a large central mass remaining uncleft. These large segments are
much flattened, and appear beneath the marginal periblast, with which, during epiboly,
they progress round the central yolk-nodule towards the vegetal pole. A similar con-
dition occurs in the pelagic egg of the sole (Pl. XXII. fig. 1), in which a series of vesicles
or segments appear under the dise in the lenticular stage, and spread with the blastoderm
so as to form a superficial layer over the entire yolk. In the extremely pellucid egg of
the sprat, again, the whole yolk is imperfectly divided into a series of polyhedral masses.
Even holding to the position that the cell is essentially of a uninuclear character, no
difficulty is presented by the multinucleate periblast, for each may be regarded as the
centre of a cell whose outline is undefined. It must be granted also that little difficulty
is presented to those who regard the yolk as a single cell—if, as BurscH11 holds, a single
cell during proliferation may exhibit all the gradations from a uninuclear to a multinuclear
condition, and from the latter retrogress to the former condition without once forfeiting
its character as a single cell. On the other hand, the syncytium, as HaxcKEL conceives
it, though formed of cells originally separate, and including therefore many nuclei, is
still a cell.
There are many appearances in the living ovum which indicate that the periblast
contributes cells to the blastoderm, such cells being segmented extra-embryonically.t
This point belongs to a later stage of development, and we can here merely make a
reference to this segmentation of the periblast in its bearing upon the real significance of
this layer.
In an ovum of Gadus aglefinus, at the close of the first day after fertilisation, the
nuclear zone was well marked, and the homogeneous protoplasm composing it rose into
minute prominences or depressed conical papillae, upon each of which a nucleus appeared
to be seated (PI. II. figs. 4 and 4a, x). This botryoidal appearance was unmistakable,
* It would not be accurate to speak of these nuclei as genuine “ autoplasts,” for these latter bodies never become
the centres of cells produced by cleavage. It is essential to the autoplast that the surrounding matrix remains unseg-
mented,
+ The growth of the blastoderm by marginal conversion of cells is a phenomenon that continued investigation shows
to be widespread ; it occurs in many Invertebrates—in Cyclostomes, and,as BALFour and Dr1GHTON unmistakably demon-
strated, in Birds. Vide “Renewed Study of the Germinal Layers of the Chick” (Quart. Jour. Micr. Sci., xxii. p. 177).
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 721
and due, there can be no doubt, to planes of cleavage passing as linear depressions from the
margin of the dise outwards. No cells could actually be seen to be completely segmented
and added to the margin of the disc, nor could this be ascertained by study of the living
ovum, for such cells transferred into the germ would enter the lowest stratum of the disc,
and would therefore pass beneath the margin along the basal region—this margino-basal
portion of the blastoderm being especially unfavourable for study in the living condition.
There is no evidence against Broox’s view, that matter passes into the archiblast in the
early stages, and thus nourishes it—a view similar to that of Horrman (No. 68), viz.,
that the nucleated periblast performs the function of provisional blood.
VII. Empryonic SHIELD anD Rim.
We have traced the development of the ovum up to the stage which immediately
precedes the formation of a distinct embryonic trunk, coincident with the radial
thickening of the blastoderm. No clear differentiation into layers can as yet be
made out, though the upper stratum is usually distinguished as a layer of ectoderm
(OetLacHER’s “hornblatt”) or epiblast (Pl. Il. figs. 1-3, 6, and 15, ep)—the cells
below, which form the main mass of the germ, being endodermal or lower layer
cells (//). ‘This saucer-shaped blastoderm (PI. II. fig. 19), consisting of two germinal
leaves or layers, arches over the germinal cavity, while peripherally it is in contact
with the cortical protoplasm of the yolk, chiefly that part of the cortex distinguished
as periblast. Then commences epiboly, that remarkable process which RaTHKe, in
1832 (No. 129), was the first to describe in Teleosteans. The germinal matter which
originally clothed the vitelline globe as a film, and afterwards becomes segregated
at the animal pole, is now seen apparently retrogressing, and again encloses the yolk,
not as a homogeneous envelope, however, but as a segmented cellular blastoderm.
With the commencement of the process the blastoderm flattens (PI. II. fig. 15, bdm),
and the vertical height of the germinal cavity (gc) is by this depression so much
reduced as to form a mere fissure, though otherwise its relations remain unaltered. On
the second or third day, in the Gadoids and other forms here referred to, this flatten-
ing is clearly shown; and LereBouLer, who describes it in Hsox, says that during the
first half of the second day the blastodermic vesicle (7.e., the germ) flattens more and
more, its two opposing walls touch,* and it becomes moulded as a serous envelope round
that part of the egg which it covers like a watch-glass (No. 93, p. 488). By this process
of flattening and extension meridionally over the yolk-ball, the germ becomes distinctly
thinner. This decrease in thickness is especially noticeable, LEREBOULLET says, in Salmo
fario as compared with Perca, and epibolic extension in the trout is much less rapid
than in the latter. Variations, too, occur in pelagic ova, but these are doubtless caused
* If our interpretation of LEREBOULLET be correct, it is not accurate to speak of the two layers, viz., the thin germ
and the periblast, as really touching, though the interspace becomes less and less.
VOL, XXXV. PART III. (NO. 19). 5 Zz
722 PROFESSOR W. C. M‘IINTOSH AND MR E. E. PRINCE ON
in a large measure by differences of temperature, light, the condition of the water, and
other features of the laboratory, though the divergence between a pelagic and a demersal
ovum in this respect is so marked as not to be fully explained in that way. Thus in
Gastrosteus a blastoderm, which covered fully one-eighth of the yolk, had embraced in
twenty-four hours only slightly over a quadrant, while in Plewronectes it had extended
over nine-tenths of the yolk-surface. Again, in Gadus aeglefinus, when the temperature of
the tanks was kept lower, epiboly was as slow as in the case of Gastrosteus under a higher
temperature. When the germ covers barely a quadrant the margin becomes visibly
thickened, this being the first indication of the embryonic rim (Kuprrer’s Keimsaum,
OxLLacHER’s Keimwulst), which plays so important a part in the formation of the
embryo (Pl. IL. fig. 17, br). This appearance of the rim LEREBOULLET connects with
the thinning out of the germ, and explains it as a process of mechanical transference—
the central cells passing to the circumference, as indicated by the increased density
of the latter, which forms “a true pad around the egg” (No. 93, p. 458). The cells
of the germ undoubtedly become greatly flattened, as we see in Pl. II. fig. 3, as com-
pared with fig. 17, when extension has proceeded largely ; but such a transmission of
cells less truly represents the process of peripheral thickening than the inflection of
old, the reception of new cells described below, and the aggregation of these in a
marginal band,
We have referred to epiboly as to all appearance a retrogression,* but it is not really
so, it is rather a process of invagination such as we find so widespread in the develop-
ment of animal germs. ‘This process, had the amount of food-yolk present allowed,
would have resulted in the establishment of an involuted epithelial lining to the gastrula.
The exaggeration of the trophic mass, which must ancestrally have been even much
greater, prevents this progress of the ectoderm, and as its extension is not arrested, it
follows that the yolk-globe is epibolically enveloped. While, as indicated, the germ
becomes thinner, yet along one radius this decrease is not so great as elsewhere ;
in other words, the germ, soon after the close of segmentation, shows a thickened
embryonic radius which never disappears (Pl. Il. figs. 15 and 17). When the
germinal cavity (gc) is formed, this portion is well marked, as the cavity lies in front
of it, 7e., eecentrically, and all through development it is thus distinguished by its
greater thickness, so that LerEBOULLET cannot be correct in saying that the embryonic
radius only commences when epiboly is nearly complete (No. 93, pp. 495-6). He failed,
indeed, to notice in his species any trace of the rim until the blastopore is in its final
stage, then, he says, a very distinct rim is formed around the “trou vitellaire” of Voer,
In the trout, as OELLACHER shows (see No. 114, Taf. i. figs. 2-5), this radius is well marked ;
but in other forms it is less apparent at an early stage, though the (embryonic) radius
in all Teleostean ova is probably distinguishable from the non-radial portion by its
greater thickness. In sections through the blastoderm before the equator is reached
(Pl. I. fig. 17, and Pl. IV. fig. 8), the germ consists merely of two layers—ectoderm (ep)
* Vide E. E. Prince, Annals Nat. Hist., July 1887.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 723
and entoderm (Hy), the cells of both being very much flattened; but along the embryonic
axis several layers are present, and the cells are, in the living germ, more rounded and
fuller than elsewhere. Similar larger cells also occur at the margin (Pl. IV. figs. 5/,
and 7), and to the presence of these, as well as their closer arrangement, no less than the
greater number of cells, is due the thickened appearance of the marginal belt or rim (br).
It is clear that the blastoderm covers a very large superficial area, when compared with
its extent at the close of segmentation, and this extension is largely, as we have hinted,
a process of “ flattening out” undergone by the originally rounded or polygonal cells of
the archiblast. The cells are thus expanded superficially; but doubtless there is also a
marginal addition of cells—periblastic in origin.
Beneath the rim and embryonic axis a single layer of cells intervenes, separating the
germ from the yolk. This layer is, in fact, the third primary layer or hypoblast
(Darmdrusenblatt), and its mode of origin is a point of great interest. How does it
arise? The answer to this question is by no means easy, but the view that it is
invaginated, z.e., an inflection of the epidermal layer, is grounded upon appearances in
the living ovum, and prepared sections (PI. Il. figs. 15, 17, hy) no less than upon
phylogenetic considerations. A folding-in of the epiblast is indeed seen at a very early
stage, but, when the germ has thinned out, this involution is more apparent (PI. II.
figs. 10, 17), and the centripetal advance of the rim can be readily followed by continuous
watching, for, starting as a narrow peripheral band very slightly denser than the rest of
the blastoderm, it advances slowly towards the central point of the animal pole.
This region, known as the embryonic scutum (OELLAcHER’s Embryonalschild), coincides
with the embryonic radial thickening, which, as already noticed, is present from a very
early stage. LEREBOULLET calls it the “ bandelette primitive” or ‘“ germe embryonnaire,”
as being in his view the first indication of the embryo (No. 94, p. 255), but this is not
so, the thickened radius preceding by an interval of many hours the inflection of the
hypoblast, and being already distinguishable, when the germinal cavity appears. At
first the scutum is a mere tubercle in the Salmonoids, as LEREBOULLET says, though
flatter and more tongue-like in Gadoids, which pushes out from the rim and progresses
towards the pole opposite to the blastopore. As it advances and extends laterally, it
brings visibly into prominence the embryonic thickening, which, however, already exists,
and when the blastoderm covers about one-fifth of the vitellus, this hypoblastic layer
spreads out asa scutiform film or membrane beneath the embryo. That this process is one
of true invagination is disputed. Goérrn, Hennecuy, CunnincHaM, KinasLey, Cony, and
others hold that it is so; whereas OxLLACHER regards it merely as a delamination,
a simple differentiation in situ of the deepest layer of the primary entoderm, and this
view RypeEr and others adopt. Kuprrer, Van Bampeke, His, Kuery, and G. Brook
regard the sub-blastodermic protoplasm or periblast as the source of this layer.
LEREBOULLET speaks of it as a vegetation or proliferation (No. 94, p. 253), though he also
seems to resort to a kind of mechanical transference of cells (No. 93, p. 488). We know
that in Elasmobranchs this layer is formed partly by conversion of lower layer cells
724 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
in situ, and partly by invagination ; in Cyclostomes and Amphibians it is in all likelihood
invagination purely, and the prevailing view, that Teleosteans illustrate this latter process
also, is probably true. In a section of an early blastoderm (PI. I. fig. 15, a) the infold-
ing has apparently begun at one point, but the cells of the single stratum—becoming
crowded together—lie over each other so as to produce a multi-layered appearance (hyp).
The layer inflected is, however, the outer or corneous layer, as GOrrE holds, and this
point is of some importance, for many authorities who favour the invagination-theory,
differ as to the layer that undergoes inflection. Thus Hennecuy, Acasstz, WHITMAN,
and others, though holding strongly to invagination, declare that the outer layer is not
concerned in the process—a linear fissure, it is maintained, wholly separating the lower
or sensory epiblast from the outermost layer, the latter indeed ceasing at a certain
distance from the margin. That the outer or corneous layer alone is inflected is the view
of Kiyestry and Conn (No. 78, p. 201) and others. Teleostean blastoderms are
particularly unfavourable for deciding critical points such as this, the cells of the various
layers being almost destitute of those peculiar distinctive features shown in many other
groups, and an element of uncertainty must necessarily be connected with such a point
as this. So far as Hennecuy’s view (No. 64, pp. 402-3) depends upon observations
on the living ovum, it cannot be relied on, for this point must be determined by sections.
If OrLLacnERr’s well-known figures be referred to, we find in very early blastoderms that
not only is the epiblast shown extending quite up to the periphery, but the flattened
cells pass beyond the limits on to the surface of the yolk (No. 114, cf figs. 4, 5, 6,
Taf. i.); but such an extension beyond the margin of the blastoderm does not take place
in the ova dealt with here, though the limits of the germ in section are difficult to
distinguish, save in such a section as Pl. IL. fig. 15, a.
In the living egg a fissure certainly can be distinctly made out, but it apparently
ceases before the margin is reached. Optical considerations, again, would favour this.
Hennecuy, however, also urges that even in sections this point may be wrongly inter-
preted, as chromic acid preparations show the same appearance as that we have just re-
ferred to, and the obliteration of the fissure he attributes to the reagent. The view
has been suggested (No. 122, p. 449), that while the process is one of invagination, it is
more than that, since it embraces also a species of budding, such as LEREBOULLET alludes
to (No. 94, p. 253), cells segmented from the periblast being added to the blastodermic
margin, and folded in along with ectodermal cells. This vegetation of periblastic cells
will probably be most active along the posterior edge of the scutum, but no evidence of
this is indicated until a later stage. The entire rim is thus a region where peculiarly
complex processes are going on, for not only is the outer edge continuously progressing
towards the vegetal pole, but the inner edge is also advancing towards the opposite
pole, and this is rendered possible by the combined inflection of epiblast-cells, and the
inclusion of periblast-elements. It appears that Kinas_ey and Conn, while holding that
the epiblast is really inflected as stated above, also regard the intermediary layer as
adding cells to the invaginated hypoblast (No. 78, p. 209). The inflected cells creep up
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 725
as a single layer, except at the margin where they are heaped together (PI. II. fig. 10),*
are very much flattened towards the animal pole, and merge with the cells from other
parts of the rim. The effect of this union (especially where the cells from the rest
of the rim meet the cells of the seutum as it proceeds towards the same pole, as well
as laterally) is, that the original very definite outline of the shield becomes irregular,
and finally almost wholly disappears. ‘The rim, however, does not vanish with the
appearance of the carina, as Kuprrer and Van BamBekeE hold, nor are the two structures
really so intimately connected as is often supposed. The rim continues even after the
alar expansion of the scutum, for the reason just stated, is no longer visible. ‘The shield,
in fact, exists before invagination of the hypoblast, if by the shield be really meant the
embryonic thickening, and not merely a visible scutiform appearance; but it passes
insensibly away on all sides, save posteriorly. The invagination-cells do not so much
produce the shield or carina as make both optically visible.t
The ectodermal and periblastic cells, which are inflected, result in the establish-
ment of a single layer of flattened cells—a sheet, in fact, of continuous hypoblast,
which, as Haxcxen held (No. 63, p. 91), limits ventrally the embryonic lamella. It
separates the carina from the yolk, save in the caudal region, where sections even more
than the study of the living ovum indicate the special activity which centres there.
It is noteworthy that the rim does not contain any mesoblastic cells, as in Rana, the
Teleostean resembling the Cyclostome (Petromyzon) in this feature. In the region of
the scutum the hypoblast, of course, includes in its fold lower layer cells, but their
significance at this time is indifferent. This view, we think, explains satisfactorily the
origin of the primary rim, the thickening of the blastoderm, the extension of both, the
definition of the embryonic scutum, and its subsequent gradual disappearance. At any
rate, it is difficult to explain these phenomena by any process of delamination such as
that of OrLLacuer, Ryper, and others: differentiation in situ of the lowest stratum of
the primary entoderm would hardly produce the definitely-bounded thickening, and the
centripetal progress of the same. The whole appearance and behaviour of the cells of
the rim in the very transparent blastoderms here considered, strongly suggests invagina*
tion rather than delamination. OeLuacuer’s figures (No. 114, Taf. i. and Taf. ii.), it is
true, as strongly indicate delamination, though figs. 2 and 3, Taf. i. might represent an
inflection of the lowest layer. At a later stage, when OELLACHER recognises a definite
“unteres Keimblatt,” the cells are rounder and larger than the superjacent cells, a
condition quite the reverse of that which obtains in the Gadoids. It would appear as
if the character of the constituent cells of the hypoblast in these groups were not only
thus unlike, but that in its mode of origin very marked differences also existed. Mr
* This centripetal passage of cells, there can be little doubt, is of profound ancestral significance; it can be no less
than “a real survival of the hypoblast cells to grow inwards during the process of involution ” (BaLFour, loc. cit., p. 530).
+ The curious notions of OnLLAcHER (vide No. 113, pp. 21, 40) respecting the various shapes assumed by the scutum
at different stages, do not seem to be borne out by study of Gadoid and other forms; and the opinion formerly expressed
by one of us (No. 123), that the shield shows differences in outline, characteristic of different species, also needs
modification.
726 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
CUNNINGHAM’s suggestion may indeed precisely express the fact, when he hints that
this layer may be produced in Salmonoids by delamination, and in the Gadoids and other
forms by a centripetal process (No. 48).
In either case the final result is the establishment of a continuous layer of flattened
cells, which extends underneath the blastoderm, and forms an alar expansion on each
side of the trunk of the embryo. AGassiz and Wurman speak of it as three or four
cells deep below the embryonic axis; but this is true only for a slightly later stage, after.
proliferation has commenced. A typical section of the Teleostean on the establishment
of the hypoblast, z.e., when the yolk is about half covered, shows (as in Pl. II. fig. 17) a
single-layered corneous epiblast, ep, formed of fusiform or flattened cells, which roofs over
a thick mass of cells for the most part derived from a second layer of epiblast, the
sensory or neurodermal stratum, //, and lastly, the single layer of cells composed of the
invaginated hypoblast, hy. The more or less acuminate snout of the embryo often appears
to dip into the hypoblast in front, or rather the hypoblast (hy) seems to creep up and
overlap the anterior end of the embryonic carina, car. (PI. III. figs. 5 and 6). Posteriorly
the hypoblast does not exhibit the flattened or squamous character, but forms a small
tract of full, conical or cubical cells, hy (Pl. IV. figs. 5b and 6). These cells, which are
quite at the blastoporic termination of the embryo, arch over a horizontal cavity, and
form indeed a superior enteric roof, constituting, as CUNNINGHAM strongly and ably urged,
a plate of dorsal hypoblast, and giving origin, as will be shown, to the notochord.
These two important points fall to be considered shortly.
The germinal area after completion of cleavage may be said to present three successive
phases,—first, it*is composed of archiblast cells (Pl. II. figs. 1 and 2) of fairly uniform
size, polygonal, uninucleate as a rule, and formed of clear protoplasm free from yolk-
spherules ; secondly, an upper stratum becomes slightly flattened, and may be dis-
tinguished as ectoderm, ep (PI. II. fig. 3), while the mass of unaltered cells below forms
the “lower layer” or primitive entoderm, //; thirdly, the ectoderm, though at first a
single layer, subsequently exhibits three or four layers, and the outer stratum is the
epidermal or corneous epiblast (“ Hornblatt,” OrLtacuer, “ Umhiillungshaut,” RercHert,
“ Deckschicht,” GOrrr); while the under stratum, which always consists of more than one
layer of rounded cells, is the sensory epiblast, JJ (Sinnesblatt of OELLACHER), and this
latter layer by rapid proliferation forms the neurochordal carina, constituting the main
mass of the embryonic thickening, which below is limited by the single hypoblastic stratum,
hyp. These three stages are represented in Pl. IL. figs. 2 and 3.
Epiblast.—Little can be added by way of special remark in regard to this layer.
Certainly the late distinct differentiation of the epiblast in Teleosteans forms a point of
contrast to the condition in Elasmobranchs and Amphibians; but RypeEr’s statement
that the epiblast, with the other germ-layers, is only split off when the shield appears
(No. 141, p. 494),* will not apply to the forms mainly treated of here, for the epiblast is
* LEREBOULLET also in his forms (Perca and Esox) made out his epidermoidal layer only when the equator was
reached (No, 93, p. 493).
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. Ti
visible, and is inflected as the peripheral rim when barely one-tenth of the vitellus is
covered, whereas fully a sixth is enveloped before the expansion of the shield is indicated.
When it first appears the outer layer is distinguishable only by the slightly depressed
appearance of its cells. It is a single layer, and is difficult to make out, as it does not
present the regular disposition or columnar character of the ectoderm in other forms.
The second stratum is well marked when the blastoderm extends over a quadrant, and,
as already pointed out, its cells are not at all depressed, but are rounded or polygonal, and
form several layers—indeed, they are distinctly marked off from the corneous layer. The
existence of this layer has been disputed by HarckEt in these words—* I do not consider
the idea of a special nervous layer many embryologists separate from the cuticular
sensory layer to be confirmed ;”* and Kuprrer denies that this layer exists laterally,
for he distinguishes the corneous stratum only, and indeed doubts the presence of a
median sensory layer as such, the outer epiblast appearing to him to merge in the neuro-
chordal mass below, as though it alone gave origin to it (op. cit., p. 248).
Mesoblast.—The origin of the mesoblast is still a point affording matter for discussion,
but the Teleostean blastoderm, it may be readily surmised, does not offer great facility
for deciding the matter.t That it is not a primitive layer, but is derived from one of
the primary layers, 7.e., ectoderm or endoderm, is beyond dispute.
LANKESTER seems to have been the first to suggest that, viewed phylogenetically, the
mesoblast arose as a paired outgrowth of the entoderm, a fact which KowaLewsky had
ascertained to be true for Sagitta (No. 85, p. 827).
In the Mollusca and Annelida we know that the mesoblast usually arises not as a
single sheet, but as two distinct masses, just as in Amphioxus and ‘many Craniates.
Thus Scorr and Osporn found in Zriton that the two bilateral masses were invaginated
as such, and were never confluent in the middle line, the axial epiblast and hypoblast being
only in contact along that line (No. 147, p. 455). Scorr also affirms in Petromyzon that
some mesoblast (dorsal) is invaginated with the cells of the mesenteron, while the cells of
the ventral mesoblast are derived from the superficial cells of the yolk; but Sarpey’s later
investigations have demonstrated that in this form no mesoblast is invaginated, the two
longitudinal bands being differentiated in situ (No. 149, p. 244). Baxrour showed, and he
is confirmed by His, that in Elasmobranchs the two bands arise in the manner just stated
(No. 14, pp. 35-56); but in Lepidosteus BALFourR and PARKER give no account of the origin
of the mesoblast. In certain Teleosteans, Harcket describes a bilateral development
(Jenaische Zeit., Bd. ix.), while Kowatewsky says it originates from an invagination
of the embryonic rim (No. 86). In speaking of the epiblast, it was indicated that our
observations do not show such an inclusion of mesoblast by the reflected layer of the
blastoporic lip ; and unlike the condition in Rana and other forms, the infolded layer, hyp
(Pl. II. fig. 15), is in close apposition to the epiblast, ep, above. In the middle line
* “Gastrea Theorie,” see Quart. Jour. Micr. Sct., vol. xiv., note on p. 32.
+It need hardly be pointed out that in so familiar an ovum as that of Rana, the precise origin of the mesoblast is
really undecided, and it is still to be settled whether the layer is derived from the “intermediary ” mass of small cells, or
from the endoderm by proliferation, as seems more probable.
728 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
of the embryonic thickening, the proliferated epiblast, ne (Pl. II. fig. 1), and the lower
layer cells, of course, lie above the invaginated hypoblast, hyp. These lower layer cells
probably become largely converted into mesoblast, though it is certain that the hypoblast
also buds off some mesoblastic cells). W. Woxrr has recently expressed a view similar to
this, though he denies that the mesoblast (Mittelkeim) arises in any way from the endo-
derm. The cells which build up the mesoblast represent, he holds, the surplus of those
blastomeres which are not used in forming the gastrula (No. 160, pp. 425-448). Accord-
ing to Kurrrer, His, and Kier, the mesoblast results solely from the differentiation of
the deeper germ-layer, while the hypoblast is stated to originate in the periblast (KLEtN’s
“parablast”’). GOrre speaks of it as formed from the invaginated layer, which gives
origin in addition to the hypoblast. The fact would seem to be that much mesoblast is
formed from the lower layer cells, // (Pl. IL. fig. 15), these cells being a continuous
sheet, viz., the primary entoderm of the early two-layered blastoderm, and they become
severed into two longitudinal masses, mes (Pl. II. figs. 2 and 11; also Pl. IV. figs. 5 and
10), by the proliferation of epiblast, ep, which produces the medullary plate, or
neurochord, ve. The sub-ectodermic mass, // (Pl. I. fig. 15), cannot be regarded as
mesoblast until it is severed mesially—the mesoblast, when recognisable as such, is defined
as two lateral plates, just as in Petromyzon (Calberla), Triton (Scott and Osborn),
Elasmobranchs, and other forms. KinGsLey and Conn speak of this continuous sheet, at
an early stage, but their figures are not decisive. Thus their fig. 25, to which they
specially refer, as also figs. 26 and 27, show a massive dorsal plate, which must be the
thickened epiblast, ¢.e., the neurochordal proliferation, and against it the notochord abuts
below. The mesoblast must, in part, constitute the lateral plates, though the authors
themselves do not so interpret their figures. This interpretation appears, im fact,
irresistible, though it is not in agreement with the view stated in the text (No. 78,
p- 200). Ryprer* records a peculiar condition in EHlecate, viz., a precocious metameric
segmentation in the two parts of the rim which diverge from the posterior end of the
trunk. This is very remarkable, for no such feature has been seen in any other form,
while in those referred to in this paper, the posterior portion of the trunk, after the
mesoblastic plates are defined anteriorly, shows no such differentiation, the three layers of
the mid-region merging, in fact, in a mass of indifferent cells at the posterior termination
(vide—prs, PI. IIL. fig. 12, and Pl. IV. figs. 5d and 5e). These two mesoblastic plates, as
seen in section mes (Pl. LI. fig. 11), have above a thin covering of epiblast, ep, and inferiorly
an insinuating layer of hypoblast, /yp, which separates the embryo from the yolk below.
Anteriorly the mesoblast thins away, and in the otocystic region is reduced to a single
layer of somewhat depressed cells, mes, between the hypoblast, hy, and the greatly
enlarged neurochord, mo (Pl. IV. fig. 4). In OxrtiacueEr’s figures of the trout at this
stage, the mesoblast is not so much reduced ; but its larger bulk is probably connected
* Ryper’s view of the origin of the mesoblast is not clear; he apparently favours delamination with OELLACHER
(op. cit., pp. 494-95), and hypoblastic proliferation (on p. 570); while on p. 501 he seems to suggest a sundering of the
“lower layer” mass, such as is insisted upon above.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 729
with the diminished neurochordal mass (vide No. 114, Taf. iii. figs. viii, and ix,) in that
form.
Further forward (Pl. IV. fig. 3) it apparently ceases altogether, the cells beneath the
optic vesicles, op, being hypoblastic, while the denser stratum, ep, above, is neurodermal
(sensory epiblast), unless the small strand of cells filling up the triangular fissure on each
side be a continuation of the mesoblast behind (marked in the fig. mes ?). OELLACHER’S
representation of this region is not unlike our fig. 3, Pl. IV., but here again mesoblastic
cells are shown as somewhat abundant; his mesoblastic “ Kopfplatten” consisting of
three or four layers, which continue laterally as flattened peritoneal plates. This latter
structure is wholly absent in our forms, the marginal ale being simply epiblast and
hypoblast, though the very minute group of cells mentioned (mes? Pl. IV. fig. 3) may
represent OELLACHER’S cephalic mesoblast. Our figures (Pl. IV. figs. 3, 4, 16, and 16a)
support the view that the mesoblast does not yet extend into the head-region, the
cells at x and y being obviously neurodermal. If the foregoing conclusion be correct,
the mesoblast arises for the most part in situ from the lower-layer cells in the trunk-
region proper—that is, excluding the pre-otocystic and caudal portions—by a process not
of delamination purely, but of mechanical separation, the intruding neurochordal cells
from above actually pushing aside the subjacent cells as two longitudinal lateral plates.
It is not easy to see why mesoblastic cells should, as appears to be the case, be absent
so largely from the cephalic region. Their absence would be accounted for if the
mesoblast be really a forward growth from the trunk-region, and most probably also from
the posterior mass of indifferent cells. Such a forward growth has been regarded as the
sole process of mesoblastic growth (KOLirkER, No. 81); and if in its differentiation the
mesoblastic cells are separated at first just in front of the primitive streak, it will be dift-
cult to show that some such process of forward growth is not involved. The cells, in fact,
below the primary ectoderm form a median layer, when the rim is first invaginated below
it, and since BaLrour and Dericuton find in the chick (No. 19, p. 180) that the main
mass of the posterior indifferent cells (primitive streak) is really produced by epiblastie pro-
liferation, it follows that some mesoblast is really indirectly of epiblastic origin. BAMBEKE,
indeed, regards the mesoblast in Teleosteans as the lowest delaminated stratum of the
primary upper layer of the germ (Von Baerr’s animal layer), ze., ectoderm. This upper
layer in his view divides into three, viz., the corneous, neurodermal, and mesodermal
layers (No. 20a, pl. iii. fig. 8, pp. 57-58). Delamination solely will not account for the
fact that in Teleosteans the mesoblast is certainly best developed in the posterior region,*
as would be implied by the theory of forward growth, and we see that it thins away
anteriorly. A comparison of figs. 3, 4, and 5a—5c, PI. IV., sutticiently demonstrates this.
Even at a later stage the same feature appears (see figs. 10 and 11, Pl IV.), as though
the mesoblast in extending anteriorly into the head receives continual additions from
behind. In Petromyzon, Sure.ey, indeed, regards the muscular elements of the mouth
* This is also the condition in Elasmobranchs, the mesoblast being accumulated at the posterior end as prominent
tail-buds (loc. cit., p. 557).
VOL. XXXV. PART III. (NO. 19). 6A
730 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
and gills, besides the eyes and mouth themselves, as developed from wandering mesoblastic
cells as well as unsegmented mesoblast (No. 150, p. 336), and these wandering cells
Wencxesacu has recently affirmed to be active in Teleosteans in building up the heart
and its connected trunks, and other parts of the embryo (No. 158). It cannot be
denied that in fig. 2, Pl. IL and figs. 4, 5a, and 5b, Pl. IV., the mesoblast has more
intimate relation to the hypoblast than to the epiblast, and the condition presented by
these early sections corroborates the view that the mesoblast is of hypoblastic origin, as
Gorre strongly holds (No. 58). That the mesoblast in the Teleostei has in fact a three-
fold origin is consonant with the figures given in various plates,—part being formed
directly by conversion of lower layer cells im situ, while part is proliferated from the
invaginated hypoblast beneath, and lastly to make up for the forward growth of these
cells into the cephalic region, other mesoblastic cells are derived from the indifferent mass
constituting the caudal region. It is singular that this account of the multiplex growth
of the mesoblast should coincide, even down to many details, with the derivation of this
layer in the chick, according to BaLrour and Dreicuton. In their paper (No. 19) part of
the mesoblast is determined to be from the indifferent cells of the primitive streak, prim-
arily epiblastic (Jbid., p. 182); some mesoblastic cells, which are stellate, are differentiated
from the hypoblast (pp. 184-5); while certain others lying below the epiblast in the early
blastoderm (see No. 11, fig. 91,7, p. 150), and really “lower layer” cells, BaLrour con-
siders “have also a share in forming the future mesoblast” (p. 154). KainesLey and
Conn, though they furnish no account of the process, come to a similar conclusion, and
hold that this middle layer is derived partly from hypoblast and partly from lower layer
cells (No. 78, p. 200).
Hyrostast.—The hypoblast, hy, which there can be ‘little doubt is pushed in
from the periphery as an inflected layer of ectodermal, for the most part “ corneous
layer” cells, ep, with some cells derived from the periblast, per, insinuates itself
between the under surface of the germ, //, and the cortex of the yolk, y, forming the
limiting layer on the ventral aspect of the embryo. It separates the neurochord (ne,
Pl. IV. fig. 5a) in the middle line and the lateral cells, mes, destined to form, in part,
the mesoblast, from the yolk, y. It remains for some time as a single layer of flattened
cells, hy, in the anterior and mid portions of the embryo; but at the posterior termina-
tion (Pl. IV. figs. 5d and 6) its character alters, for it is there less definite, merging, in
fact, with the heaped-up periblast, per, like the thickened layer of dubious cells, which in
the chick continue into the “germinal wall” behind (No. 19, p. 179). This tract of
mingled hypoblast and periblast is the site of much developmental activity, and about
the time that the blastopore closes it becomes defined as a bridge of swollen columnar
cells, hy, in the median line, arching over a fissure below, and pressing against the
neurochord, ne, above (figs. 5b and 6, Pl. IV.). We see here the very phenomenon which
Kinestry and Conn * and CunniycHam have suggested, viz., that the invaginated hypo-
blast is really “dorsal hypoblast, roofing over a primitive enteric cavity, whose floor is
* Op. cit., p. 201.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 731
granular protoplasm with many nuclei, and cells apparently forming around them.”
Anteriorly, the hypoblast still preserves its flattened character (hy, Pl. IV. fig. 5a),
while in the otocystic region it seems to merge in the neurochordal cells, ne, unless the
undefined cells in the middle line be a thin stratum of mesoblast, in course of formation,
and destined partially to constitute the nuchal and cephalic mesoblast (PI. IV. fig. 4).
A similar indefinite axial tract occurs in the chick (No. 19, p. 184). Further forward the
hypoblast is once more fairly defined (PI. IV. fig. 2), and at the tip of the snout, as before
mentioned, it may often be distinctly seen to overlap the epiblast as a thin veil (figs. 4-6
and 19, Pl. III.).
The Blastopore.—The blastopore (Dotterloch—trou vitellaire) may be said to exist
from the moment that epiboly begins. It coincides with the margin of the germ, and
forms in fact the border of the saucer-like blastoderm at the conclusion of cleavage.
Later, however, it is more distinctly recognisable as a kind of spacious mouth, from which
the ball of yolk is seen projecting. Small granules often occur plentifully at the margin
of the rim, and are imbedded in the periblastic ring (PI. III. fig. 16). The continued
extension of the germ over the yolk produces certain changes, notably in its diameter,
which are easily observed.
Contrary to OELLACHER’s view, the rim seems to progress at an equal pace at all
points, and it thus imcreases in diameter until the process of enclosure is half accom-
plished; but after the equator is passed, the aperture necessarily diminishes, and finally
presents a fairly circular form. OELLACHER regards the caudal end of the embryo as
a fixed point, so that the parts of the rim further away from this point advance at an
increased rate—progress being, in fact, rapid in proportion to their remoteness (No. 114,
p. 4). This assumption, however, is very questionable, the snout of the embryo being
apparently the fixed point, while increase in length takes place in the caudal region.
No part of the rim can be shown to be stationary, for the embryo lengthens as epiboly
proceeds, and no part presents more signs of active growth and development than the
posterior extremity, as already indicated.
The lip of the invaginated rim, for which the name blastopore is on every ground
justifiable, attains its maximum size when the equator is reached, and after that stage it
continues to diminish until finally it closes. Often it assumes an oval form (bp, Pl. IIT.
figs. 7, 23; and Pl. XXVIII. fig. 5), doubtless due to the plastic nature of the yolk; but
usually an almost perfectly circular outline is preserved. In some cases the blastopore
has the rude outline of a flask, the narrow portion forming a bay, which coincides with
the caudal end of the embryo, and this has suggested the theory of concrescence in these
forms. In most cases no such terminal bay is seen, the embryo in fact projecting more
or less prominently, and breaking the circular outline of the blastopore in a manner
exactly the reverse of that just mentioned. In the later stages of development in
ovo the conerescence theory is not clearly borne out, e.g., by the view of the gurnard
(Pl. XIV. fig. 7), in which the rim forms a backward loop at the tail. This concrescence,
however, may occur without a visible bay or angle directed forward, as indicated by
732 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
J. T. Cunntncuam. Again, it is observed that towards the closure of the blastopore the
“limbs” of the blastoderm seem to go—so far—into the embryo. When this projection is
less marked the caudal end of the embryo may still destroy the regularity of the
circumference, as in Pl, III. fig. 23, recalling the horse-shoe-shaped blastopore of Astacus,
such variations being easily explained by the bulk of the contained deutoplasmic matrix
and the tension of the blastodermic membrane. This pressure outwards, as VAN BAMBEKE
pointed out, and the restraint of the blastoderm, frequently produce a contracted opening,
like the mouth of a balloon (see Van BamBeke’s figure, No. 20a, pl. ii. fig. 9), from
which a plug of yolk protrudes, just as in the Crustacean ovum, mentioned above, an
endodermal protrusion fills up the blastopore. In Teleosteans, as in Astacus, the plug
diminishes as the blastopore closes. In the gurnard, as the blastopore closes, projecting
cells are seen, which often send out protoplasmic processes, those protruding from the
blastoporic lip somewhat resembling the processes which under pressure are pushed out
from the marginal cells of the blastodermic ring at an earlier stage (PI. II. fig. 16). The
time of the closure of the blastopore of course varies, according to circumstances, in
common with the other features of development. Thus in Trigla gurnardus the closure
was observed to be effected on the third day after fertilisation; whereas in another series
earlier in the same season (May), the temperature being lower, this did not occur until
the fifth day. As closure takes place the yolk may often, in side views, be seen still to
project as a diminished yolk-plug (Pl. IIL fig. 15); but usually as closure is effected
the blastopore forms a trumpet-shaped opening, round which the deeply corrugated lip
rises as a circular eminence (PI. III. figs. 9, 10, 21).
Kupfjer’s Vesicle-—When the blastopore closes, or often a few hours earlier,* a minute
vesicle arises on the ventral aspect of the embryo slightly anterior to the caudal termina-
tion. Its advent is preceded by the appearance, in some cases, of vesicles or small
elongated spaces (PI. III. fig. 17), evidently filled with colourless or pinkish fluid. They
occur quite at the margin, as if the advancing embryonic area became elevated at these
points, and progressed over them. In other cases a granular thickening occurs in which
a few rounded vesicles are imbedded, as can be readily seen in Trigla gurnardus and
other forms shortly before the blastopore closes. K1in@stey and Conn noted such a group
of minute vesicles, which in five hours apparently by coalescence showed the characteristic
form and appearance of Kupffer’s vesicle. It is defined in their figure, above by hypo-
blast, and below by periblast (No. 78, pl. xvi. fig. 54). It is variable in the precise time
of its appearance, for Hennecuy noticed it in Salmo fario when only about half of the
vitellus was covered by the blastoderm (No. 80). In Molva vulgaris, Gadus morrhua,
and other species it is usually not visible during the open state of the blastopore, but
both in position and time of its appearance it varies, though the clear vesicular structures,
with a delicate envelope, are usually exhibited. Kuprrer, who first described it in
Crastrosteus, Gobius, and others, calls it the “allantois,” and says that it acquires a coating
of cylindrical epithelium, and finally becomes the bladder, though he did not show how the
* J. T. Cunsrycuam found that in Clupea it was late in appearing (January 1886).
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 733
primary ‘‘ Urnierengange” communicated with it (No. 88). Hrnneauy also speaks of a
cellular wall, but it appears to be more truly a wall of clear protoplasm in which nuclei
rapidly develop, and not wholly a wall of cylindrical cells. In regard to form, it may be
more or less spherical (kv, Pl. XXII. figs. 8, 9), or markedly ellipsoidal (Pl. XXIL. fig. 12),
this latter figure being frequently altered by the flattening of its floor (kv, Pl. ILL. figs.
21, 22) and the increased curvature of the roof,—changes best seen in side views; while
again its shape may be wholly irregular (PI. III. fig. 14); or lastly, it may simply take the
form of a sub-embryonic fissure. Secondary vesicles are very frequent, and they present
the same features as the normal vesicle (Pl. XXIII. fig. 9); but may extend all along the
ventral line almost to the pectoral region. In the gurnard this multiplicity of vesicles
is often a very striking feature, whether extending along the sub-alimentary region, or
accumulated together as a prominent cluster of bubble-like structures. A small anterior
vesicle in addition to the normal one is often seen (PI. III. fig. 20, and Pl. XXIIL. fig. 8),
and a connecting granular strand, but there is no apparent tendency to amalgamate.
The diameter of the larger vesicle in an example of Gadus eglefinus was found to be
‘005 inch, but occasionally, as in Trigla gurnardus (third day), the vesicles which form
a group may even be five or six times larger than the ordinary vesicle. An embryo
of G. eglefinus was observed to exhibit one or two small vesicles near the large
vesicle, and three hours later, the large or normal vesicle and one of the smaller were
almost free from the embryo, being in fact pressed into the surface of the yolk.
Other three vesicles had developed and occupied the region whence the large vesicle was
protruded, and shortly after, on viewing from above, the vesicles were seen to be upon
one side of the trunk, viz., that to which the tail was bent. Still more remarkable was
the situation in some examples of G. morrhua, for just before the blastopore closed,
in addition to the ordinary vesicle, a large clear vesicle also occurred midway along
the trunk, and it deeply indented the yolk. Moreover, a vesicle also appeared at the tip
of certain protoplasmic pseudopodia which were pushed out from beneath the embryonic
trunk. In another example, Kupffer’s vesicle was situated posterior to the caudal termina-
tion upon a process of protoplasm. AGassiz and WHITMAN called attention to appearances
similar to the foregoing (No. 2, p. 73), designating them “ secondary caudal vesicles,”
and observing that they differed little if at all from Kupffer's vesicle. Whatever signifi-
cance be attributed to this latter structure, it is in any case simply a fissure or cavity
beneath the embryo (see section kv, Pl. IV. fig. 5b), and is defined usually by the dorsal
hypoblast, hy, above, and the periblastic matrix, per, below. Its contents are usually
homogeneous and clear, evidently a translucent plasma, though occasionally granules
find their way from the basal portion of the vesicle into its lumen. Such being its
structure, it is not remarkable that it should vary in shape, or often be a compound
instead of a single vesicle. Batrour (No. 11, p. 61), RaAvBER (No. 133), and Bavsrant
(No. 9) favour the view that it is of ancestral value, and represents the invaginated
enteric cavity of Cyclostomes and Amphibians.* Hrnnecuy could not make out any
* See also a discussion on the subject by J. T. Cunnincuam (Quart. Jour, Mier. Sci., January 1885).
734 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
canal connecting it with the exterior, either in transverse or longitudinal sections;
but sections cannot satisfactorily demonstrate this point, the vesicle itself being evanes-
cent, and its walls of delicate protoplasm are so readily affected by reagents, that a
minute fissure is easily reduced or closed, so as to be indistinguishable. Study of
the living condition is therefore most reliable upon this point, and it must be observed
that Hennecuy did make out a canal connecting the vitellus with the dorsal surface of
the embryo ; but he regards it as wholly independent of Kupffer’s vesicle, for this latter
structure, he says, has disappeared some time before. But in so delicate and transitory
a structure as this vesicle, it is important only that its site should be regarded, and there
can be no question that such a posterior canal passing to the yolk beneath the embryo is
in communication with that site, even though the vesicle itself be no longer distinguish-
able. The enteric cavity at this stage is little more than a fissure between the (dorsal)
hypoblast and the yolk-cortex or periblast ; and Henneguy’s canal can be no other than
the post-anal passage trending round from the dorsal groove to the under surface of the
embryo (that is, the surface of the yolk in HennEauy’s view), and connecting the
transitory medullary groove, with the no less transitory primitive enteron known as
Kupffer’s vesicle. Ryprr admits that a neurenteric canal is represented, but not by a
tubular connection ; the solid caudal mass, where hind gut and neurula mingle, must, he
holds, in its axial part, represent the canal. But Ryprr also noticed a fine canal passing
from the vesicle to the blastopore, and says—‘‘1 reserve my decision as to its true
nature” (No, 141, p. 527).
Neurenteric Canal.—As the blastopore closes, a favourable side view of the caudal
region shows a faintly marked fissure (nec, Pl. III. figs. 9, 20, and 22), or rather what
seems to be a tubular connection of the external blastopore and the ventral surface of
the embryo. Unless the chamber « (Pl. IV. fig. 5d), be an artificial product, the
tubular character is demonstrated in the section. This slight cavity curves downward
from the blastopore, and widens out laterally beneath the embryo (PL III. figs. 8 and 8d),
passing for a short distance forward as a mere line marked by fine granules, and dis-
appearing, as Kupffer’s vesicle, or the site of it, is reached. Any actual union of the
two vacuolated spaces is not easily made out, but the merging of the tract just described
and the protoplasmic wall of Kupffer’s vesicle is unquestionable (PI. II]. figs. 20 and 22).
In fig. 9, Pl. ILL, the course of the canal, nec, from the corrugated blastopore, bp, forward
is well seen, but Kupffer’s vesicle is not yet defined ; and the relation of the two is better
seen in figs, 20 and 21, above mentioned, where the vesicle, kv, a minute lozenge-shaped
chamber, is undoubtedly related to the tract, nec, posterior to it. Certainly the passage, nec,
in fig. 22, is most readily, and without doubt correctly, interpreted as a neurenteric canal.
The existence of such a canal in Teleosteans has often been questioned, and, indeed,
Miss JoHNSON amongst others declares that no such structure is known in these fishes,
nor an invagination giving rise to a blastopore (No. 76, p. 666); though KowaLewsky
is stated to have announced in an early volume of the Arch. f/ Mikr. Anat. (vol. vii.
p. 114) such a connection of the alimentary tract with the dorsal groove in Teleostei; and
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 735
Kinestry and Conn refer very briefly to what they style a “neurenteric canal,” of
which they give a figure (No. 78, fig. 30, pl. xv.). RArrar.E also recently alluded to it
in Uranoscopus (op. cit., p. 28). That it has been rarely observed, and never fully
described, is probably due to its evanescent character, and it may in some cases, indeed,
never be developed. Batrour and Detauron (No. 19, p. 185) speak of it as “ that
most variable structure in the chick,” and the same description may be applied to
it in the Teleostean ovum. This canal can hardly be due to the supposed process of
concrescence, as it has not the character so much of a vertical fissure as a depressed cavity
passing obliquely downward and forward between the embryo and the yolk, and is best
seen in transverse or side view. It is, indeed, less of a tubular canal than of a tranverse
fissure between the convex embryonic surface and the concave yolk-surface, and opening
externally by the blastopore. In PI. III. fig. 8, in the living condition its course is
clearly indicated, the shallow dorsal groove continuous with the blastopore indenting
the caudal region, and then merging in the descending tract, nec, which widens out and
becomes lost in the mass of periblastic protoplasm, kv, in which Kupffer’s vesicle
makes its appearance. Sometimes this neurenteric passage connecting the neuro-
chordal groove above and the enteric region below is a distinct interspace (Pl. III. fig.
9, and possibly nec? Pl. IV. fig. 5d). It is often marked by granules (Pl. III. fig.
22), or even a tract of undifferentiated protoplasm, in which two or three clear spheres
are imbedded (PI. III. fig. 20). Fig. 8, Pl. ILI., for instance, showed this last named
condition at 10 a.M., with a connecting tract opening externally between the closing lips
of the blastopore. An hour and a half later, a spindle-shaped plug (PI. IIL. fig. 8a)
sending outward an acuminate process, interrupted the canal, nec, and presented
amceboid movements. The plug then coalesced with the margin of the blastopore, and,
assuming a distinctly granular appearance, formed a bridge across the fissure connected
with the inferior tract (fig. 8c).* Meanwhile, the clear vesicles mentioned above had
enlarged, and finally coalesced to form Kuprrer’s well-known structure. Such a plug
as we have described BaLrour and Dertcuron noted in the chick, and they speak of a
mass of rounded cells pushed up through the neurenteric canal (No. 19, p. 186). The
phenomenon just detailed shows two important points, viz., the connection of the
external blastoporic orifice with the region of Kupffer’s vesicle, if not with the actual
structure itself, and the obliteration of the passage of connection, v.e., the neurenteric
canal, by a plug probably pushed up from below.
The section figured in Pl. IV. fig. 5d, and already referred to, passes through the
precise region we have been dwelling upon, and a few loose cells alone obstruct the
connection of the dorsal and ventral (enteric) groove, ne. The section is interesting as
showing a portion of Kupffer’s vesicle, or the groove itself imbedded in a thick layer of
periblast, per, as we have before described.
Now the sections figured (Pl. IV. figs. 5b-5d, and fig. 6) clearly show the continuity
* Fig. 8b is an intervening stage, when neither plug nor connecting bridge are visible.
736 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
of the enteron formed by an arch of columnar hypoblast, hy, and a floor of nucleated
(periblastic) protoplasm, per, the ill-defined ascending interspace or canal, nec, being
bordered by indifferent cells, and opening by means of the blastopore into the dorsal
groove above. ‘This dorsal groove is more fully treated of on another page, and it can
be no other structure than the primitive involution forming the medullary canal in so
many forms, but in Teleosteans simply appearing as a transient, ancestral reminiscence,
and, except for this, now obliterated. Certainly its connection with the subsequent
permanent neural cavity cannot be demonstrated.
So rapidly does the dorsal groove become effaced that in a large series of sections of
early stages none indicate this structure favourably; but a reference to OELLACHER’S well-
known figures (No. 114) sufficiently shows this, the deep groove in fig. iv. 3, Taf. ii,
being merely indicated in fig. vii. 5, Taf. ii.; while the figs. in Taf. iv., such as fig. iv. 1,
show no trace of it, nor can the permanent cavity be said to be more than foreshadowed.
Owing to the rapid and complete obliteration of the medullary groove, the absence of a
post-anal canal has been generally accepted for Teleosteans, and for this reason BALFourR,
though adding a query to his cautious statement, concluded that no neurenteric passage
was “apparently developed” (No. 10, p. 286). Baxrour and Parker (Phil. Trans., 1885,
ii. p. 865) speak of the neural canal arising in Lepidosteus as a slit-like lumen, and not due,
as supposed by OrLiacHeER for Teleostei, to an actual absorption of cells. ‘ When first
formed, it is a very imperfectly defined cavity, and a few cells may be seen passing right
across from one side of it to the other” (fifth day after impregnation). The connection in
Teleosteans between the primitive enteron, no other than the gastrula-cavity (see page
713), and the primitive dorsal groove cannot be questioned if our interpretation of figs.
9, 21, and 22, Pl. III., be correct, for the continuity of this groove, nec, and the blastopore,
bp, is very apparent. The formation of a neural canal by a dehiscence of neurochordal
cells is a secondary process, and the Teleostei therefore form no exception to the condition
which so widely obtains in other Vertebrata, and which was demonstrated by GAssER in
birds, by Kowatewsky, Ba.rour, His, and others in Elasmobranchs, by OwssANNIKOW in
Cyclostomes, and by Gorre and others in Amphibians.
Medullary Groove-—The permanent neural canal is formed comparatively late in
osseous fishes, whereas in most vertebrates its appearance as a groove on the dorsum is a
very early feature in development. Fora short period, soon after the optic vesicles are
defined, a transient longitudinal indentation passes along the median dorsal line from
the head to the tail, just as LereBouLLer figures (No. 95, pl. ii. fig. 36). It may be
regarded as actually reaching to the lip of the blastopore, though the depression is
so slight, in the extreme posterior region, that it is in some cases indistinguishable.
In Rana at a certain stage the hind part of the neural groove cannot be made out.
Spencer, however (No. 151, p. 97), found that it extends quite to the caudal margin,
but in this latter region it is obliterated—the cavity closes up, and the nervous cord
becomes solid. The hind end of the trunk in the embryonic Teleostean often appears
like a flattened plate, in which the neurochord spreads out like a spatula (PI. III. fig. 16).
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 737
This flattened condition frequently continues for some time after the closure of the
blastopore (Pl. III. figs. 18 and 20). It is merely a shallow groove, barely perceptible
posteriorly, and does not therefore enclose the blastopore, which remains open for a
short time, as a pore with a corrugated margin, but in the cephalic region the groove
forms, as in the gurnard (dg, Pl. UI. fig. 4), quite a deep fissure, showing itself
earliest anteriorly, and extending, as VAN BampBeke describes, in the form of “a
slight depression,” the “sillon primitif” (see his fig. 12, pl ii.), to the tail. In the
forms here considered, the two lateral folds are by no means sharply ridged, and
viewed from above the furrow is difficult to make out; and is thus unlike the condi-
tion in Hsow, which LEREBOULLET says is distinctly marked by two parallel lines
—the groove being deepest in the mid-trunk, and gradually disappearing before and
behind (No. 95, p. 516). In the mid-trunk, he remarks, it likewise remains open
for the longest time (p. 528). This groove is, however, as before suggested, merely
a reminiscence of the ancestral condition, and wholly disappears chiefly by the horizontal
widening out of the embryonic trunk as the blastoderm proceeds to envelop a larger extent
of the vitelline globe.* This is evidently the case posteriorly, but in the head-region
obliteration is achieved less by elevation of the base of the groove than by coalescence of
its walls.
Kurrrer maintains that it is not by any means the homologue of the medullary
groove of higher Vertebrates (No. 87, p. 251); while OkLLacnER regards it as pro-
duced by the formation of the carina, the furrow deepening as the keel presses down-
ward, and it is certainly true that the furrow is produced subsequent to the growth
of the carina, and does not, as he proved, become the medullary canal; but the view
adopted in these pages, that the carina is a neurodermal proliferation and the dorsal
furrow an ancestral reminiscence, agrees best with appearances in life and in sections.
Certainly no confirmation is given to CaLBERLA’s opinion that ectodermal cells are
involuted along the central dorsal line to form the epithelial lining of the neural canal,
as the same authority, supported by W. B. Scorr (No. 145), holds to be true for
Petromyzon.t
As a matter of fact, the dorsal groove in Teleosteans does not appear to become any
organ, but wholly passes away. It is subject to great variation, just as in the chick, for
at times it is apparently entirely wanting, or at most is represented merely by a
shallow depression, which may be discernible in the short posterior part of the indifferent
caudal mass.{ This posterior mass of indifferent cells, to which reference has frequently
been made, forms the termination of the embryo (Pl. III. figs. 18, 20-22), where it
reaches the lip of the blastopore, bp. In it neither neurochord, notochord, nor mesoblastic
* The superficial extent of the Teleostean embryo is a characteristic feature, and the dorsal groove is thus opened
out on account of the large bulk of the yolk upon which the germ lies flattened. Ryper makes a passing reference to
this (No. 141, p. 564).
+ This epidermic involution in Petromyzon has now been disproved by the recent investigations of SairLey
(No. 150, p. 9).
t Compare the observations of Batrour and Dercuton on the chick (No. 19, p. 183).
VOL. XXXV. PART III. (NO. 19). 6B
738 PROFESSOR W. GC. M‘INTOSH AND MR E. E. PRINCE ON
plates can be distinguished, for all these melt into a common aggregation of cells, below
which even the hypoblast, as BaLrour and DricHTon note also in the chick (No. 19,
p. 180), is hardly separable as a defined layer (PI. III. figs. 3 and 12, and Pl. IV. figs. 5b
and 5c). The epiblast (ep, Pl. IV. fig. 5d) laterally is partially differentiated ; but in
the middle line it merges in the cells below, to which, indeed, it gives origin. All these
features point to its identity with the primitive streak of higher forms. The primitive
streak, it is true, according to the accepted interpretation, arose in the process by which
the embryonic trunk, notably in the Sauropsida, was removed from a marginal to a more
central position on the surface of the yolk. This transference drew after the embryo, as
it were, the diverging arms of the blastoporic lip, and their cells form a post-embryonal
mass, which is the primitive streak. In Rana temporaria, as SPENCER found (No. 151,
p. 97), the point where the medullary groove opens into the blastopore becomes solid, the
neurochord losing its canal, and the epiblast, mesoblast, and hypoblast fusing as an indif-
ferent mass just anterior to the blastopore. The Teleostean embryo reaches to the
periphery of the blastodermic area, and any similar aggregation of mdifferent cells is
reduced to its smallest limit, yet such an aggregation exists, as a transient posterior
mass, into which the notochord and other structures, anteriorly placed, pass and disappear.
It is so in the chick, and in both the structure is transient—its importance goes with
the earliest embryonic stages, and it disappears, or rather is used up, partially as we have
seen, in the production of mesoblast, and still more by the extension posteriorly of the
embryonic trunk, and the development of the tail. Its position on the anterior margin
of the blastopore is easily explained, the present anterior margin is really the primitive
posterior margin. If the blastopore extended to the ventral surface of the embryo, an
increase in the amount of food-yolk would cause its true anterior margin to be pushed
away from the ventral surface, and as it was thus carried outwards, the true posterior
margin remaining unmoved, the parts of the blastopore would become reversed, just as a
pendulum, if held horizontally ina north and south direction with the weight north, would
with the first swing become reversed, the fixed attachment would point north, and the
weight (¢.¢., the true north end) would become south, and thus it is that the present
posterior edge of the blastopore is really the former anterior margin. According to
this view, we see that the blastopore, having drifted outwards, no longer coincides with a
ventrally placed anus; and the relations of the primitive mesenteron, post-anal gut
(Kupffer’s vesicle), and neurenteric connection with the dorsal groove are placed in a
clear light by means of the blastopore.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 739
VIII. Generat DEVELOPMENT OF THE TRUNK.
After the closure of the blastopore, the definition of the embryo as a cylindrical
rod, pressing somewhat deeply into the surface of the yolk (Pl. IIL figs. 1-4),
becomes marked. Anteriorly its enlarged cephalic region soon rises boldly above
the surface of the periblast; while the trunk, though prominently standing out
along the dorsum, and indenting the yolk in a pronounced manner ventrally, yet
laterally, by the alar expansion of the scutum on each side, gradually merges in the
general expanse of the blastodermic envelope, as observed in the serial sections
(figs. 3, 4, 5a-5d, Pl. IV.). The true limits of the embryonic trunk are in reality
not defined, the neurochord, ne, and myotomic masses, mes, are distinctly marked, but
more distally, in the snout and tail, as well as the lateral regions, no sharp line of
demarcation divides the young fish from the blastodermie area beyond. The embryonic
Selachian or bird is pinched off more or less sharply at an early stage; but the Teleostean
embryo, instead of becoming folded off as it were from the yolk, continues to lie
extended upon its surface, and gradually draws the vitellus into its large subenteric
enclosure, the abdominal walls, as we shall see ultimately, entirely encompassing the
yolk. In some forms the yolk persists less prominently than in others, the somato-
pleure more rapidly extending ventrally and enveloping it. It never projects, as in
_ Elasmobranchs and Sauropsida, in the form of a dilated sae distinctly separated from
the ventral surface of the body, except at one point, where a narrow vitelline stalk still
connects the two. LerEBouLLer speaks of such a pedicle in Esox (No. 95, p. 612); but
this has not been confirmed, and in no case probably does the splanchnopleure surround
the yolk, and form a narrow pedicel, until the latter has diminished to a very large extent.
Epiblast.—The external epiblast undergoes little change. We have seen that it is
established as a single layer of cells, which very early become flattened and in section
spindle-shaped. They form, in fact, an epidermis or corneous stratum, ep; but are not for
some time marked off with any distinctness from the lower-layer cells of the blastoderm.”
In the region of the head they first show their characteristic features ; but they retain
their primary rounded, polygonal outline at the posterior extremity of the embryo till
much later (Pl. IV. fig. 5c). These last-named cells, as remarked on a prior page, are
not differentiated fully from the cells beneath until the closure of the blastopore. While
over the trunk, and the area of the blastoderm beyond, the corneous epiblast extends as
a single stratum of squamous cells, yet it may often show slight proliferation, and
present more than one layer. In section, through the head of an early flounder
(Pl. IV. fig. 3), this is so, though it is true the protrusion of the optie vesicles may
have cut off a thin superior stratum of neurodermal epiblast. Over the blastoderm
generally a single layer of corneous epiblast seems to be present; the nervous layer, on
the contrary, is many-layered, and in the middle line becomes so dense as to form
* In some Teleosteans this distinction would seem to be well marked, for Kowaewsky speaks of it as dis-
tinguishable soon after cleavage is ended in Carassius, Polyacanthus, and Gobius (op. cit., 1886).
740 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
the thickened carina, ne, which presses upon the yolk (vide Pl. IV. fig 4). Very often
it is so distinctly separated from the epidermal cells above, that a fissure intervenes,
forming at the sides quite a spacious interstice (PI. III. fig. 2), The cells of the neurochord
are full and rounded (ne, Pl. IV. fig. 4), but as downward proliferation proceeds, those
forming its lateral boundary become columnar, and unmistakably mark off the neuro-
chord from the adjacent cells, especially in the fore part of the trunk. In this region the
cells so rapidly proliferate ventrally and laterally, that they come into direct contact with
the limiting hypoblast, hy, below and at the sides, or at most permit a mere trace of
mesoblast to find a place there. Further back (Pl. IV. figs. 5a and 5b) the mesoblastic
plates, mes, lie upon each side, and its ventral ridge alone touches the hypoblast, hy, while
above it is limited only by the flattened stratum of epiblast, ep. Both layers of epiblast
seem to extend over the blastoderm, and form the outer stratum of the yolk-sac, while
below lies the extended hypoblast, which rests directly upon the periblastic cortex of the
yolk. It is below the second epiblastic layer, which here assumes the character of a loose
mucosa, a rete Malpighii—or rather in the lowest stratrum of this mucous layer, that the
pigment occurs as amorphous bodies which extend over the surface of the yolk. In
P. platessa and other forms, in which the epiblast lies immediately upon the periblast,
the hypoblast being apparently absent, the pigment may send processes into the yolk-
cortex ; indeed pigment may develop in the periblast itself as described on a subsequent
page.
Notochord.—In the earliest sections of the trunk, no trace of the notochord is seen,
the neurochord, ne, being limited below by the single layer of hypoblast, hy, and having
the thick mesoblast, mes, upon each side (PI. IV. figs. 5a—5d). About the time that the
lip of the blastopore has reached the equator, a median mass of cells (nc, Pl. III. fig. 11)
intervenes between the keel of the neurochord, nec, and the hypoblastic stratum, hyp.
These (notochordal) cells are rounded, and rapidly show a somewhat concentric
arrangement, quite unlike the depressed cells of the stratified neurochord above
(Pl. Ill. fig. 11; Pl IV. fig. 5b), The notochordal cells, nc, it is true, are not
separated by any definite line of demarcation from the ventral ridge of the neurochord,
ne; but as the cells of the latter are unmistakably squeezed upwards by the pressure
of the notochord below, this could hardly happen were the cells of the notochord a
downward proliferation of neurochordal cells. The ventral ridge of the neurochord is
evidently indented and its cells greatly flattened by these axial cells below. In such a
section of the early notochord as shown in PI. III. fig. 11, the possibility remains that this
axial rod of cells is a remnant of median mesoblast, left when the lateral mesoblastic plates
are sundered as protovertebrae, but the difficulty of such derivation lies in the fact that
the mesoblast never appears to be confluent in this region; on the contrary, when once
the notochord is indicated, it is sharply marked off from the mesoblast on either side.
Thus in the section (Pl. IV. fig. 10), while the notochordal mass, ne, is not clearly
separated from the hypoblast, hy, below, or from the epiblast (neurochord), ne, above, a
very distinct line of division passes between it and the lateral mesoblastic plates, mes,
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 741
though in another section of the same date (PI. III. fig. 13) the notochord and mesoblast
are not distinctly separated.* In the chick the early notochord is continuous laterally
both with the mesoblast and hypoblast (No. 19, p. 185); while VAN BAMBEKE, in agree-
ment with OELLacHER, decides from his sections that the notochord is directly mesoblastic
(No. 114; also see his fig. 14, pl. iv.). A comparison of a large number of sections shows
that the mesoblast, mes, is very clearly separated as two lateral plates, e.g., as in Pl. IV.
fig. 5a; but the notochord, even when detached from the hypoblast, and apparently in
intimate connection with the epiblast (neurochord), is neyer united to the myotomes.
The hypoblast, hy, it is noteworthy, is hardly distinguishable in this region, as though it
had been almost entirely used up in the formation of the notochord, for at the sides it is
well-defined. Batrour noticed a similar thinning out of the hypoblast, and he states
that only by high powers could the continuity of the stratum be made out (No. 14,
p- 683). Van BamBeEke again denies that the hypoblast exists here at all, affirming that
the notochord is at first in direct contact with the periblast below (No. 20a, fig. 15, pl.
ii.), a layer of cells being afterwards pushed in from each side, and thus separating the
notochord from the cortex of the yolk. The character of the cells, on close examination,
shows the distinguishing features insisted on earlier, viz., the (dorso-ventrally) depressed
condition of the neurochordal cells, ne, and their arched stratified disposition ; whereas
those of the notochord do not exhibit these features, and the contrast is still more
emphatic at a later stage. In addition to their rotund condition, the notochordal cells
are seen in longitudinal section to have a transverse arrangement, such as would be pro-
duced by an antero-posterior pressure (nc, Pl. IV. fig. 15), and this is interesting as indi-
eating, what we have already suggested was possible (see p. 729), viz., that the notochord
may be pushed forward to a certain extent from the primitive streak.
Unlike the condition in Elasmobranchs, the notochord of Teleosteans is at first clearly
differentiated in the mid-trunk or mesenteric region (Pl. XXII. fig. 12, ve), and gradually
extends forward, ending indefinitely above the middle of the cardiac rudiment, as in Molva
vulgaris, on the first or second day (Pl. V. fig. 8). It curves downward, and sometimes
seems to turn slightly to the left, as in 7. gurnardus, on the ninth day. A section through
the otocystic region (PI. IV. fig. 4) shows a mere trace of median hypoblastic proliferation,
while in the post-mesenteric region the activity of the hypoblastic cells has resulted in the
formation, not of a distinct notochord, but of an arch of columnar enteric cells bridging
over a cavity (Pl. IV. fig. 5b), suggesting a condition identical with that represented in
Barour’s figure of this region in Petromyzon (No. 11, fig. 39, p. 86), in an Elasmobranch
(No. 15, fig. 1, c, pl. xxix.), and in Lacerta (No. 14, figs. 2, 3, pl. xix.); while Scorr and
Oszorn’s figure of Triton (No. 147, fig. 5, pl. xx.) no less closely resembles it. The
last-named observers clearly saw that the notochord originated from the upper wall
of the alimentary canal, as is indicated in their figure just mentioned. The outgrowth of
the notochord from this enteric roof, figured in Pl. IV. fig. 5b, is not actually seen, but
* In Lepidosteus, Baurour and Parker noticed a similar sharp separation from the mesoblastic plates, while the
hypoblast had more intimate relation to the notochord, but they could not decide as to its real origin.
742 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
it is demonstrated that where the hypoblastic cells are not converted into the enteric arch
they proliferate to form the notochord anteriorly ; while the notochordal cells, ne, origin-
ating in this way merge posteriorly in the enteric roof (Pl. IV. fig. 5¢), precisely as they
unite in Elasmobranchs (No. 15, p. 683).
The notochord arises then as a ridge, or median proliferation, of the hypoblast in the
posterior portion of the mid-trunk; extending from that region, anteriorly, chiefly by a
progressive proliferation of hypoblast below, but doubtless to some extent, as already
mentioned, by a forward pressure of the hind part of the rod which is first formed.
K6LLIkEr’s view, that the notochord is continuous with the primitive streak (No. 81),
from which latter mass of cells the mesoblast arises and progresses forward, is consonant
with such a forward growth of the notochord in Teleosteans as we have indicated.
While the mesoblastic origin of the notochord is not generally accepted, there remains a
possible mode of origin which sections do not directly discountenance. If it is neither
formed from mesoblast nor hypoblast, it may yet be an axial differentiation of lower-
layer cells, constituting in sitw a median rod, when the mesoblast plates are cut off
laterally, and the neurochord is defined above. Such a derivation has much in its favour,
if we consider such sections as are given in Pl. III. figs. 2 and 11, and it is the conclusion
adopted by BaLrour and Drrcuton. In the case of the chick they found a median plate
of cells, not as yet divided into mesoblast or hypoblast, together with a short column of
cells originating from the primitive streak (No. 19, p. 186), and these form the notochord.
In Cyclostomes (Petromyzon) the notochord is formed by a vertical reduplication of axial
hypoblast-cells, as CaLBerLA (No. 39) showed, and as Batrour confirmed (vide No. 11,
p. 87, figs. 39, 40); but whether this holds true for the Elasmobranchs, or whether axial-
layer cells, as above stated for the chick, form it, BaLrour found himself unable to decide.
This uncertainty in regard to the origin of the notochord is further shown by the fact
that RupwANErR was of opinion that it arose from the epiblast ; while Kryestey and Conn
considered it hypoblastic, as also did Catperza for Petromyzon, Syngnathus, and Rana.
Braun, again, held that in the parrots the notochord was mesoblastic.
In Teleosteans Kuprrer affirms the origin of the notochord to be one of the unsolved
problems of embryology, and he declines to come to a decision on the question (No. 87,
p. 222). We have pointed out, however, that its hypoblastic origin is most in accordance
with the sections. The large cells (nc, Pl. 1V. fig. 5b) above the primitive enteron,
there is little doubt, are the first traces of the notochord, which further forward is already
partially defined. Fig. 11, Pl. III., again, is most satisfactorily interpreted as demon-
strating the meeting of cells from above (the neurochordal proliferation) with the noto-
chordal cells (hypoblastic proliferation) below. The cells of this longitudinal rod, ne, present
much the same features as the adjacent cells, mes and hyp, though the neurochordal cells,
ne, above always exhibit a more or less depressed appearance. At its anterior end the
notochord grows rapidly forward, and, as Scorr found in Petromyzon, it extends beyond
the hypoblast of the alimentary canal into the cephalic region. There is, in fact, an
anterior proliferation of notochordal cells (No. 146, p. 145). We see that in a series of
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 745
sections (Pl. IV. figs. 5b—5d) through the posterior region during the early stages of the
notochord ne, it widens out and becomes lost in the primitive streak (prs), or rather
merges in the upper wall of the gut, both disappearing in the caudal mass of indifferent
cells (prs, Pl. III. figs. 3 and 12), just as in Lepidosteus the notochord is not separated
from the lateral mesoblast, nor the latter from the neurochord, posteriorly. When ulti-
mately it is defined, and extends from its hind emargination to its oral termination
(ne, Pl. V. fig. 4), its cells do not long retain their primitive condition. They are not, as
in Triton, primarily large cells which divide into small cells, and again break up to form
larger cells once more (No. 147, p. 467), but are cells of small diameter—agreeing with
such as for the most part compose the embryonic trunk, and become larger by an increase
of their substance. Thus in a haddock of the fourth day (ve, Pl. IL. fig. 13) with the rim
at the equator, they can only with difficulty be distinguished from the mesoblast-cells,
mes, on each side; yet when the blastopore is just closing (fifth day, Pl. IV. fig. 10),
these cells, ne, are conspicuous for their large size and rounded contour, while their tend-
ency to assume a radial arrangement is marked. The larger size of the cells in transverse
section must, no doubt, in some measure be due to the forward pressure mentioned on a
previous page, for only three or four cells reach across the diameter of the notochord. In
their smaller, earlier condition six to eight cells extend across the same diameter.
While the notochord is well defined posteriorly (ne, Pl. IV. fig. 10), save at its
extreme aboral end (and Batrour and Parker found a similar obliteration of the notochord
posteriorly in Lepidosteus),* anteriorly it is even more distinctly marked (nc, Pl. IV. fig.
11), though as yet no chordal membrane surrounds it. When the blastopore is closing
the notochord does not reach as far as the pectoral region, but on the first or second
day afterwards it extends quite to the point where the cardiac swelling appears (PI. V.
fig. 8). About the time that the lenses of the developing eyes are visible the oral end
of the notochord is sufficiently well marked to exhibit the characteristic flexure in
front of the heart; but at its aboral end it spreads out slightly, and vaguely terminates
in the tail which is now defined and prominent (nc, Pl. XXIII. fig. 9; PL V. figs. 8
and 10). Transverse striations soon cross the notochord, due to the continued for-
ward pressure of its cells from behind, and cells here and there are seen breaking
down, so that discoidal plates, or rather irregular vertical septa separating intra-
cellular chambers, are formed. From its oral to its aboral end a continuous series of
these chambers appears, resembling the “interrupted pith” of botanists (nc, Pl. IV. fig.
12). The process of vacuolation, of the breaking down, and aggregation of flattened
cells in serial fashion, is preceded by the assumption of a radial arrangement in the cells
about to suffer alteration, their nuclei showing a centripetal movement, so that they are
mainly found along the central line of the notochord (nc, Pl. IV. fig. 10, just as
OELLACHER represents in No. 114, Taf. iv. fig. xvi, &c.). The process in Clupea, according
to KuprFEr, is not such as we have described for our forms, for the refractive dises, he
states, are formed by the confluence of minute granular particles in the primary cells as
* Phil. Trans., 1882, ii. p. 365,
744 PROFESSOR W. GC. M‘SINTOSH AND MR E. E. PRINCE ON
they become flattened. A simple series of these transverse divisions, termed by him
“ secondary cells,” is formed, and in a longitudinal section of the notochord he figures the
various stages (No. 87, Taf. iv. fig. 44). The irregular transverse septa in section (nc,
Pl. IV. fig. 12), are, however, evidently due to the adhesion of the walls of the primary
notochordal cells, and the confluence of their protoplasm to form large interstices.*
These septa become still more desiccated, and form a fine but complex meshwork, the
outermost portions of which constitute a limiting membrane. No such investment as the
latter as yet exists, though at a very early stage in Elasmobranchs BAaLFour made out a
special sheath, in fact, very soon after its formation (No. 11, p. 684). In Teleasteans
the neurochord above, and the hypoblast beneath, are in direct contact with the
constituent cells of the notochord during the early metamorphosis just described. A
stratum of flattened mesoblastic cells, it is true, at so early a stage as fig. 12, Pl. IV., may
clothe the sides of the chorda, nc, while a thickened layer of similar cells may intrude
between it and the hypoblastic enteron, g, destined, no doubt, to contribute to the later
perichordal sheath. This external mesoblast is probably the special sheath described by
LEREBOULLET at an early phase in Hsox (No. 93, p. 527); but at this stage the mass of
cells is external to and independent of the notochord, which must be regarded as a naked
cord of cells undergoing rapid vacuolation.
When vacuolation has proceeded so far that the mere transverse fissures of fig. 12,
Pl. IV., become converted into the spacious chambers more or less rounded, especially
in the caudal region (Pl. XV. fig. 4, ne), and subsequently into the more irregular
spaces (Pl. XI. fig. 11, and Pl. XV. fig. 7, ne), those collapsed cells which are not
included in the septa will be pushed outwards, and form, as in fact they do, a continuous
circumscribing sheath. The process is purely one of vacuolation, and the breaking down
of the boundaries of smaller cells to form larger ones. No dot-like aggregations, such as
Kuprrer describes, seem to take part in the process, nor do scattered yolk-spherules
(Baxrour, No. 11, p. 684) or oily elements occur (LEREBOULLET, No. 93, p. 527) in the con-
tents of the notochordal cells. The contents of the cells are fluid, clear, and homogeneous,
and often exhibit a slightly pinkish tint in certain lights, as in 7. gurnardus on the fifth
day. LereBouLer did not notice in his forms the early condition—the primary cells of
the notochord, for it was already transversely striated when he first observed its
structure; and he notes the remarkable feature, just referred to, that through all its
substance oily elements are dispersed (No. 93, p. 527, pl. ii. fig. 44). With its increase
in length the notochord grows in diameter, a condition which is precisely the opposite of
that described by Scorr and Oszorn in Z’riton, for in that form the notochord is largest
in cross-section during its earliest stages, and greatly diminishes in diameter during sub-
sequent stages (No. 147, p. 467). The increase in diameter of the Teleostean notochord
stretches the cells of the sheath, z,e., the superficial cells of the chorda; thus they become
* These interstices, with fine membranous limits, form a series of discs placed one behind the other along the
whole length of the chorda. They form large discoidal cells, which at many points do not entirely pass across the
notochord, as they vary considerably in diameter.
~
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 745
very thin, and at times almost imperceptible (ne, Pl. VIL. fig. 6). The true notochordal
sheath during the later larval periods is very delicate and fine (PI. VII. figs. 6, 6a), nor
does it, as BaLrour indicates (No. 11, p. 546), ever become thicker or more definite. It
is nucleated (n, Pl. XV. fig. 7), as GuGENBAuR showed in the greatly thickened sheath
of Salmo salar ;* but the nuclei are irregularly arranged, and in some sections they
are so sparse as to suggest the presence of an enucleate stratum (cs, Pl. XV. fig. 7),
though this condition is easily explained by its mode of origin. In horizontal sections
of the chorda the flattened cells of the sheath overlap and produce a more or less regular
tessellated appearance (Pl. XV. fig. 7). Kuprrer says that this sheath in the herring is
homogeneous and without nuclei (No. 87, p. 222), while he describes a round nucleus in
each chamber of the vacuolated notochord. Such nuclei in our forms are rare, though
sections often pass through the points, where several septa unite and produce the same
appearance as nuclei in the septa would do, but they are simply sections of the junction
of cell-wells, or, at times, merely the collapsed contents of the notochordal chambers.
Of the subnotochordal rod, which has been described by BaLrour, OELLACHER, RYDER,
and others, nothing definite can be here stated. It would, in fact, not appear to be
developed in the forms specially considered in this paper, though RypER mentions it in
Alosa and Salmo as a well-marked strand of cells ; and OELLACHER is of opinion that it
shares in the development of the aorta along the under surface of the chorda dorsalis.
The intruding mesoblast limiting the chorda below in the Gadoids, gurnard, and others
is an indefinite lamella figured in its earliest condition in Pl. IV. figs. 12 and 18, which
subsequently forms a median meshwork in which the early heemal lacunze are developed,
while laterally the renal connective and other tissues are formed out of it (vide Pl. VIL.
figs. 1, 4, 6).t
Vertebral Column.—The vertebral column and its costal appendages belong as such
to a stage subsequent to the larval condition proper, and, in this place, little more
can be done than simply to touch upon certain points observed before the close of the
first month after extrusion.
The cod and haddock will be mainly referred to, as the condition of the vertebral
column shows great differences in various Teleosteans; in some forms cartilage-cells
appearing, and cartilaginous arches developing soon after hatching, whereas in others
no such elements are present until the embryo is about a month old. LerEBoULLeT,
indeed, was unable to make out any ossification in the perichordal sheath, in Perca, until
the young fish was three months old (No. 93, p. 644).
The condition of the notochord before and after hatching has been described,
and sections of G. morrhua or G. eglefinus, on the seventeenth to the twentieth day,
show the same simple structure almost unchanged—the cuticular layer or nucleated chordal.
* Comp. Anat., Lond. 1878, fig. 221), p. 427.
+ The myotomes are broken up into fibres about the ninth day (two days before hatching in P. flesus). Eight or
ten of these fibres, in horizontal section, are seen passing across the shorter axis of the myotome, which is rectangular,
and measures about ‘001 in. x ‘0018 in., the longer measurement including the columnar external stratum of cells
lying beneath the epiblast.
VOL. XXXV. PART III. (NO. 19). 6c
746 PROFESSOR W. C. M‘SINTOSH AND MR E. E. PRINCE ON
sheath proper (cs, Pl. XI. figs. 14, 15) being very thin, and the mesoblastic perichordal
sheath (pes) but little increased in thickness. This latter sheath, of protovertebral
origin, is equivalent to the skeletogenous layer of Plagiostomes, though in them it is
greatly thickened. In this perichordal sheath an outer lamina can be made out, especially
when the rudiments of the vertebral bodies and arches are developed, as it forms their
outer investment. Below the sheath and its elastica externa, a layer of cells in the sharks
intrudes, coming, as BaLrour thought, from the outside, and forming the cartilaginous
tube around the chordal sheath. From this intruding layer the future vertebre are
formed, and it may be termed the inner skeletogenous layer: it is the inner half of the
skeletogenous tube. Outside the membrana elastica externa, however, another meso-
blastic layer is formed, viz., the outer half or outer skeletogenous layer from which the
neural and hemal arches are developed. In the less primitive sharks, such as Mustelus,
the Rays, and others, the inner skeletogenous layer is much reduced, and the elastica
externa is considerably nearer the chorda than in Cestracion and Notidanus. If we
consider the process of reduction to have affected the external portion until no outer half
exists, we can then look upon the perichordal sheath in Teleosteans as the inner half of
the skeletogenous layer, reduced, but still bounded by its outer limiting layer, viz., the
membrana elastica externa (mel, Pl. XI. figs. 14,15). There is, of course, difficulty
in separating the parts of a sheath so thin as that surrounding the notochord in
Teleosteans, but in a few forms, e.g., Cyclopterus, in which cartilage develops somewhat
precociously in the vertebral column, large chondral cells appear in this external layer,
which passes upward, and over the spinal cord as a membrana reuniens superior. The
cells likewise ascend up each side of the cord, forming the rami of the neural arch.
Similarly the ventral arch is developed. In many forms, however, the arches and outer
osseous laminze of the vertebral bodies are not preceded by preformed cartilage. In such
cases (e.9., Gastrosteus) the osseous matter is clear, homogeneous, and brittle (PoucHET’s
“ spicular substance,” KOLLIKER’s “osteoid matter”), and exactly resembles in its chitinous
appearance the clavicular portion of the pectoral girdle, and the maxillary elements of the
upper jaw. The presence or absence of this spicular substance seemed to KOLLIKER of
diagnostic value for classificatory purposes, but as PoucuEr points out (No. 119, p. 274),
both spicular substance and osteoplastic tissue may occur in the same form. PovucHET
states, and seems to be the first to do so, that in some cases osteoid processes, and in
other cases cartilage, with osteoplasts, form the superior and inferior vertebral arches.
But whether arising as bars of regularly disposed chondroplasts, or as homogeneous
spicular deposits, the vertebral bodies, and their projecting dorsal and ventral rami, are the
products of the perichordal sheath, and arise within its definite limiting layer. The view
that the main part of the sheath in Teleosteans is a thickened membrana elastica interna,
and derived from the cells of the chorda itself, is not supported by sections, inasmuch as
the hypoblastic notochordal sheath always remains extremely thin, and even when
well developed, as in the Salmonoids, is still merely a single stratum of flattened cells.
In Elasmobranchs W. MU uer recognised an elastica interna closely investing the
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 747
chordal sheath, and BaLrour refers to both layers as closely adherent, though distinct, but
the former apparently decreases in thickness, and is then ditlicult to see (No. 15, vol. xi.
p. 421). From the mesoblastic perichordal sheath alone the vertebral bodies originate,
while its outer limiting stratum (the elastica externa) gives origin to the arches. The
neural arches precede the hemal in development; uo trace, in fact, of the ventral
processes being discernible when the neural arches project some distance dorsally.
Of course, in a degenerate skeletogenous layer, such as the Teleostean perichordal
sheath, the identification of the precise layers, seen more favourably in other fishes, is
attended with much difficulty ; and one of us, in attempting to distinguish the different
lamin, has referred to the outer layer as a “ limitans externa” (No. 122, p. 454) ; indeed,
the opinion expressed that the existence of an “ elastica externa” in Teleosts, is a doubt-
ful point, is supported by the fact that such a membrane does not properly exist in
Amphibians, as well as in the Amniota. Favourable sections of Teleostean embryos,
especially such a form as Cyclopterus, bear out, however, the above interpretation, the
external layer being very distinct. Outside the perichordal sheath itself in post-embryonic
stages plates of spicular substance develop. Thus in a young but mature specimen of
Pleuronectes, the oral end of the notochord is seen to have acquired such a spicular
sheath—formed apparently in the connective tissue outside the external limiting
membrane—a distinct interspace separating the plate from the perichordal sheath. Four
rami of the same chitinous substance project, one pair dorsally and one pair ventrally,
and are well seen in sections through the otocystic region.
Branchial System.—The head of the Teleostean embryo consists, as already indi-
cated, of an expanded mass, chiefly neurochordal, or rather brain-tissue, and separated
from the cortex of the yolk below by a thin layer of hypoblast (hy, Pl. III. fig. 1). The
hypoblast forms here the roof of the sub-oral cavity, which has no floor, or rather, its floor
is simply the periblast enveloping the yolk. Behind and below the ears a large oval area
is apparently pushed in, resulting in the perforation of the lateral epiblast on each side of
the otocystic region, these fenestrae (poa) communicating with the primitive mouth-
chamber within (Pl VIII. figs. 3, 4). This opening, which may be called a primitive
opercular opening (pow), though the true operculum is a new and later growth, is plairly
visible in Molva vulgaris on the fourth day, along with a number of superficial irregu-
larities, doubtless connected with the active changes going on at this point in connection
with the branchial arches (Pl. X. fig. 6). The significance and function of this cleft
(Spritzloch) upon each side is not readily understood, as the cesophageal lumen is not
apparently open in front, and any perivitelline fluid which gains access to the sub-cephalic
chamber, probably cannot find passage into the alimentary canal. HorrMan, however,
speaks of it as produced by an evagination of the cesophagus, at first below the otocyst,
but shifting forward and opening in front of the ear (No. 69, p. 7; vide his pl. i. fig. 5,
emb. sp., also fig. 3, on p. 7). These embryonic “Spritzlocher,” he says, are merely
‘transient structures, and the interesting question is raised as to whether they may be a
reminiscence of the outer or extra-branchial system of the Cyclostomes, of which traces
748 PROFESSOR W. C. M‘IINTOSH AND MR E. E. PRINCE ON
are observable in the Elasmobranchs. Each aperture, poa, has a strongly marked
corrugated border or fold, which sweeps in a graceful curve round the opening, and
passes forward beneath the otocysts (aw, Pl. VII. fig. 4), for in pelagic forms, the shifting
of which Horrman speaks was not observed, and in front the fold is gradually lost.
The opercular flap is a much later outgrowth from the tympanic region, apparently a
fold of the integument, which protrudes, and grows backward over the gill-slits (ope,
Pl. XI. figs. 10, 11). Below the hind-brain and otocysts, the hypoblast shows great
increase in its cells, so that by the time the heart is defined it forms a thick supra-cardial
plate (Pl. XI. figs. 2, 7, 8), beneath which mesoblastic cells make their way by a down-
ward growth of the lateral cephalic masses. The sub-cephalic floor of hypoblast and
mesoblast is limited below by a somewhat ill-defined layer of nucleated periblast (per,
Pl. XI. fig. 8). The mesoblast thus intruding into the oral hypoblast becomes columnar,
and forms paired rod-like masses (PI. XI. figs. 5, 6, 7). The cells are concentrically
arranged along the axis of the transverse bars. LEREBOULLET evidently refers to the down-
ward growth of mesoblast, and speaks of it as a ventral lamella (7.e., splanchnopleure), out
of which, he adds, is formed later “the maxillary and hyoidean elements, and the gill-
supports.” While the appearance of serial mesoblastic thickenings along the floor of the
pharynx is a marked feature in Teleosteans some days before emerging from the egg,
their disposition and conformation are very difficult to make out. There is indeed con-
siderable variation in the condition of the branchial region, and this is especially seen in
newly-hatched gurnards. Usually three branchial bars are visible (Pl. VIII. fig. 8) as pale
structureless bands, with intervening cellular tissue, and passing transversely towards the
mesial ventral line beneath the otocysts. Batrour and Parker (No. 18) noticed in
Lepidosteus, six days after fertilisation, two transverse streaks on either side of the hind-
brain, From a comparison with the sturgeon they judged them to be branchial clefts, but
in section these clefts could not be detected. In the early condition of the branchial
system the study of sections is by no means easy. C. Voer shows, in an embryo of
Coregonus palea, thirty-six days old, branchial vessels, but indicates no skeletal bars (vide
No, 155, Taf. ii. fig. 58). The fact seems to be that, soon after the arches are distinctly
formed as definite bars, a vessel, or rather a long thread-like lacuna, is formed along the
posterior margin of each bar (Pl. XI. figs. 9, 11). Five transverse bands, some-
times an indication of a sixth, extend later on each side across the floor of the wide and
flattened cesophagus, from a point just behind the eye to a little distance beyond the
otocyst, so that the floor becomes raised into a series of cross-ridges which cease in the
middle line, and between the ridges the hypoblast is pushed so that the mesoblastic
ridges gradually become separated by hypoblastic septa. PARKER speaks of these ridges
as separated by the dehiscence of the thinned interspaces between them (No. 117), but
this hardly describes the process correctly, the rib-like thickenings being more truly
separated by the paired hypoblastie diverticula or septa, these being pushed out from the
sides and floor of the pharynx and affecting the differentiation of the serial gill-arches.
Dehiscence takes place, it is true, but much later, and it results in the formation of
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 749
actual slits, a phenomenon not seen until long after the arches are fully differentiated.
From this protrusion of enteric hypoblast, Sepcwick likened these paired pouches to
nephridia ; indeed, he considers them homologous, the kidney-system of vertebrates never
overlapping them, but commencing behind their posterior limits (No. 148, p. 67). The
clefts or gill-openings are probably not formed until some time after extrusion from the
egg, but the hypoblastic diverticula indicate their future position, and the dense meso-
blastic masses between them form the branchial skeleton or gill-arches. The latter in
their early condition appear as a series of rounded or subquadrate structures, when seen
from below (PI. VIII. fig. 5), but viewed from the side fine striations merely are observed
passing dorso-ventrally with a slight inclination forward, these striations being the linear
outpushings of the oral hypoblast (P]. VIII. fig. 6). The arches thus early indicated are
not simultaneous, and LEREBOULLET observed in the embryo of Perca that they appeared
successively from behind forward (No. 93, p. 616). The precise stage when the branchial
clefts are open cannot be stated. There is no doubt it is very late, for long after the
arches are clearly defined the slits are still unformed, even in so advanced an embryo as
Gastrosteus (Pl. XI. fig. 9), in which the mouth is open, while the hypoblastic cells, hy,
which pass down between and surround the bars, bra, still form a continuous layer. A
fifth branchial arch can be made out, but remains rudimentary in the Gadoids and other
forms here considered ; while anterior to the four branchial arches proper, two pairs of
stout bars are developed at an early stage, viz., the hyoid (hy, Pl. X. figs. 2, 3;
Pl. XIII. figs. 5, 6), and in front the mandibular (mn,—MeckeEv’s cartilage). Both these
arches undergo a more complex development than the branchial rods behind, and with
the appearance of cartilage-cells, both are readily distinguished by their greater length
and stoutness, as well as by their direction, both extending forward and tending rapidly
to complete the arch on the floor of the mouth. The upper portion of the first or man-
dibular arch becomes expanded (PI. IX. fig. 6; Pl. XIII. fig. 5); and Parker speaks of
it as well marked in the salmon (No. 117, p. 113), splitting longitudinally into two,
giving origin in this way to a fore part, the mandible proper, and a hind portion, the
hyoid. In our forms the hyoid is already well developed when the division of the man-
dibular cartilage takes place, and it would appear therefore that the posterior portion, hm,
which is the stronger, and much expanded at its upper extremity, is really the hyo-
mandibular, thus arising as an element separate from the hyoid, while the narrower
anterior part, pg, also split off, becomes the palato-quadrate. Before this splitting is
complete, the extended lower part separates as the primary lower jaw or mandible, mn,
and its proximal part becomes enlarged (PI. IX. figs. 6,7; Pl. X. figs. 2, 3), to afford
an articulating surface for the two suspensory elements above, the palato-quadrate and the
hyomandibular, which separately articulate, the former doing so earlier than the latter, and
more directly (Pl. IX. fig. 7). From the proximal portion of the mandible an anterior
process grows out at a subsequent stage (Pl. IX. fig. 7), while in the angle below the
end of the stout and broad hyomandibular, a small element, the angular, develops. The
forward growth of the palato-quadrate cartilage must be a late phenomenon, for the pre-
750 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
maxillee and maxillee develop in advanced embryos as paired translucent rods (PI. XI.
fig. 20), which gracefully curve, like bars of chitin, below the eyes forward to the
ethmoidal region, and form the sole lateral supports of the oral roof (Pl. X. fig. 1;
Pl. XIII. fig. 7). They are essentially superficial, and lie in a thin stratum of membrane
which stains deeply, called by Poucuer “ tissue générateur,” and occupying the situation
of Parker’s “ subocular bands,” though he regards them as the rudiments of the pterygo-
palatine arch (No. 117, p. 113). The homology of these dermal maxillary rods, with the
labial cartilages of more primitive forms, as suggested by Dr GUnrueEr (No. 61, p. 90),
is of much interest. A pair of curved bars, probably palatine elements, are also developed
in the roof of the oral chamber at a late embryonic stage. They are irregular in thick-
ness, slightly curved, and attenuated at the extremities (PI. XI. fig. 18).
When first distinguishable, the pharyngeal bars consist simply of solid mesoblastic
thickenings passing along the lateral and ventral walls of the mouth, and more or less
oblique in direction ; moreover, in cross-section, these thickenings are found to be paired,
and united in the middle line, forming a roof over the pericardial chamber (PI. XI.
figs. 1-3, 6-8). The cells assume a columnar arrangement, and constitute lamine,
which appear as parallel superposed strata, when the bar is cut longitudinally (Pl. XI.
fig. 9), but in a cross-section of a bar these strata are observed to be somewhat concentric
and laminated (Pl. XI. figs. 6-8). Each rudiment of a branchial arch (fg, Pl. XI.
figs. 6-8), when fairly defined, consists of a cylindrical mass of cells, concentrically
arranged round the central point of the bar, and limited above by the epithelial hypoblast
of the pharynx, and below by the pericardial hypoblast. They increase in length, and
change from the transverse to the antero-posterior oblique position (PL VIII. fig. 9), the.
inner extremity of each pair of arches apparently shifting forward, so that they point
anteriorly (Pl. X. figs. 2, 3, 5); while their upper and posterior parts, which extend
up the lateral walls of the pharynx, have moved very slightly from their primary position.
Neither the mandibular nor the hyoidean arches are so markedly transverse in situation as
the branchial bars proper, and they alter very little in position as development proceeds.
In the gurnard, three days old, at the anterior end of the hyoid arches, 7.e., where the
copula is formed, a large boss occurs, formed chiefly by a free development of the lining
membrane of the oral floor, This membranous expansion (really a lingual rudiment) pro-
jects as a large irregular elevation on the floor of the mouth, and is lifted up by the
erratic movements of the hyoid arch, as though the operation of deglutition were being
performed (Pl. XIV. fig. 2). Gradually the arches lose their dense indifferent appear-
ance, and become converted into cartilage, the small primary cells being broken down, so
that each bar consists of larger flattened elements placed transversely, and giving the
arches a transversely striated appearance (PI. IX. fig. 5). The flattened cells become
hyaline, and each arch shows a single column of hyaline discs contained in a thin peri-
chondrial membrane. The first two arches wholly assume this character, and are seen to
be composed of these discs or chondroplasts placed one above the other along the
whole length of each bar (see the figure just referred to); but in the four arches which
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 751
follow, only a portion undergoes this change, viz., that part of each bar nearest the
pharyngeal cavity, 7.e., throughout the entire upper part of each. The rest of the bar
remains indifferent in structure until a tubular cavity is formed from end to end. This
tube at first is apparently single, but later is divided by a delicate septum into two tubes,
an upper arterial and a lower venous trunk. External to and below the hemal canals
the loose epithelial covering of the bar becomes nodulate, a double row of papillee pro-
jecting on the posterior and ventral side of each arch. The appearance of these gill-
rudiments is thus preceded by a considerable interval by the conversion of the arches
into cartilage, as LEREBOULLET observed in Perca (No. 93, p. 623), the same author noting
in that species the growth of the gill-tubercles from the soft cellular membrane covering
the gill-arches (see his plate iii. fig. 7). Moreover, he speaks of them as hollow (p. 627),
an appearance probably due to the intrusion of mesoblast into each papilla, which is thus
provided with a mesoblastic core and a hypoblastic epithelial covering.
The formation of these branchial tubercles belongs, it may almost be said, to the first
post-larval stages, and their subsequent development into the branchial fringes of the
adult leads beyond the present limits.*
The further development of the early cartilages may be easily followed in a large
chondral element such as the hyomandibular, or the massive mandible itself. The disc-
like chondroplasts which form a single column along the entire length of the bar (Pl. IX.
fig. 5), slightly alter in form, becoming wedge-shaped when seen laterally, and lie over
each other in an alternate manner, as though about to separate into two rows,—sometimes,
indeed, a disc becomes thin in its median part, and divides, resulting in two wedge-
shaped chondroplasts. Thus the original single column of chondroplasts becomes broader,
and exhibits two or more rows (PI. IX. fig. 7). In the mandible this change affects the
upper or articular portion, while the anterior growing part, which continues to lengthen
until the cartilages of each side meet at the tip of the extended oral floor, still maintains
its simple columnar character, and consists of a single series of chondroplasts. In other
cases, as Poucner noted (No. 119, p. 296), the chondroplasts towards the extremities
lose their disc-like form—becoming irregular in outline and mingling with the enveloping
tissue—just as in the limbs of young Amphibians. In the region of the joints, as in the
upper or articular portion of the mandible, the chondroplasts become irregular, numerous,
and disposed round the joint conformably to the contour of the articulating element
(Pl. IX. fig. 7). The development of a crest is due to the protrusion of similar small
irregular chondroplasts, which grow out, row upon row, as a strong lamella. PoucnEr
regards these new chondroplasts as not due so much to fission of existing chondro-
plasts as to development from the nuclei, so plentiful in the perichondrium or “ tissu
générateur” which clothes the bars (No. 119, p. 298). These nuclei he describes as
crowded at the margin, and, as they pass inward, become separated by the intrusion of
the hyaline matrix.
* In Esox and Perca the yolk has decreased and its circulation has been almost obliterated, according to
LEREBOULLET, when the gills are formed (No. 93, pp. 613, 627).
752 PROFESSOR W. C. M‘SINTOSH AND MR E. E. PRINCE ON
In the young cod, three weeks after hatching, the branchial system is wholly converted
into cartilage, and forms a complex series of translucent hyaline bars, in which the four
parts—the epi-, cerato-, hypo-, and basi-branchial pieces can be distinguished, and the
small rod-like azygos pieces in the middle of the oral floor form the several copulee for the
respective arches.
In 7. gurnardus, and other pelagic forms, the cartilages of the jaws apparently
become stiff and immobile about the eighth day after hatching, and the hyoidean
apparatus also shows no regular movements. The fish, however, by its forward jerking
motion, drives water into the widely-open mouth, and aeration is thus easily effected, for
the opercular opening is broad, and the operculum itself projects outward and backward,
as a thick flap of the integument.
The mandibular rami, mn, continue to lengthen upon each side to such a degree that
they project much beyond the upper jaw, and asymphysis is formed at the anterior margin
(Pl. X. figs. 1-5). No feature is more striking than this extraordinary development
of the lower jaw, and in sickly and abnormal embryos it produces the most fantastie
appearances—the protruding mandibles frequently curving downward, so that the gape
of the young fish is remarkably wide (Pl. XIV. fig. 2), and even in normal examples this
extension of the floor of the mouth, and the mobility of the lingual and hyoidean struec-
tures, increase the oral aperture very much (Pl. X. figs. 1-3, 5, 5a), and contribute
doubtless to facilitate the capture of the minute organisms which form the earliest food
of the young Teleostean.
Skull.—The capsule enclosing the brain is, like the rest of the body of the embryo,
simply a thin epiblastic layer composed of the flattened corneous stratum, and the thicker
sensory remnant beneath.
Between this ectodermal covering, ep, which though expanded in the form of
a bulbous protective capsule, can scarcely be regarded as a cranium, and the brain-mass
below, a space intervenes occupied by a transparent substance, apparently of a jelly-like
consistency. This space, ss, filled with fluid, is inconsiderable during the earliest stages
within the ovum (PI. XIX. fig. 10), and even in a newly-hatched fish (ss, Pl. VIL. fig. 6),
above the mid-brain, mb (optic vesicles), it is small, though larger in front (between the
nasal capsules), fb, and behind, Ab (over the cerebellum and fourth ventricle); but it in-
creases at the end of the first week (Pl. VIII. fig. 7), and during the second or third week
after extrusion it becomes enormously enlarged, and imparts to the more advanced embryos
avery grotesque appearance (ss, Pl. XII. figs. 2,6; Pl. XVI. figs. 1, 3,5). Often this
sub-epidermal enlargement abnormally develops, and embryos with the cephalic region
remarkably swollen are not uncommon—fig. 3, Pl. XVI. being probably such an example ;
but under ordinary conditions the enlargement is considerable, and median sensory papillze
appear in it, immediately beneath the corneous layer, with connecting nervous filaments
passing downward, probably to the lateral sensory tract (sno, Pl. XVII. fig. 1).
At an early stage the mesoblast of the head consists of a thin stratum chiefly aggre-
gated between the eyes and the neurochord (mes, Pl. IV. fig. 17), while, above, the brain
eo
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 75
is directly in contact with the inner surface of the epiblast. Later, however, this meso-
blastic tissue extends and finds its way into the lateral sinuosities of the brain-surface,
and it passes upward as a thin membrane composed of much flattened cells, which
finally more or less completely invests the brain. The relation of the two is very
intimate, and probably the pia mater is at this time separated, though any differentiation
into distinet strata cannot be made out in the membranous investment (mes, Pl. IV.
figs. 14,21). From this layer, however, the three membranes—dura mater, arachnoid, and
pia mater—are ultimately differentiated. On its inner surface pigment rapidly develops,
as early, indeed, as the fourth day after fertilisation in some forms (p, Pl. IV. fig. 13).
We have thus a double covering over the brain, for to the simple ectodermal layer (ep,
fig. 14), which primarily covers the neurula, there is added a thickened mesoblastic
membrane (mes), constituting the primitive membranous cranium (Pl. IV. fig. 215
Pl. XXIII. figs. 1, 2, 83a; Pl. XXIV. figs. 3, 5, 6). Meanwhile changes are proceeding
at the base of the brain, and whereas it at first lay almost directly upon the yolk
(Pl. IV. figs. 3, 4), separated only by a thin layer of hypoblast (iy), it now rests
upon a floor of mesoblast (PI. IV. fig. 21). This mesoblast is apparently an exten-
sion forward of the pectoral mesoblast, which pushes anteriorly as the notochord advances,
and when the latter finally terminates beneath the mid-brain, a plate of intruding meso-
blast is seen extending upon each side of it and passing as a thin sheet beneath the fore-
brain.
At the fore end of the notochord quite a dense plate is formed (Pl. XI. fig. 2), and
a thickened continuation of this mesoblast passes beneath the eyes, forming a projecting
ridge of epiblast with a core of mesoblast (Pl. XI. figs. 2, 3), which is doubtless
Parker's “ sub-ocular band” (No. 117, p. 119). These two ridges form on each side a
lateral flap or curtain, and the head is thus raised slightly from proximity to the yolk.
As already pointed out, before an actual oral slit appears, an oral cavity exists whose
roof slopes considerably on each side, and meeting in the middle line forms a highly
arched chamber. A section through this acutely angular cavity in the region of
the posterior prosencephalon (thalamencephalon) shows the apex, so to speak, marked
by a small and solid mass of cells, a cylindrical rod in fact, which in sections further
forward is found to flatten out in the form of a bilobed plate, strongly suggesting the
union and depression of two cylinders of cells. We see then at this early stage, about
the time of hatching, that the base of the brain is strengthened by two parachordal masses,
which lie on each side of the notochord at its oral end, e.g., in the section of Anarrhichas
(Pl. XXIV. fig. 3), and form a dense basilar plate, while further forward the flattened
parachordals cease, and in their place two thin cylinders, the trabeculae, can be dis-
tinguished (Pl. XXIV. figs. 5, 6), which, as just pointed out, unite and form beneath the
thalamencephalon a single rod.* This rod again expands beneath and in front of the
* The early appearance of the trabeculs is noteworthy when connected with the early development of the neural
arches in the trank. Parker’s view that the trabeculw are ventral arches of the vertebral column, serially followed
behind by the branchial arches, has been much disputed, and the early appearance of the neural arches of the vertebral
column is opposed to PARKER'S view.
VOL. XXXV. PART III. (NO. 19). 6D
754 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
fore-brain, to terminate in a pair of large flattened lateral horns, and an internasal plate
centrally (Pl. XI. fig. 11). These early skeletal structures are the first indications of the
cartilaginous cranium, but as yet they are formed of closely-aggregated cells, which
stain deeply, and on account of their density are readily distinguished from the adjacent
mesoblastie cells out of which they have been differentiated. Whether their cells break
down or not is difficult to make out, but they undoubtedly become antero-posteriorly
flattened, and in cross-section the rods under consideration begin to assume a more trans-
lucent appearance, due to the discoidal character of the constituent cells. Within a week
or ten days after hatching, these elements are converted into clear boldly-marked nucleated
cartilage-cells, The large parachordals as they become cartilaginous extend outward, and
meet to coalesce with the dense cartilaginous floor of the auditory capsules (Pl. VI.
fic. 9; Pl. XXIII. fig. 2). The trabeculee between the eyes contract, and approach the
base of the brain in the region near the infundibulum—becoming very narrow as the
roof of the brain expands. Further forward the trabeculze, however, spread out, forming
a large anterior plate of cartilage, slightly thinner medially, and more thickened later-
ally, .e., in the portion forming the cornu (Pl. XI. fig. 11).
While cartilage thus abundantly develops in the skull, no trace of it is seen in the
axial skeleton of the trunk—metameric aggregations of mesoblastic cells (PoucHET’s “tissu
générateur”) alone indicating the points along the notochord where the future vertebrae
will be formed. During this time also cartilage appears in the form of four small plates
around each eye, all with a concave surface towards that organ, and formed of large
cartilage-cells placed over the summit of the eye—beneath and on the anterior and
posterior surfaces. Whether the first or supraorbital cartilage expands later to form the
tegmen cranii, and the second to form suborbital elements, while of the remaining two
one becomes the lachrymal, and the other or postorbital becomes alisphenoid and post-
frontal, though probable, could not be determined from an embryo in the second or third
week after hatching. About the middle of the third week, indeed, four series of cartilages
may be distinguished—(1) the posterior basal, (2) the posterior lateral (auditory), (3) the
anterior lateral (optic), and (4) the anterior basal.
The first named constitutes the basis cranii proper (parachordal and occipital elements);
the second includes a basal auditory plate (Pl. VI. figs. 9, 10), very dense and
massive, and affording an outer articular surface for the hyomandibular (Am), and
probably consisting of opisthotic and pro-otic elements, as yet undifferentiated. Above
the ear a small aggregation of cartilage-cells (epot, Pl. VI. fig. 3) occurs, from which the
epiotic and supra-occipital are probably formed, while the third series are in a condition
too early to identify, and are best regarded simply as circumorbital cartilages developed
at four separate centres on the surface of the sclerotic membrane. The fourth and last
series occurring at this stage are the trabeculee, with their expanded internasal element
and the curved lateral cornua. Into the theoretical question of the significance of these
paired basal bars it is here unnecessary to enter.
Of the further changes in the skull and facial elements little can be said, as at the end
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 755
of the first month the young embryo shows little further modification. The development
of translucent spicular plates upon the surface of the more exposed bones, especially of the
face, is a noteworthy feature in the young fish, but belongs to the post-larval period.
It may be noted, however, that these homogeneous spicular plates are not solely of
dermal origin—in fact, they develop as a thin outer layer of the true cartilaginous
elements, and arise within the nucleated perichondrium.
The connective-tissue septa of certain muscles which are much used, become changed
into thin rods of clear spicular substance, a median rod, for example, passing up beneath
the pericardial cavity, and forming a fulcrum for the retractor hyoidei muscles. A similar
bar occurs also between the genio-hyoidei.
Brain.—The anterior enlarged portion of the neurochord, of which frequent mention
has already been made, is really the brain. It extends the whole depth of the fore-region
of the embryo, forming a somewhat rhomboidal mass, rounded above, deeply carinate
below, and arched over by the epiblastic integument, while it is limited ventrally by the
hypoblast (Pl. IV. figs. 3, 4). The growth of the large optic vesicles, as two massive
ellipsoidal bodies (op, Pl. IV. figs. 14, 16), protruding laterally from this region, is an
early and notable feature; but the details will be considered later, with the sensory organs.
The part which becomes the mid-brain (mb, Pl. IV. figs. 16, 17) is very early distinguished
by its greater breadth and volume from the narrower and prominent snout (fb), while the
hind or metencephalic part (1b) gradually passes away into the neurochord (ne) of the
trunk. No division as yet separates the encephalic from the spinal portion of the neuro-
chord, and the former is distinguished only by its increased breadth and depth. It is
remarkable, too, as extending fully one-third the total length of the embryo in its early
condition. No transverse cerebral folds appear until about four-fifths of the yolk are
enveloped, when a cleft, very obliquely directed, appears on each side of the post-optic
region. An anterior portion—the united mid- and fore-brain—can now be distin-
guished from the hind-brain (4b). The latter is, very shortly after, separated by a
similar though less marked fold from the nervous cord (ne) behind, LEREBOULLET
noticed this early transverse folding, which he says is due to the brain becoming doubled
upon itself; but he erroneously supposed that the cleft first formed is the metencephalic,
instead of the mesencephalic, and further conceived the neural tract to consist of two
parallel tubes. These becoming folded, produce two vertical projections, which he calls
the cerebellar lamellae (No. 93, p. 533). It is really the cerebral fold, the cerebellum
being, as just stated, marked off slightly later. The mid-brain, lastly, is constricted off
by an interorbital fold, so to speak, and the three regions of the brain are now defined
(Pl. IV. fig. 17). Reference has already been made to the dorsal or medullary groove ;
but it is at this stage, when the brain is separable into cerebellum and united mid- and
fore-brain, that this groove often appears in a very marked manner. Thus, in 7. gurnardus,
on the fourth day, a deep median fissure may be seen—the sides of which slope at an angle
of about 70°. It isa temporary groove, as previously pointed out, and not apparently con-
nected with the subsequent cerebro-spinal canal. Soon after the closure of the blastopore,
756 PROFESSOR W. C. M‘INTOSH AND MR E, E. PRINCE ON
sometimes a little earlier, a fine cleft (mc) appears by separation of the median cells of the
encephalon along a vertical longitudinal plane. It commences in the mid-brain, and passes
into the fore-brain, extending almost to the anterior limits of the latter (PL IV. fig. 17).
This is the first indication of the true neural canal. It passes dorsally, ceasing before
reaching the upper surface of the brain, and ventrally, leaving below a thick tract of
nervous cells uncleft. The early brain thus becomes incompletely divided, as RypER
aptly expresses it, into “two flat thick plates of cells placed vertically between the eyes”
(No. 141, p. 503). At its anterior termination the canal sends off two lateral vertical
continuations, forming a cruciform fissure which marks off the fore-brain (fb, Pl. LY.
fig. 17; Pl. VI. fig. 6); while in the mid-brain, as the fissure ascends, it bifurcates laterally
and horizontally, so that the lumen of the mesencephalon, in cross section, is T-shaped
(Pl. IV. fig. 21), the roof being thinner than the walls and floor, which are very dense, a
feature better seen in sections of Anarrhichas (Pl. XXIV. figs. 3, 6). No continuity of the
central canal with the lumina of the optic vesicles seems to be completely established, and
certainly no trace of such a connection is observed in sections at this stage. The canal
now rapidly extends posteriorly into the trunk, and as it does so vertical lateral cavities
are sent off, one pair in front of the cerebral fold, forming the optic ventricle or [ter
a tertio ad quartum ventriculum, and a second pair, constituting the fourth ventricle,
immediately posterior to the cerebellar fold (cb, Pl. VI. fig. 6). The most notable
feature at this early stage is the continued lateral extension of the mesencephalon (mb),
and its progress backward over the metencephalon (cb), until it almost covers the
latter with its two broad lobes, which continue to increase in breadth (compare figs. 5
and 7, Pl. VL). Between the eyes we have, therefore, a prominent mesencephalic
dome formed of two halves, narrower in front, but broad and overlapping the narrower
posterior fore-brain (thalamencephalon) and the base of the mid-brain. Several days
before hatching this extension of the mid-brain takes place, the T-shaped chamber
(optic ventricle) increasing in its upper portion and its lateral regions until the roof
above exhibits a considerable decrease in thickness and a marked columnar disposition
of its cells.
An embryo before hatching usually shows such a development of the mid-brain as
above described (vide Pl. XIV. figs. 1, 2), and the brain-mass as a whole exhibits that
separation and arrangement of its parts which permanently remain in Teleosteans. The
mesencephalon embraces the largest extent of the brain, and by its prominence above
imparts that rounded bulbous form to the head which is so characteristic of the young
fish (Pl. VI. fig. 75 Pl. Vii Sigs. a6.) 7, 105° BL XI, sfiga::d 55,6292 ae
figs. 2, 4). Thus the medulla oblongata (mo), with the anterior transverse fold or
cerebellum, forms a hind-brain plate of triangular shape, the mid-brain (mb) constitutes
a similar triangular mass, and both have their broader sides or bases towards each other
(Pl. VI. fig. 6), just as Kuprrer deseribes in Clupea (No. 87, p. 220). The cerebellum is
almost entirely covered by the posterior enlargements of the optic lobes (op, Pl. VI.
fig. 7), but it protrudes distinctly as a thickened ridge passing across the front end of
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 757
the fourth ventricle. A very thin roof continues from the cerebellum and covers the
medulla oblongata, whose triangular floor is becoming better defined and dorso-ventrally
deeper. Laterally the cerebellum (cb) does not break continuity with the double fold of
the mesencephalon (mb), of which, indeed, it appears to be merely a thickened posterior
portion or third fold (Pl. VI. figs. 5, 6). This fact has led many anatomists to deny to
this fold the name of cerebellum. MM. Puitipraux and VULPIAN regard it as merely a
third lobe of the optic mass, and they, with many others who follow Weber (Anatomia
comparata nervi sympathici, Leipzig, 1817), regard the two swellings passing along each
side of the medulla oblongata, and composed of grey vesicular matter, as the cerebellum.
MM. Puitieraux and Vunrian emphasise the view that the cerebellum consists of the
two hollow lateral masses which flank that part of the optic mass usually called cerebellum
(No. 118, p. 171). More recently Mixiucno-Mactay has urged a similar view regarding
the Elasmobranch brain, and he interprets the prominent anterior portions of the corpora
restiformia as the true cerebellum. Beneath the cerebellum the medulla continues
forward and merges in the basal region of the thalamencephalon, and even in this
early condition distinctly turns upward, the curvature becoming marked somewhat later
(Pl. XXIV. figs. 1, 2). Ryper states that in Alosa this upward bend is not indicated
(No. 141, p. 504), but it is probably a notable feature in most Teleosteans. Dour, for
instance, indicates it in Belone and the Lophobranchs, and the result of it is that the fore-
brain is brought down below the front termination of the medulla oblongata, and a false
cranial flexure is thus effected. The actual relations, in regard to position, of the brain-
vesicles to, say the notochord, are not altered, nor does the head-region externally
present a marked flexure downward (Pl. XIII. figs. 1, 5); yet a longitudinal section
through the brain shows, as in the section of Anarrhichas (Pl. XXIV. fig. 2), the
mesencephalon raised up, while the prosencephalic region bends down. If we follow
the course of the medullary canal, we find in front of the cerebellum a marked
ascent—the hollow optic lobes occupying a much higher plane than the thalamen-
cephalon and the hemispheres, and the result is that, without the remarkable shifting
forward of the parts of the brain seen in the chick, the prosencephalon comes to
lie on the ventral side of the medulla and cerebellum. This modified flexure, which is
not comparable to the true and extensive bending down of the prosencephalon, e.g., of
Elasmobranchs, has this simple explanation, that without any very obvious displacement
of the other parts of the brain, the floor of the myelencephalon and metencephalon are
flexed upward, and, as a consequence, the mesencephalon is raised, and the thalamen-
cephalon and hemispheres come to occupy a distinctly ventral position. This false
flexure persists even after the embryo has emerged from the ovum, but with the fuller
development of the oral region it is at a later post-larval stage corrected.
The remarkable displacement just described does not change the external aspect of
the embryo. The mid-brain still occupies the summit of the head—its greater pro-
minence being due to the process of median upheaval from below, which brings the
lateral margins of the optic lobes into proximity inferiorly with the eyes. The optic
758 PROFESSOR W. C. MINTOSH AND MR E. E. PRINCE ON
lobes, as before stated, laterally overlap the basal region of the mid-brain, at an early
stage; but this superposition is now considerably increased—indeed, it reaches fully to
the middle lateral line behind the eyes (PI. XXIV. fig. 3). The fore-brain still forms a
narrow, laterally compressed mass projecting anteriorly to form the round snout or face
of the embryo. Its bulk is less than half that of the mid-brain, and it encloses a small
dorsal chamber (Pl. XXIV. fig. 5). The prosencephalic floor is very dense, the side
walls less so, while the roof thins out greatly. A small fissure continued from the
chamber above passes into and partially divides the thick floor of the fore-brain; but
sections of this region show a condition much in contrast with the capacious hollow
vesicle of the Elasmobranch fore-brain. Several folds appear on the superficial aspect of
the fore-brain (Pl. VIII. fig. 6) about the time of hatching or even before: but not until
the second or third day after emerging does the deep fold appear which divides the fore-
brain into two parts, the cerebral or anterior fore-brain and the thalamencephalic or
posterior fore-brain (Pl. VI. fig. 7). A longitudinal fold passes over the dorsal surface of
the fore-brain (fb) before it is markedly separated into front and hind prosencephalie
regions, and it thus becomes longitudinally bifid at an early stage (Pl. VI. fig. 6).
No olfactory lobes proper exist as yet; indeed, as MARSHALL found in Salmonoid larve,
these structures must be comparatively late in appearing.
The changes which ensue when the primitive brain of three vesicles is finally divided
into a series of five, are very complex and difficult to follow; but the main features may
be indicated. The five parts of the brain distinguished are as follows :—
(1) Anterior fore-brain or cerebral hemispheres, &c. (“ Vorder-
Prosencephalon, hirn,” GEGENBAUR and Bakr).
(2) Posterior fore-brain or thalami optici (“ Zwischenhirn,” Barr),
(3) Mid-brain, or optic lobes, &c. (Mittelhirn, Barr, Zwischenhirn,
Mesencephalon,
GEGENBAUR).
Metencephalon a Hind-brain or cerebellum (Hinterhirn, Barr, Mittelhirn,
; a | GrGENBAUR).
Myelencephalon, — (5) Medulla oblongata (Nachhirn, GrGENBAUR).
From the fourth ventricle a narrow fissure, the aqueductus Sylvii, leads into the third.
The base of the latter partly overlies, and partly abuts against, the mass now separated,
as already indicated, from the cerebral hemispheres or anterior fore-brain by a transverse
superficial cleft (Pl. XIII. fig. 1). This posterior portion of the fore-brain is the
thalamencephalon, and it is the part of the brain which, for the most part, overlies the
roof of the mouth.
Very early a portion of the hind part of the thalamencephalic floor is directed back-
ward as a prolongation beneath the elevated medulla oblongata, and during its course its
direction is slightly downward. The cells composing this encephalic diverticulum have a
somewhat columnar arrangement, and surround a cavity continuous above with the third
og ee
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 759
ventricle. The structure thus formed is the hollow infundibulum (inf, Pl. XXIV.
fig. 1), which abuts on the roof of the oral cavity below, though the two remain
separate. The anterior part of this basal region gives origin to the optic nerves, which
will be considered under the sense-organs. A chamber, or rather a loose meshwork of
cells (Pl. XXIV. fig. 1), most probably hypoblastic, though possibly mesoblastic, lies
behind the infundibulum, and into this loose mass the oral end of the notochord (no)
pushes as it bends downward. In some sections the notochord and infundibulum are
brought into closer contact. The elevation of the oral roof too is very distinctly marked at
this time, and such probably (see Pl. XXIV. figs. 5, 6) corresponds to the curvature pro-
duced in Elasmobranchs by the acute cranial flexure characteristic of those fishes and higher
forms. On the summit of this arch a mass of cells appears, evidently a proliferation of
the oral roof-cells rather than a diverticulum. This ovoid mass is the pituitary body
(pt, Pl. XXIV. fig. 1). It lies in front of the infundibulum, and from its origin is in
close relation to the base of the thalamencephalon. The precise origin of this body in
these forms is difficult to make out, but its cells, as Horrman has clearly shown in the
salmon and trout, are indistinguishable from the oral epithelium.* A small median
swelling, not unlike the hypophysis in structure, lies in front of the latter—that is, behind
and slightly under the point where the optic nerves decussate. When further advanced
such appears to form the hypoaria or lobi inferiores—so well developed in Percoids, and
their special ventricles in the adult communicate with the lumen of the infundibulum.
The anterior fore-brain and the mid-brain at a very early stage so far overlap the
intervening mass (the thalamencephalon) that only a small portion of its roof is super-
ficially exposed (Pl. XXIV. fig. 1). This small extent of roof becomes very thin, as does
also the roof of the anterior fore-brain, and it is much folded. In a transverse section
through the mid-portion of the thalamencephalon before its walls have thinned out, a
central aggregation of cells can be distinctly observed, and this soon exhibits a marked
concentric arrangement, and become slowly pushed out as a papilliform process (PI. VIII.
fig. 6). A lumen develops at a later time, and it communicates with the (third)
ventricle below. Its cells, which were rounded and not dissimilar to the adjacent cells of
the thalamencephalic roof at this time, assume a columnar disposition, and it now forms
that very prominent and interesting structure in young fishes—the pineal gland. The
primary rounded or conical form is not long retained ; it either becomes truncated, i.e.,
depressed, or more or less plicated, and pressed against the thin developing arachnoid
membrane, which alone separates it from the integument. In the salmon and trout
HorrMan gives a slightly different account of its origin. It arises, he says, as a true
evagination, not a solid protuberance, and its lumen is continuous with a portion of the
ventricle below distinctly marked off as a special recessus infra-pinealis (No. 69,
pp. 100, 102). Moreover, its cells are at first epithelial in character and columnar,
* Dourn states that the hypophysis makes its first appearance at the same time as the endodermal evaginations
of the oral and branchial clefts. It arises as a pair of more or less distinct pouches much anterior to the paired oral
slits.
760 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
whereas the rounded form is only assumed later when the cells have increased in number,
and form two or three layers (No. 69, p. 103; ef: figs. 9, 12, Taf. iv.). Much later, when
the absorption of the yolk is accomplished, the lumen of the epiphysis becomes obliterated,
and it is separated off as an oval, lobed, or deeply folded solid mass of cells (No. 69,
p. 103, Taf. iv. fig. 17).
The spinal cord, when fairly advanced, proceeds quite to the termination of the
notochord, but its general features call for no detailed description. Usually the terminal
filum is very delicate and attenuated ; but at times a remarkable enlargement is observed.
This final nervous swelling was very well seen in a young embryo of Motella mustela
(Pl. XV. fig. 4, ne), but in other forms it was also made out, e.g., Cottus scorpius
(Pl. XIII. fig. 2) and Molva vulgaris (PI. V. fig. 7).
Auditory Organs.—The otocysts are very early differentiated—that is, about the
same time that the lens of the eye is invaginated and defined (as pointed out by Kuprrer,
No. 88), 2.e., in many pelagic forms about the fourth to the sixth day after fertilisa-
tion. In Salmo salar, according to Parker, the ears are pushed in from the outside
shortly before hatching; and he refers to these “auditory involutions” as “still widely
open” during his “first stage” (No. 117, p. 113). This description, however, is quite
unlike the mode of formation in the Teleosteans specially referred to in this paper; and
LEREBOULLET'S account, in the case of Esox luctus, is certainly more in accordance with
observations at St Andrews, where he says that the early ears “are two small spheres,
symmetrically placed, and formed by the grouping of plastic elements, . .. . at first
solid; but becoming hollow, and transforming into the auditory capsules” (No. 93,
p. 529). The otocysts are, in fact, not involutions of the external epiblast, but solid
proliferations of the sensory or neurodermal epiblast (av, Pl. IV. figs. 4,11, 16a). In
Lepidosteus Batrour and Parker describe the ear as originating from the under or
sensory layer, but as a hollow thickening, over which the epidermiec layer is externally
continuous (No. 18); and Horrman, while he rightly speaks of this external layer
as extending unbroken over the otocyst, says that the otocyst itself is formed as a
hollow invagination of the under-layer (Grundschicht), a condition not exhibited by
our sections of pelagic embryos. The earliest phase seems to be that of a rounded mass
just becoming visible in the early haddock, «e., a solid proliferation of the sensory
stratum (conf: Pl. IV. fig. 11, the figure referred to, with Horrman’s, No. 69, figs. 3
and 4, Taf. i., and fig. 1, Taf. iv.), in which very soon a radial arrangement of cells can
be made out preparatory to the formation of a lumen. ‘The latter rapidly appears
(au, Pl. IV. fig. 13; Pl. V. fig. 8), and is at first minute and spherical, but soon
enlarges to form a spacious ellipsoidal chamber (aw, Pl. VI. figs. 5, 6), very obtusely
rounded, depressed laterally, and with its inner wall abutting against the neurochord (ne),
while on its outer side, and superiorly, it is separated from the exterior only by the
tegumentary epiblast (ep). The walls of the otocyst are very dense when the lumen is
small (au, Pl. IV. fig. 13), but they apparently stretch as the chamber expands, and
become comparatively thin (au, Pl. V. fig. 9; Pl. VIL. figs. 1, 2, 7). LeresouLLer
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 761
noticed that, as the auditory vesicles elongate, ‘a mass of yellowish granules” appeared
in them prior to the formation of the true otoliths (No. 93, p. 529). The contents of the
otocysts seem, however, to be clear, homogeneous, and without granules in our forms, but
usually before the end of the first week, and within twenty-four hours after the lumen
in each is defined, two minute calcareous bodies appear on the floor, usually towards
each extremity of the longer axis of the otocyst (oto, Pl. VI. fig. 5; Pl. XII. figs. 1-5).
These otoliths have the appearance of two very small dense grains, and are, as Dr
CARPENTER remarks (No. 37), similar in character and mode of formation to the concre-
tionary spheroids common in the urine of the horse, the integument of the shrimp, and
other forms. It is well known that when a solution of lime-salt in gum-arabic is slowly
decomposed, carbonate of lime is deposited in spheroidal concretions. Sometimes, as Mr
Raney found, two of these will unite in dumb-bell form, and occasionally a number will
unite in the form of a mulberry (No. 126, p. 19).* The walls of each otocyst are com-
posed of columnar or rather spindle-shaped cells, and at first over much of their surface
several layers are superposed (Pl. VI. figs. 3, 4). Subsequent changes, however, not
only affect the thickness of the walls, and cause them to thin out, but alter their contour.
Moreover, being pressed in, from above, anteriorly, the otocyst (aw) when viewed from
the side, loses its angular elliptical shape, and has more or less the outline of an oyster-
shell (Pl. VIII. figs. 4, 6, 8, 9; also Pl. XII. figs. 1-4, 7). A ridge also appears on the
floor, caused apparently by some of the internal nervous tissue being aggregated along
the shorter axis of the capsule (PI. VIII. fig. 8). In Hsoxv, about the time the cardiac
chamber is formed, and the embryo rises erect upon the yolk, the otocysts, according
to LEREBOULLET, become more transparent, and have a thick investment like cartilage
(No, 93, p. 529). No such investment appears in our forms until very much later, the
walls retaining their original cellular structure (Pl. VI. figs. 3, 4), though at certain
points they become thickened, sensory cushions (new) being formed of large fusiform
cells, which take a slightly radial disposition. An embryo of 7. gurnardus, six days
after hatching, shows three such nervous aggregations provided with erect motionless
cilia or palpocils. That situated upon the floor is by far the largest, but it may vary
somewhat in outline as well as position. The remaining two are anterior and posterior
(Pl. VI. fig. 2). In one specimen, viz., the example figured, a dorsal hernia (x) or
process of the cellular wall occurred. A long trumpet-shaped tunnel (can) passed
anteriorly and superiorly, the inner end being faintly granular and botryoidal in appear-
ance from the irregularity of its cells. In some forms the ears become so enormously
developed that they may nearly meet in the middle dorsal line, or may, as PARKER
describes in Salmo, actually overlap the posterior border of the eyes (No. 117, p. 113).
In the gunnel (aw, Pl. XIII. figs. 5-7) they are certainly very much larger at a com-
paratively early stage than in any other form reared at St Andrews, and they may
* A still more striking example of definite concretions in a clear fluid is that afforded by certain Anuelids, ¢.,
the stylets of the Nemerteans. LerEBoUuLLET proved their calcareous nature in fishes; he says—* Treated with acid,
they effervesce and disappear. No membrane is left, or it is too thin to distinguish” (No. 93, p. 633).
VOL, XXXV. PART III. (NO. 19). 6E
762 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
be larger and more rapidly developed in the embryos of demersal ova than in pelagic
forms, though in the clupeoids with both demersal and pelagic ova the spacious nature
of the otocysts is a characteristic feature.
It is difficult to follow the changes in the structure of the ear in the transparent
living fish, on account of its complexity. The semicircular canals seem to be developed
primarily from thickenings of the cellular lining of the auditory sac, like the nervous
cushions, a soft hernia being produced which grows inward as an increasing ridge, in
which a cavity is formed, as shown in PI. VI. fig. 10, can. Viewed from the side, at
a later stage the semicircular canals protrude into the chamber of the otocyst as three
short knobbed processes directed inward from the margin. The median and inferior
canals end abruptly in the middle of the chamber. Frequently the otoliths, instead of
lying apart, each in a depression of the auditory floor, may shift, so as to lie towards the
same part of the otocyst, e.g., in the anterior depression, as in Pl. VI. fig. 7, and Pl. XII.
fig. 7. At times three otoliths occur, and when two are present, as is normally the
case, there is usually a marked disparity in size, LeresouLLer remarking that in
Perca fluviatilis the posterior otolith acquires a diameter triple that of the anterior
(No. 93, p. 632).
In preparations very deeply stained with hematoxylin-the otoliths not only show the
usual glistening crystalline structure with radial striations (ote, Pl. VI. figs. 2, 3, 4, 9),
but less numerous concentric striations, and a very marked dark central core surrounded
by an external stratum, which stains more faintly (PI. VI. fig. 11).
A further stage in the development of the Teleostean ear is observed in the young
flounder (Pl. XV. fig. 8), in which the disparity of the otoliths and the complex
condition of the auditory chamber are well shown.
Olfactory Nerves and Pits.—The olfactory pits are distinguishable on the sixth day
or later, z.e., about the time that the heart’s pulsations commence. They are produced
by a paired thickening of the sensory epiblast (ep*, Pl. IV. fig. 17) in front of the upper
part of the hemispheres. Each soon forms a flattened oval sac of slightly elongated cells
(ol, Pl. IV. fig. 2), beyond which a small portion of the fore-brain (fb) extends (Pl. IV.
fig. 1). A depression commences from the outside, and each nasal sac becomes a cup-
like structure, whose cells are now fusiform and radially arranged (o/, Pl. IV. fig. 17).
The flattened corneous layer is no longer present at the two points where the pits are
formed, and as they become deeper and the walls of each sac increase in thickness, they
may be brought into close contact with the anterior fore-brain, upon whose front they
seem to lie in the living embryo (Pl. VI. figs. 6, 7, 8, 10; see also Pl. XII. figs. 1, 3,
7, and Pl. XIII. figs. 1, 3, 5, 6, 7). So small is the space at this time separating
the sacs from the brain that it is difficult to detect the nerve-strand which connects
them. Horrman, however, made out the origin of the olfactory nerves as minute pro-
liferations of the wall of the anterior fore-brain (No. 69, p. 87). This minute outgrowth,
on reaching the nasal sac, coalesces with the proximal surface of the nasal pit. No olfactory
lobes are at this time discernible ; indeed, MarsHatt doubts whether in the Teleosteans
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 763
(Salmonoids) he examined true olfactory lobes ever are formed. At any rate, he cannot
regard them, and justifiably so, as embryonic structures (No. 100, p. 313). The proximity
of the olfactory pits and the brain renders the determination of such a point in the
minute Teleostean forms here considered very difficult; but MarsHa.t’s conclusions
admit of little question. In the Elasmobranch-embryo the olfactory lobes are not
distinguished until almost all the features of the adult are attained (BALrour’s stage O)
(No. 100, vide pl. xiv. figs. 24, 33, 34), and in the chick they cannot be made out
until the seventh day (No. 17, p. 162). There is no trace of these lobes in Rana during
the earlier stages, according to MarsHALt, and the nerve-strand passing to the olfactory
pit is very short.
A similar condition is found in Teleosteans ; a solid strand of cells passes from the
roof of the fore-brain, before it shows any trace of external division, to the pits (ol,
Pl. IV. fig. 16), and these latter as they increase in bulk approach, as in Pl. IV.
fic. 17, and come into such close proximity to the fore-brain (fb) that an actual
reduction in length of the primitive nerve results, so that it is barely distinguishable
(Pl. VI. fig. 6). The histological character of these primary olfactory strands supports
the view that they are merely diverticula from the brain, in which organ no fibres are
yet formed, for the first pair of nerves have a similar solid cellular structure. This
structure MarsHaLu found to be retained, when the other cranial nerves had assumed
the fibrillar character. It is remarkable that the olfactory nerves, which are amongst
the earliest to be given off, retain their primitive structure longest. MarsHa.i could
not make out any ganglionic enlargement (No. 100, p. 312); but Bearp in some later
researches found that, as in Rana, a ganglion does arise in connection with the epiblastic
thickening forming the pit, and that the olfactory nerve itself is also split off from
the skin (vide his figs. of Rana and Rhodeus amarus, figs. 3 and 4, pl. viii. No. 22).
The dorsal position of the nasal pits is interesting, as in the Elasmobranchii and Aves
these structures are on the under side of the head. The nerves shift down from their
first position, and are found to connect with the fore-brain ventrally (1, Pl. XXIV.
fiz. 4; also vide Marsuaut, No. 100, pl. xiv. fig. 33). Of course in the Teleosteans this
transference is much reduced, as the fore-brain does not grow so extensively as the hinder
portions of the brain; but MarsHatt has undoubtedly given accurately the facts of
the early development of the first pair of nerves, which, however, HuxLry considered
to be developed late, and to have but one paired connection with the brain, and that a
ventral connection (No. 74, p. 71). This ventral origin is secondary, and comparatively
late, but it is very much later before the basal swellings known as the olfactory lobes
are clearly indicated (Pl. XXIV. fig. 4).
In the early forms treated of in this section the division of the original single nasal
opening into two was not followed. It is readily observed in the wolf-fish (Anarrhichas) *
and in the young flounder (Pl. XV. fig. 8).
Optic Nerves and Vesicles.—One of the earliest features in the development of the
* Vide section xiii. p. 254.
764 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
Teleostean embryo, as already noted, is the enormous development of the anterior
cephalic region, which is chiefly due to the protrusion of two rounded lateral masses from
the sides of the narrow fore-brain (Pl. V. fig. 1, op), and not, as LEREBOULLET stated,
from the walls of the mid-brain (No. 93, p. 522). The pair of massive bulbs thus
formed are rapidly defined as the ellipsoidal optic vesicles, the first of the sensory
organs to appear. In section (PI. IV. fig. 16) the cells of the neurochord, at a point
midway between the dorsal and the ventral surface, actively push their way outward,
and pass for the most part upward, so that a pair of stalked vesicles are formed, lying
against the sides of the fore-brain—not quite upright, but placed at an angle which
brings the lower and smaller lobe in proximity, while the upper and much larger lobe is
pushed away from the brain (Pl. IV. fig. 3). Sections clearly demonstrate the abundant
protrusion of cells to form the optic bulbs, which Kryestey and Conn regard as formed
in the main by a constriction or fissure commencing above and behind the lateral
enlargement, and progressing forward and downward (No. 78, p. 207), but the constriction
which they carefully describe is preceded by a very apparent bulbous outgrowth. These
protruded cells are indistinguishable in size or contour from the neurochordal cells which
gave them origin, but the outer limiting layer of cells assumes a columnar disposition, as
also does a double plate of cells along the median dorso-ventral plane. This latter feature
has been referred to (No. 122, p. 452) as a radial disposition of the central cells and
“as though about to dehisce along a central vertical plane in order to form a median
chamber, longitudinally placed ;” but a chamber converting the solid optic proliferations
into capacious hollow vesicles, such as the early condition of these structures is generally
described, is never completed—a very narrow fissure being all that is usually formed, and
even this may at times fail to be developed before the invagination of epiblast presses
the outer layer against the inner layer of the primitive optic vesicle. RypbrEr describes
and figures the narrow fissure referred to (No, 141, p. 499, pl. v. figs. 26, 27); and
in section (Pl. IV. fig. 17) it is plainly seen asa slit in the midst of the optic vesicle.
This separation of the median cells is interesting, for, though the Teleostean eye is not
pushed out as a chambered sac from a hollow brain-vesicle, as is the primitive mode of
origin, it secondarily acquires a trace of this vesicular condition. In the living embryo
it rarely presents more than the character of a delicate median line or slit in the optic
bulb (PL. V. fig. 1). Pl. IV. fig. 3, shows the first indication of this slit-like lumen,
which can be traced along the short thick stalk into the fore-brain, where it is lost. In
horizontal section we see that while the cells—pushed out to form the optie vesicle—in the
main pass upward, they also extend posteriorly, carrying the vesicle some distance behind
its pedicel or point of origin: the optic vesicles on their appearance are thus defined
most distinctly behind. Each vesicle, in fact, forms a depressed pyriform body,
which by its smaller end remains attached to the brain, while the swollen upper
portion extends dorsally, backward and distally (Pl. IV. fig. 16). ScHenx, who first
gave a full account in his well-known researches on the eye of fishes (No. 143), seems
not to have recognised the fact that the eye and the entire central nervous system in
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 765
these forms is primarily solid and without a lumen. Kuprrer appears to have been the
first to describe the true condition (No. 88).
It is important to notice that the nerves—that is, the stalks of the optic vesicles—arise
at a different level from the olfactory and other nerves, a fact inconsistent with the
derivation of the nerves from a ridge or “ sinnesplate,” such as GOrre and others
distinguish, A dorsal stratum of neurochordal cells may perhaps be regarded as a
neural crest from which the posterior nerves spring, but such a crest does not pass
further forward than the hind-brain ; the first and second pair of cranial nerves, as will be
seen, arise, the one primarily as dorsal and the other as lateral median evaginations of the
prosencephalon. In pushing backward the optic vesicles shut off a thin stratum probably
of mesoblast which later forms an enveloping cup, and gives origin to some important
structures in the developing eye. This mesoblast (mes, Pl. IV. fig. 17) is probably a
forward growth from the thin plate of the same layer in the otocystic region (Pl. IV.
figs. 16, 17). Meanwhile, the short, thick connecting stalk becomes constricted, and
the vesicle itself alters both in form and position. Viewed from the side, the latter
is now almost perfectly elliptical (op., Pl. XXII. fig. 12), and is nearly perpendicular in
position, z.e., parallel to the vertical axial plane of the embryo (Pl. V. figs. 3, 10).
The columnar cells along the central vertical plane of each vesicle (Pl. IV. fig. 3)
separate sufficiently to mark a slight but distinct fissure (Pl. IV. fig. 17; Pl. V.
fig. 1). This fissure persists when the optic vesicles have altered their position, so that they
lean by their upper portion against the neurochord, and this median chamber, instead of
passing upward, outward, and posteriorly, as when first indicated (PI. V. fig. 1), now
passes downward and outward (op, Pl. IV. fig. 14). As already indicated, the pyriform
outline is almost wholly lost, the optic vesicles lying obliquely against the fore and mid-
brain—as elliptical bodies laterally flattened, and traversed by a vertical lumen longi-
tudinally separating each into an inner and an outer half, the latter layer being very
much thicker than the inner half (PI. IV. fig. 17). This condition does not remain long.
Before the end of the day these “ primitive optic vesicles ” become indented by the pressure
of the epiblast lying external to them, the deeper layer of which becomes rapidly thickened
so as to form in section (PI. IV. fig. 17) an almond-shaped mass on each side, pressing upon
the central region of each optic vesicle (op), which gradually becomes cup-shaped, the hollow
of the eup being occupied by the thickened mass of epiblast, which forms a dense spherical
body, the lens (/, Pl. IV. fig. 14). The optic cup or secondary optic vesicle becomes thinner
marginally, and this portion creeps round to the outer side of the lens (Pl. 1V. fig. 21),
forming a circular lip around it, which is incomplete on the lower side. This gap, the
choroidal fissure, is very distinctly seen at this stage (ch, Pl. VUI. figs. 6, 7, 8; Pl.
IX. figs. 1, 3; Pl. XII. figs. 1, 2), and it persists for some time (Pl. XVI. fig. 1).
The mesoblastic cells, which were included as a thin plate between the optic
vesicle and the brain (mes, Pl. IV. fig. 17), have spread over the former as an outer
layer (Pl. IV. fig. 21), and pushed their way through the choroidal fissure into the
interior chamber of the eye, as is seen in section (Pl. IV. fig. 20). A similar horizontal
766 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
section, at a lower plane (PI. IV. fig. 19), shows the fissure disappearing. These intruding
mesoblastic cells (mes) appear to become packed between the lens and the retinal surface
of the optic cup, and doubtless break down to constitute the vitreous humour of the adult
eye, forming also, as some observers think, the “capsula hyaloidea,” in which a rich
vascular network afterwards develops. The differentiation of the cellular optic vesicle
into its various layers has already taken place before the embryo has emerged from the
ovum. The formation of these layers can, however, only be very briefly touched upon.*
We have seen that the eye, soon after its appearance as a solid bulbous protrusion
(op, Pl. IV. fig. 16), separates by a slight fissure into two layers, constituting the primary
vesicle (Pl. IV. fig. 17). With the obliteration of the lumen, the two layers become
closely apposed, and the eye consists of a thick-walled cup of undifferentiated cells
(Pl. IV. figs. 14, 21), whose chamber—the lumen of the secondary vesicle—is closed
in front by the growing lens (/). An investing layer of mesoblast (mes) forms the
sclerotico-choroidal sheath, absent, however, from the front of the eye. As the time for
extrusion approaches, scattered pigment-spots occur outside the optic vesicle and in the
external investment. These spots are unbranched amorphous particles, sparsely
distributed as an irregular pigment-layer over the whole surface of the optic cup, save
in front of the aperture of the pupil (Pl. XIV. fig. 1; Pl. XVII. fig. 10). On each
side of the lens they are densely aggregated (Pl. V. fig. 6; Pl. XVI. fig. 8). The
outermost layer of the cellular vesicle, 7.e., the stratum of cells internal to the layer of
pigment, assumes a marked columnar character (Pl. XI. figs. 6—8)—bold striz passing
across it, and dividing it into wedge-shaped radiate masses as indicated in P]. XXIIL fig. 3a.
At the same time the cells within, constituting the main bulk of the vesicle, separate,
though somewhat obscurely, into two layers of great and almost equal thickness—the inner
layer being slightly thicker (in section) than the outer. The line of separation is delicate
and indistinct at first, but subsequently develops into a fine molecular band—the prominent
internal molecular layer. The inner surface of the columnar stratum shows a delicate
membrane, possibly the posterior or membrana limitans externa (“limitans interna” of
Horrman, No. 69, p. 50).t From the outer stratum consisting of columnar elements
the rods and cones are developed, while the two thick inner layers with their intervening
lamina give rise to the other layers of the retina. Such is the condition of the six
layers of the retina shortly before the time of hatching in pelagic forms, e.g., the cod and the
haddock. In other forms, chiefly demersal, which reach a somewhat advanced embryonic
stage while within the ovum, the eye attains a much further degree of development.
A haddock, on the second or third day after extrusion, shows additional changes, the
second layer being better marked, as is also the inner molecular layer, though both
are still very thin amine. The columnar character of the bacillar stratum is still more
ce
* The minute description of the development of the Teleostean eye is in the able hands of Dr Marcus Gunn, one
of the surgeons at Moorfields.
+ This layer Dr Gunw has identified as the “external molecular layer”—a “thin dark finely granular line ;”
and should this be so, then the “imitans externa” must be developed at a much later stage, as Dr Gunn states.— Vide
Ann. Nat. Hist., Sept. 1888, p. 268,
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 767
distinct. During the first week after hatching, the internal molecular layer undergoes
great development, and rapidly becomes a thick and bold stratum separating the external
granular layer from the internal granular layer. The external molecular stratum is
slowly differentiated on the inner surface of the columnar layer, while the inner
granular layer shows, though very obscurely, a separation into an inner and an outer
portion. The pigment of the choroid is much more abundant than before, and in the
living embryo gives to the eyes a dense appearance, so that the minute transparent
fish can usually be discerned in the tanks of the laboratory by the two large dark eyes,
which form a most prominent feature (Pl. XVI. figs. 3, 6,7,* 9; Pl. XVIIL. figs. 1,2). The
structure of the retina exhibits little further change during the later larval stages, but in
the post-larval conditions other features appear, which need not, be noticed in detail by
us, as Dr Marcus Gunn has specially occupied himself with this subject. Thus in a
young flounder, still transparent and colourless, the pigment-layer is greatly increased in
thickness, and it sends prolongations into the bacillary layer. The cylindrical rods
form a very distinct stratum, while the flask-shaped cones are well defined, and present
a contrast to the corresponding layer in Amphibians, which have a very insignificant
stratum of cones. Indeed, as Max ScuuLrze pointed out, this layer in Teleosteans recalls
the condition in the Mammalian retina (No. 144, wide sect. iv. of his paper). The
double disposition (twin-cones) in the adult eye of osseous fishes has not yet been
assumed, so far as can be made out. The striking coloured globules so prominently seen
in this layer in Batrachians, birds, and some reptiles are absent, nor do they at any
subsequent stage appear to be developed. That Teleosteans should have a layer of rods
and cones so early and so well developed, whereas in Selachians (and cartilaginous fishes
generally, it is said) no cones can be made out, is a remarkable circumstance. Bats,
hedgehogs, and other nocturnal forms amongst Mammals, are destitute of cones.
The limitans externa in the post-larval stages is a very delicate lamina; but it is
well defined. The external granular stratum now consists of several layers of large
cells separated from the inner granular layer by a comparatively broad external mole-
cular layer.
The inner granular layer itself Horrman separates into three portions
stratum of “tangentiale Fulcrumzellen,” a ‘‘ medialer Theil der inneren K6rnerschicht,”
and a “lateraler Theil” of the same layer. In the flounder, as well as in such forms as
Cottus and Cyclopterus, only the outer “tangential” cells can be distinguished from the
remaining elements of the inner granular layer, which form a very thick band. Internal
to the last-named layer is the internal molecular stratum, anterior to which the
ganglionic layer can be distinguished. The internal molecular layer HuLKE describes as
including a large quantity of connective tissue, in the midst of the fibres of which are
large branched corpuscles of very considerable dimensions (No. 71, p. 247), but in com-
paratively late post-larval stages no trace of these structures can be made out. The
an outer thin
* Mr Cunnincuan’s figure (op. cit., pl. vi. fig. 4) appears to be, as he supposes, this species, viz., Liparis
Montagut.
768 PROFESSOR W. C. M'INTOSH AND MR E. E. PRINCE ON
ganglionic layer is composed of large cells, which form a remarkably broad layer—quite
unlike the narrow ganglionic stratum in the Salmonide. Anteriorly it is defined by the
fibres of the optic nerve, and the limitans interna (Horrman’s “limitans externa”) or
anterior limiting membrane, which forms the lining of the optic globe. Some observers
look upon this membrane as the hyaloid capsule of the vitreous humour; HUvLKE,
however, regards it as a separate membrane, and such it would appear to be, since it
precedes the formation of the vitreous fluid by a long interval (wide No. 71, p. 248).
An anterior annulus, the lip of the secondary optic vesicle or cup, remains unaffected
by these histological changes, and a mass of indifferent cells fills up the interspace between
the retina proper and the circular curtain—the extension of the choroid in front of the
eye. ‘These cells are in fact involved in the formation of the iris and ciliary ridges, the
ciliary muscles being developed from the mesoblast (mes) entering by the choroidal fissure
(Pl. IV. figs. 19, 20). Even in the later larval stages this complex anterior annulus,
formed of the cells just mentioned, and the pigmented choroid which grows round to
enclose a circular opening in front of the eye—the pupil, constitutes a brilliantly
opalescent iris, which adds to the remarkable appearance of the minute transparent
larva (Pl. XVI. figs. 3, 7,9; Pl. XVIII. fig. 11).
Cranial Nerves.—The optic, olfactory, and auditory nerves are treated elsewhere, and
in this place only the larger and more important nerve-origins will be referred to, the
Teleostean embryo being little favourable for tracing the development of the smaller
cranial nerves, such as III., IV., and VI. The trigeminal (V.) is large, and readily made
out. In Elasmobranchs it arises as two lateral outgrowths from a median dorsal ridge at
the anterior end of the hind-brain. Ata late embryonic stage this nerve springs from
the upper lateral margin of the hind-brain, but so far forward that the optic lobe covers
it at this point, and it appears to emerge from the overlapping lobes at a point imme-
diately posterior to the eyes. This lateral position must be secondary (as MarsHALL
suggests in the case of Scyllium), the original median dorsal position being altered by the
rapid growth of the roof of the brain, so that the origins of this pair of nerves become
further and further separated, until finally they are lateral (No. 101). Just as the
nerve emerges it separates into several rami, the outermost being the maxillo-palatine
branch, while a second large branch, the mandibular, passes backward a short distance in
close contact with the side of the medulla oblongata. Each of these main rami shows, near
its origin, a very large ganglion, the two ganglia being so close together as to appear
like slightly separated moieties of one primary ganglionic swelling. From the ganglion of
the maxillary nerve a small nervous branch passes forward over the orbital arch, possibly
the abducens (VI.), though more probably it is the ramus ophthalmicus of the VIth nerve.
Between the two main rami just mentioned a large blood-vessel passes, and a third
ganglion appears beneath it, also apparently one of the trigeminal group, while a slender
nerve, whose destination could not be made out, was connected with this smaller ganglion.
A little posterior to the trigeminal the VIIth and VIIIth arise in close proximity to each
other, the auditory being posterior and exhibiting a large ganglion.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 769
It is difficult to follow the fibres of two nerves, so contiguous, to their centres in the
brain; but fibres can be traced from the upper lateral edge of the medulla over
a wide curve which brings them near the base of the third ventricle, or more correctly
above the pyramids ; these must belong to the facialis ; and the auditory (VIII.) consists of
those fibres which come out close to the surface of the medulla just below the overlapping
posterior part of the optic lobe. These two nerves, in regard to their nuclei, thus are
widely separated ; but where they arise from their common site on the upper margin of
the medulla they are separable only by the fact that the fibres of the facialis pass down to
the mandible and posterior margin of the hymandibular cartilage ; while the VIIIth nerve
has a very short course, breaking up on the under surface of the auditory sac to supply
at least three special sensory areas (neu, Pl. VI. figs. 3, 4, 9, 10) in the otocystie chamber,
and forming a prominent ganglion outside the ear before doing so. Of the glosso-
pharyngeal nothing can be said here, but the vagus (X.) apparently arises by two complex
roots ; the first, which probably includes the fibres of the IXth nerve, issuing from a point
near the lateral summit of the medulla oblongata, which point is in the same transverse
plane as the oral termination of the notochord. It passes along the side of the medulla
and penetrates the auditory cartilage, sending twigs apparently to the four gill-arches and
to the pharynx. The nucleus of this portion of the vagus is confined to the superficial
swelling of the lateral ridge of the medulla. Not so with the second part of the vagus.
Its fibres describe an arch or curve, and can be traced to the median region of the medulla
below the floor of the fourth ventricle and above the pyramids, while part of its fibres have
a more superficial origin. On emerging they form a very massive, prominent root, passing
in the main through the hind part of the ear-capsule, just above the thick basilar plate
where it is in contact with the otocyst, and forming in front of the pectoral girdle a large
double ganglion below and to some extent internal to the ear. The section which shows
this bifid ganglionic mass presents another ganglion, apparently the ganglion of the first
part of the complex. This ganglion is smaller, somewhat higher, and posterior to the
large double ganglion. The former lies on the inner side of the anterior cardinal trunk,
below which is a slender ganglion, whence twigs can be traced to the opercular region and
to the skin, forming, between the muscle-plates and the neurodermis, a nervous tract,
probably the origin of the lateral line.
The large double ganglion first named lies just above and external to the pronephric
swelling, the intimate relation of the two structures being noteworthy. Its fibres go,
as before said, to the pharynx and the branchial arches, From the smaller ganglion,
described above, pharyngeal and important cardiac branches also pass.
Lateral Sense-Organs.—Little can be added to the observations of Horrman (No. 69)
with reference to the development of the lateral sense-organs. In a young gurnard,
about eight days old, they are very distinctly seen in the transparent though somewhat
corrugated and glandular integument. Generally three or four can be made out in the
haddock, one on the top of the head, just behind the eyes, a second situated a short distance
behind the pectoral fin (see Pl. XVII. fig. 1), while one or two occur along the caudal trunk,
VOL. XXXV. PART III, (NO. 19). 6F
770 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
They are not, however, regularly arranged, and the distal enlargement protruding from
the integument is often absent. Thus, in the gurnard above referred to, nerve-filaments
were observed passing across the sub-epidermal space from the trunk, and terminating in
the skin without an enlarged sensory-organ. The external sensory-organ (Pl. VI. figs.
8, 8a) consists of a somewhat elliptical aggregation of granular columnar cells, from which
a number of very fine and apparently rigidly erect palpocils (plp) project. A delicate
nerve-filament (nv) passes from it to the muscular plates (my), and so to the central
nervous system. This filament shows a slight enlargement at its proximal end, and
another dilatation just as it approaches the external sensory-organ.
As noted on a previous page, large spaces (ss) filled with a clear plasma exist below
the integument (ep), separating it widely from the trunk (Pl. XV. fig. 7), and across
these spaces in more advanced embryos fine nervous threads pass from the myotomes to
the skin, occasionally giving off in their course delicate secondary filaments. The nerve
going to the cephalic sensory-organ apparently comes from a cutaneous sensory branch;
and Horrman states (No. 69) that the development of the ramus lateralis nervi vagi
always precedes the appearance of these sensory-organs.
No sections of the early stages show the longitudinal sensory tract called the “ lateral
line” in fishes. There is, however, in the caudal trunk of an advanced haddock a canal
apparently surrounded by nervous cells and mucous tissue which stains deeply (Pl. XI.
fig. 16), but it can only be traced a short distance in the tail of the example referred to.
As noticed elsewhere, the facial region is provided with numerous papilliform sensory
bodies, and these are large and very noticeable in what may be called the maxillary or
sub-prosencephalic region. They exhibit a structure similar to the lateral sensory-organs,
and are composed of lengthened spindle-shaped cells (Pl. XXI. fig. 7, sb).
Alimentary Canal.—In its earliest condition the alimentary tract consists merely of
a thickened sub-embryonic layer of hypoblast, intervening between the neurochord above
and the yolk, or rather periblastic cortex of the yolk, below. Posteriorly, when little
more than one-third of the yolk is covered by the blastoderm, the hypoblastic cells
beneath the embryonic axis, as already pointed out, assume a distinct columnar character
(hy); a lumen (hg) appears below, which is arched over by columnar hypoblast, and
has a floor of nucleated periblast (per, Pl. IV. figs. 5b, 6). This is the first indication of
the alimentary tube, and it forms the posterior section—the continuity of which with the
neurenteric canal and medullary groove has been already described. From the arched
enteric roof the notochord is differentiated. The lumen at first extends but a very
short distance forward, and is lost in an anterior aggregation of hypoblastic cells. These
cells, formed by the proliferation of the thin sheet of invaginated hypoblast, reach as
far as the cardiac region, where they thin out rapidly, and form a delicate limiting
membrane below the head (hy, Pl. IV. figs. 3, 4). As this thickened mesenteric mass
arises, the embryo is necessarily raised from the yolk except in the cephalic region—
the snout still lying in close contact with the yolk below, so that a pseudo-cranial
flexure is produced, and a pericardial space (pd) formed beneath the otocystic region
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. tis
At the sides of this space, 7.e., beneath the eyes, the hypoblast becomes thickened
as two lateral longitudinal ridges (PI. IX. fig. 1; Pl. XI. fig. 1), but elsewhere in this
region the layer forms a very thin plate (Pl. IV. fig. 21). That the roof of the primi-
tive enteron is thus formed as a dorsal sheet of invaginated hypoblast, admits of no
doubt. Such sections as figs. 5b, 6, and 10, Pl. IV., demonstrate this, and the ventral
wall of the canal is formed of cells either pushed in from the side—that is, formed of true
hypoblastie cells or aggregated as masses of protoplasm around the scattered nuclei of the
periblast, and budded off. While the posterior portion is formed in this way, the mesen-
teron proper appears to develop in a different manner, being formed by a multiplication
of the invaginated (hypoblastic) cells ; and a ventral and a dorsal wall are not definitely
formed from periblastic and hypoblastic cells respectively, but doubtless periblastic cells
contribute in some degree to build up this portion of the tract also, though in such
sections as figs. 13 and 14, Pl. IV., the hypoblast (hy) is a very definite and continuous
layer. The mid and fore portions form a dense cord, in which a lumen appears later by
the forward extension of the posterior enteric chamber, this cesophageal slit extending in the
ling, two days old, in front of the otocystic region. At first the hind gut is open to the
yolk below (as in Pl. IV. figs. 5b, 6), but no sections show this to be true of the enteric
tract further forward. According to Horrmay, paired involutions of hypoblast produce
the tract which he thus holds to be open to the yolk beneath (vide No. 69a, Taf. i. fig. 3),
but no section in pelagic forms indicates such a mode of origin of the mesenteron, and
certainly not of its cesophageal portion. The earliest condition of the alimentary tract is
a continuous sheet of hypoblast, thickened on each side in the oral region to form the
lateral walls of the oral chamber. Lrresou.er regards the alimentary canal as developed
by a folding-in of the “ mucous layer,” though the pharyngeal section, he holds, is not
formed till later. In his earlier researches he states that the enteric tract is possibly
formed by “une végétation celluleuse,” such as Voor had described as involved in the
formation, not only of the intestinal tube, but of the liver and kidneys (No. 93, p. 538).
Dourn believes that the oral hypoblast is a forward growth of the mesenteric mass, nor
is there evidence to show that this is not so. At any rate, in the embryo whose optie
vesicles are in process of formation, the hypoblast (hy, Pl. IV. figs. 4, 13, 14, 20) is a thin
sheet—a single layer of cells for the most part over the entire ventral surface, save at the
posterior extremity (hy, Pl. IV. fig. 10). At a somewhat later date, when the invagina-
tion of the lenses is completed, the mesenteron is a massive cylinder, and the oral tract a
wide flattened sheet of hypoblast formed either by proliferation of the invaginated layer,
or by forward growth of the denser hind gut, probably a combination of both. In any
case, LEREBOULLET'S view is the correct one, viz., that the pharynx is a separate and later
formation than the mesenteron proper. By the time the walls of the otocysts have
thinned out and their chamber has enlarged and contains the otoliths, a fine horizontal
fissure traverses the pharynx, and a lumen thus continues from the oral to the blind anal
end of the alimentary canal (PI. IV. fig. 11). The cells now assume the full cubical
columnar character characteristic of the enteric epithelium, and, at first a single layer
772 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
(PL. IV. figs. 11, 19), they increase until the enteric walls are thick, and include many
layers of wedge-shaped cells (PI. VII. figs. 7, 9). In P. flesus of the ninth day (z.e., two
days before hatching) the walls are just ‘001 inch in thickness, and the lumen in the
middle or widest part measures in horizontal breadth slightly less. A delicate inner layer
lines the lumen, which has a granular or mucoid appearance, but it subsequently forms a
ciliated enteric lining. It is not more than ‘000125 inch in thickness. The lumen of
the mid gut is large and round in transverse section (mg, Pl. VII. fig. 3), but much more
depressed further forward. A section through the pectoral region, where the enteron is
oval and the lumen a wide transverse fissure, shows a diminished dorso-ventral capacity,
while in the oral region proper a mere horizontal slit extends from side to side of the
wide and very much depressed layer of cesophageal hypoblast (Pl. XL. figs. 2-8). The
tract is thus a closed sac (Pl. IV. fig. 12), flattened anteriorly, round and cylindrical poste-
riorly, the mouth and anus being “ the last parts,” as LereBouLLEr said, “ to be formed.”
Around this tube of hypoblastic cells the splanchnopleure (sp) grows, forming a thin
external sheet which pushes in below the notochord, and cuts off that structure from the
mesenteron (PI. VII. fig. 6). These mesoblastic cells do not become a fibrous layer for
some time, but later they give origin to the muscles of the canal and its connective-tissue,
while externally they give rise to the epithelial peritoneal layer.
In the cesophageal region the course of the hypoblastic cells is extremely difficult to
follow. They give origin to a cardiac swelling which is sub-oral and median (Hr, Pl. IV.
fig. 13; Pl. V. fig. 8), while other cells pass into the hypoblast laterally to form the
core of the visceral folds. During the first few days after hatching the anus is still
undifferentiated, as LEREBOULLET found to be the case in Perca; nor is the oral cavity
externally open, as the same observer also proved in Perca by experiments with various
colouring matters (e.g., indigo), the alimentary tract being in fact a closed cylinder, con-
sisting of a very thick inner wall of cylindrical cells (hy, Pl. IV. fig. 11), whose free
rounded ends project into the cavity of the gut (fy), and externally of a thin layer of
flattened mesoblastic cells (sp) not yet transformed into muscular and other tissues (vide
No. 93, p. 625).
Many preparations show a lining apparently of cilia,* and there is thus great probability
that the enteric tract—the cesophageal portion at least—of young Teleosteans is ciliated.
Its walls for some time are straight and smooth, but in later stages folds and wrinkles are
formed, the intestine especially showing a complexly folded internal surface (Pl. XIV. fig. 5;
Pl. XVIII figs. 1, 11). The various parts of the tract become rudely marked during the
first week after hatching. Thus a gurnard on the thirteenth day (Pl. VII. fig. 9) shows
very distinctly a capacious though depressed oral chamber, the floor of which is ridged by
the branchial bars and hyoidean framework, followed by a wide cesophagus (fg), the lumen
of which is so flattened as to be little more than a horizontal fissure in transverse section.
From this portion the duct of the swim-bladder passes (Pl. VII. fig. 4).+ The enlarged
* Suiprey has recently described the cesophagus in Petromyzon (47th day) as ciliated (No. 150, p. 351).
+ Vide the highly suggestive remarks of Prof. CLeLanp on Teleostean pneumatic ducts—Memoirs, dc., in
Anatomy, 1889, p. 170.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 773
stomach (st) follows, and beneath its thin walls the hepatic mass lies. A fourth portion
of the tract succeeds, viz., the pyloric section, the dense walls of which give origin to those
remarkable diverticula, the pyloric cosca. These seem to be merely blind evaginations, and
gradually assume a lanceolate form, as we find in young cod from } to 14 inch in length.
Ventrally a well-marked duct passes from the liver, viz., the ductus choledochus, with
several ramose biliary ducts. The intestinal walls are very dense, rapidly develop a glandu-
lar character, and have a narrow oval lumen (/wy) with local enlargements, especially in the
mid portion of the gut. Posteriorly it narrows again until the rectal region is reached,
where a cincture or valve occurs, behind which its capacity once more enlarges (see
also hg, fig. 8 on the same plate); it then bends downward, and narrows to form the small
anal aperture (@) opening upon a muscular papilla. A similar condition of the intestine
and rectum is seen in the figure of P. platessa (Pl. XIV. fig. 5). The rugose walls often
exhibit vermicular movements, which are, however, very irregular, and involve and pro-
duce great contortions in the alimentary tract ; thus a peristaltic motion may pass from
the mesenteron to the rectum, narrowing its capacity as though by an embracing cincture.
Mouth.—A. stomodzeum or involution of epiblast to form the mouth is never really
formed in pelagic Teleosteans.* The oral cavity is capacious, and the branchial frame-
work supporting its floor and sides is fairly advanced when a fine transverse fissure is
seen passing across the under surface of the head below the eyes (m, Pl. IX. fig. 2).
This fissure enlarges and lengthens, forming an almond-shaped opening (m, Pl. IX.
fig. 3) across the subcephalic membrane. This is the mouth, and it is formed as a slit by
the lumen of the buccal chamber bursting through. Its edges are jagged, and strands of
cellular tissue often pass across from one lip to the other one or two days after the oral
opening appears (Pl. IX. fig. 3), showing that it is an actual severance of a complete
epiblastic membrane. There is no indication of the double origin, the coalescence of two
lateral clefts which Dourn has described in Gobius, Belone, and Hippocampus (No. 52a) ;
but in the ling—the species illustrated in the figures just referred to, and in other forms
—this median transverse fissure suddenly appears, and in the course of two or three days
widens antero-posteriorly to form a large median tubular opening.t The lips do not
move, but the hyoid cartilages are flexible and mobile, and the floor of the mouth is thus
raised and depressed. The mandibular cartilages rapidly grow forward, and the oral
opening—at first ventral, transverse, and shark-like
adult Teleostean, the prolongation of the mandible not only bringing forward the aperture
of the mouth (Pl. XII. figs. 2, 6, 7), but proceeding so fast and to such a degree that the
floor actually extends beyond the snout, and the aperture now opens from above
(Pl. X. figs. 1, 2,3, 5, 5a). The suborbital curtains, which hang down like two mem-
branous flaps, diminish, and become denser on account of the development in their tissue
assumes the shape found in the
of maxillary bars, the chitinous character and form of which are elsewhere described.
* Parker describes a true stomodeum in the salmon, but probably his account of the ingrowth of epiblast to
form the mucous membrane of the mouth and fauces requires confirmation.
+ Dourn, on the contrary, describes the centre of the oral slit as still closed when the lateral portions have broken
through.
774 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
Anus.—The anus in the forms here described is not a proctodzeum, as it is not
produced by the ingrowth of the external epiblast, but is at first a lateral opening (see
Pl. VIL. figs. 12-15), which five or six days after hatching is formed by the protrusion
of the anal section of the alimentary canal. In Molva vulgaris, early on the second day
after emerging, the anal tract seems still to end blindly, being continued backward
nearly in a straight line, or in some cases sending down a terminal process at right angles
to the main axis of the canal. This terminal prolongation is carried down to the middle
of the marginal fin, and generally on the second or third day is found to break through
in a manner not unlike the oral opening. The rectum is thus a eapacious thick-walled
tube, sending out a narrow anal continuation consisting of a fine tube lined by a single
layer of cubical epithelium, and it passes through the thick tenacious plasma contained in
the space behind the urinary vesicle (Pl. VII. figs. 12, 13). This space is enclosed between
the two epiblastic lamellze of the caudal membrane, and the anal tube curves round and
opens laterally on the surface of the latter, some distance from the ventral margin.
Later the membrane below the aperture becomes absorbed, the rectum assumes thicker
walls (hg, Pl. VIL. figs. 8, 9), and the usual muscular rectal portion of the alimentary
canal is formed during the second week after emerging. The anus then opens in the
ventral middle line, as in the adult fish.
Liver.—Soon after the otocysts are formed the ventral wall of the mesenteron in its
fore part shows an enlargement— an ovoid dilatation just before and below the early
pectorals,” according to LerEBouLtLer (No. 93, p. 584), and his description holds to a
large degree for pelagic Teleosteans. Certainly the liver is a distinct outgrowth from
the ventral wall of the mesenteron. Horrman has expressed the view that the liver
originates from the yolk-periblast, and that the hepatic diverticulum is really a prolifera-
tion of ‘“ parablast entoderm” (No. 69a). Such sections as fig. 2, Pl. VIL, do not
support this view, for the periblast (per) is a distinct, granular layer beneath, and
separated by a delicate stratum of hypoblast (Ay) from the cells which build up the liver.
The liver, in fact, is largely a solid proliferation of the ventral wall of the mesenteron, and
is periblastic, or formed of “ parablast entoderm ” only in the degree that the ventral wall
of this region is periblastic, and this we have seen at this point to be at a minimum.
Into the early liver (/r, Pl. VII. fig. 5) a delicate canal (de) passes, a direct prolongation
of the enteric lumen, doubtless the ductus choledochus. LrreBouLLer noticed this
especially when the mesenteron dilated and contracted as it does in later embryonic
stages (No. 93, p. 593). In Perca, on the sixth day, the same observer describes
numerous ramifying fissures or prolongations from this delicate canal; and the gall-
bladder he regards also as a tubular outgrowth of the intestine. The hepatic pro-
liferation becomes bifid, a dorsal and a sinistral ventral lobe being distinguishable. The
liver also becomes divided into small lobuli (/7, Pl. VIL. figs. 1-3), in the midst of which
the spacious gall-bladder (gb) appears as a clear vesicle, limited by an epithelial wall
of a single layer of cells.
Swim-Bladder.—From the dorsal wall of the mesenteron (mg) the swim-bladder (sb)
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 77
Or
is given off as a very thick-walled diverticulum (PI. VII. fig. 5), which presses upwards
against the notochord, and remains connected for some time by a fine canal (Pl. VII.
figs. 2, 4). Before the embryonic period ends, however, the duct atrophies, all the forms
specially referred to being physoclistous.
Heart and Circulation.—The heart is developed at a very early stage—before the
cesophagus is formed—as a cylindrical structure (hr, Pl. IV. figs. 8, 12), in front of the
pectoral region, 2.¢e., between the otocysts and the optic vesicles. Soon after the alimentary
tract is defined, or, as WENCKEBACH expresses it (in the case of Belone), after the ventral
closure of the gut, and when about twenty-four proto-vertebre are marked off, the heart has
a vermiform shape, and is still solid. This solid condition LerEBouLEr described in Perca,
but in Sa/mo and other forms the heart is stated to appear in the form of a single or
double tube (vide Horrmay, No. 69a; Batrour, No. 11, p. 637). That the heart
develops as a single tube in the Gadoid and other forms here considered is not surprising.
When the heart arises as two tubes it appears to be connected, as BaLrour pointed out
(No. 15, vol. xi. p. 689), with the non-closure of the pharynx inferiorly, but in those
Teleosteans where the cesophageal cavity is formed later by a forward growth of the enteric
lumen, the solid tract is really closed below, and this is the condition correlated with an
unpaired cardiac rudiment. Its first indication in the living embryo is seen as a rounded
projection beneath the solid cesophagus bulging out towards the subjacent periblast.
It is a ventral outgrowth of that splanchnic mesoblast, which also forms the branchial
arches. LeEREBOULLET describes this cardiac swelling (on the seventh day in Perca) as
having its inferior portion, the auricle, resting directly on the yolk (No. 93, p. 584; vide
his pl. iii. fig. 13). It is a median unpaired projection, and carries down before it a
very thin layer of hypoblast. At times this delicate stratum of hypoblast cannot be
made out, and in P. platessa it would appear to be absent; nor can a layer of hypoblast
be distinguished over the rest of the surface of the yolk, though such a layer is readily
seen in other Pleuronectids, as well as in Gadoids (Pl. VIII. fig. 11). In all cases, however,
the continuity of the rudimentary heart and the “ branchial” mesoblast above is
maintained.* Horrman describes in Salmo two lateral folds of splanchnic mesoblast,
which pass down beneath the pharynx, and produce by a dorsal and a ventral union a
tubular heart (No. 69a; vide fig. 9, Taf. ii.). Before the tube is complete inferiorly, some
intruding cells of “ parablastic entoderm,” i.e., periblast, form the cardiac endothelium
(No. 69a, Taf. iii. fig. 6; Taf. iv. fig. 6). Such a process does not accord with the appear-
ance of the heart in the living condition, for in the embryonic cod, haddock, and others
no lumen is visible at first, as OELLACHER and Gorve also hold, and indeed after the lumen
is formed the endothelial lining is absent (vide surface-views, Pl. VIII. figs. 3, 7; and
* WENCKEBACH (op. cit., and Jour. Roy. Mier. Soc., February 1887) describes its first appearance as a band of meso-
dermic cells close behind the optic vesicle on the lower surface. They arise from the indifferent mesodermic cells of the
head which wander round the gut. The mass of cells splits to form a kind of pouch—the heart. The blood-vessels
have a similar mesodermic origin. The heart opens into the segmentation-cavity, and its lumen is nothing else than
part of the blastoce:l. The blood is mesodermic in origin, he avers, neither endoderm nor free periblast, i.2., nuclei,
having any share in its formation.
776 PROFESSOR W. C. MSINTOSH AND MR E. E. PRINCE ON
sections, Pl. XI. figs. 2, 3), indicating that the epithelioid layer is not formed in some
Teleosteans simultaneously with the formation of the cardiac tube, and favouring the
view that the heart becomes tubular by dehiscence of its median cells, or, as LEREBOULLET
says, the linear cavity is formed partly by separation of cells and partly by absorption
(No. 93, p. 551).* It seems probable that in different Teleosteans this organ has a
different structure primarily, and certainly at later stages the circulatory system diverges
in various species. Thus in the Gadoids, Pleuronectids, Trigla, and other pelagic forms,
no yolk-circulation is ever developed, whereas in most demersal forms a circulation upon
the surface of the yolk is a very striking feature, and may be said to a certain extent to
precede the heart’s aetion ; for Truman found in Esox that blood-corpuscles were formed
in patches in the cortex of the yolk, constituting the “ islands of blood-corpuscles” which
Genscn has described (No. 56), and that before the heart pulsates, blood actually moves
towards that organ, At the eighty-sixth hour TrumaN saw these moving corpuscles reach
the heart, but it was ten or twelve hours later before the organ exhibited any motion, and
even then no corpuscles passed into its cavity (No. 154, p. 191); so that the pulsations
are independent of any stimulus given by the presence of blood-corpuscles within its
chambers. Muscular twitchings, again, are often observed in the heart of the gurnard
before the proper pulsations begin. We have already seen that the cardiac chamber is
enlarged by the raising of the head of the embryo, and LEREBoULLET noticed that as this
took place in Perca the heart becomes detached from the head, its anterior end following
the retreat of the yolk, sinking slowly, while the hind end remains attached under the
embryo. While yet a simple tube, the heart is contractile, the early pulsations, which
commence usually one or two days after the heart is formed, being one of the most note-
worthy features in the developing embryo, though no hemal fluid can be made out.t At
first the pulsations are very slow and intermittent, the intervals between the contractions
being irregular. In an embryo, four days after fertilisation, the beats are more rapid and
regular, averaging 48 pulsations per minute, while the rate at times is greatly increased.
Thus Dr Truman found in sow, soon after the heart began to beat (at the ninety-
ninth hour), they reached 104 per minute (No. 154, p. 193), but the conditions
must have been abnormal. The rate noted by LerEBouLLer in Perca, viz., 40, 50, or
60 times per minute, is normal (No. 93, p. 451). In a ling of the second day (Pl. XIII.
fig. 4) the pulsations were observed to have reached the rate of 80 beats per minute.
The endothelial lining of the heart appears as a single delicate layer of cells, very much
flattened and loosely suspended in the cardiac chamber, apparently derived from the
myocardium or thick contractile layer. OXFLLACHER regards it as developed in the trout
from the hypoblast beneath, and his figures on Taf. iv. (No. 114) are very clear; but
no such continuity of the endocardium with the limiting hypoblast below is shown in
* In certain insects Parren has found that two mesodermic plates by a median longitudinal fusion form a solid
cord (Phryganida), while in others (Blatta) it is hollow from the time of its formation, and the mesodermic folds pulsate
long before they unite to form the heart (Parren, “ Develop. of Phryganids,” Quart. Jour. Micr. Sci., vol. xxiv., 1884,
pp. 587, 597).
+ Trawling Report, 1884.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES, 777
sections of our forms. Certainly it is not formed, as has been suggested for the chick,
by wandering corpuscles from the area vasculosa, which, finding access to the heart, cling
to its walls as a loose lining, for in Teleosteans this endocardium is present before the
hemal circulation is in action. Horrmay’s figures (No. 69a, Taf. iii. fig. 9, Taf. iv. fig. 6)
do not represent the primary condition in our forms, for the heart usually pushes down
before it a delicate stratum of hypoblastic cells (hyp, Pl. VIII. fig. 11; Pl. XI. fig. 2) ;
but this limiting ventral layer apparently becomes obliterated anteriorly, and the
pericardial chamber is open to the subembryonic space, which is undoubtedly the persist-
ing germinal cavity. The vermiform outline (4, Pl. VIII. fig. 3; Pl XII. fig. 4) soon
undergoes modification, and the posterior end becomes expanded, while the anterior and
upper ventricular portion remains narrow (h, Pl. XIV. fig. 1). Thus the simple cardiac
tube becomes cone-shaped, the apex of the cone being continuous with the sub-cesophageal
mesoblast (mes, Pl. VIII. fig. 11), while the lower anterior end is comparatively free,
though not perfectly so, as a thin mesoblastic membrane (PI. VIII. fig. 5) continuous
with the free edge of the auricle separates the myocardium from the exterior, and a space
is formed—the pericardial chamber (pd) around the heart.
By its mode of formation as a downward growth the heart has at first a somewhat
vertical position ; but with its increase in length it extends further and further forward
beneath the head, and moreover it becomes flexed to the right (PI. VIII. figs. 2, 9). The
anterior position of the heart at this time is quite characteristic of the early embryo.
The before-mentioned delicate pericardial walls are involved in the rhythmic movements
of the organ, and sway to and fro with each systole and diastole.
The splanchnic mesoblast, out of which the heart and pericardium are formed, has
relations similar to the splanchnopleuric prolongation in the region of the trunk proper,
—the pericardial cavity surrounding the heart just as the cceloma encloses the abdominal
viscera,—the view that the former is merely a part separated off from the latter by the
posterior (pericardial) septum being strikingly supported by the condition in the
Cyclostomes, in which an intercommunication of pericardium and body-cavity persists
throughout life.
The first change in the position of the slightly curved cylindrical heart (Pl. VIL.
fig. 5) results in its assuming an L-shaped form (as in Pl. IX. fig. 1, 4), the small arterial
end (ventricle, ven) still occupying the median position, while the auricular end (aur) is
turned at right angles. In the figure before referred to, the flexure is still more apparent ;
while in fig. 3, Pl. XIL., the auricle, previously directed to the front (Pl. VIIL. figs. 3, 6, 8),
is now posterior (see also Pl. VIII. fig. 9), the flexure continuing to increase as development
proceeds. Thus the relations of the auricle and ventricle are reversed, and the latter,
which is now anterior, becomes bulbous (ven, Pl. VIII. fig. 7), and distinctly marked off
by a constriction; while the auricle (a) itself is separated by a cincture into auricle
proper and sinus venosus (sv). The blind continuation of the ventricle into the sub-
pharyngeal mesoblast (mes, Pl. VIIL. fig. 11) above is really the rudimentary bulbus
arteriosus, so that the four parts may be distinguished, as Ryprr pointed out (No. 141,
VOL. XXXV. PART IIL. (NO. 19). 6G
778 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
p. 537), about or soon after the time of hatching. Occasionally one or more detached cells
may be seen loosely suspended in the auricle, near its external opening, and they swmg
to and fro with the heart’s pulsations. No blood, as such, exists until a later stage, and
any fluid included in the lumen of the heart and the pericardium must be non-corpus-
culated, and its presence cannot be demonstrated. It may be doubted whether the stray
corpuscles above referred to are blood-elements at all, for LEREBOULLET is almost certainly
correct when he says that it is erroneous to assert that the corpuscles which first appear
in the heart are detached from its walls: “they are different in character, and too
coherent to become detached” (No. 93, p. 585). In our specimens these had the appearance
of papillae on the cardiac wall, Ryprer regards the periblast as the source of the blood-
corpuscles, in accordance with Horrman (Zool. Anz., 1880, p. 633); and in this view
their connection with the so-called free nuclei around and beneath the early blastoderm
is naturally suggested. Ryprer contends (No. 141, p. 537) that the pericardial cavity
is really the persisting segmentation- (or more correctly, germinal) cavity, and that the
passage of periblastic blood-elements mto the heart is thus secured. It must be
remembered, however, that the roof of the germinal cavity consists of the subembryonic
hypoblast, a layer which stretches beyond the tip of the snout of the young fish, and
extends as the under-stratum of the double-layered yolk-sac (ys, Pl. V. fig. 8). This
subcephalic chamber, with its floor of periblast and roof of hypoblast, is never obliterated;
but though its periblastic floor does not bud off cells to form the ventral half of the
mesenteric wall, yet its roof (ys) becomes pushed downward (vide Pl. XII. figs. 1, 3)
until it lies below the pericardium (Pl. XII. fig. 2; also see Pl. VIII. fig. 6), and is
separated only by a narrow fissure from the periblast (per) beneath. The germinal
cavity diminishes in a less degree laterally, and the latero-pharyngeal spaces into which
the embryonic breathing aperture opens from without (see p. 747) are its more visible
remnants (ss, Pl. IV. fig. 21; Pl. XI. figs. 6, 7, 8). The floor of the pericardium
appears (vide Pl. IV. fig. 21) to be obliterated anteriorly, but even in this case
the delicate hypoblast would seem still to separate the pericardial from the germinal
cavity below. The absence of the limiting layer from a certain area may be explained
also, not by obliteration, but by a different method of origin, and it is quite possible that
the pericardium may be a fold of mesoblast directed forward. Truman, indeed, speaks
of such a mode of development in sow, a membranous fold being reflected from the
under part of the head (No. 154, p. 190).
Meanwhile the vascular canals of the trunk are in course of formation, a small arterial
vessel (the dorsal aorta) being hollowed out of the loose trabecular tissue (really the
intruding mesoblastic cells above the gut which are broken down) along the under side of
the notochord (x, Pl. VII. figs. 1, 4, 6; Pl. XII. fig. 8), and two venous trunks of large
calibre are similarly formed in the lateral connective tissue just external to each head-
kidney. In the living larva of Molva vulgaris, on the fourth day, the subnotochordal
tissue seems to be traversed by a single large vascular channel (vn) separated by an
interval, probably the dorsal aorta (ao), from the chorda (nc). The large channel can
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 779
be traced from the liver posteriorly to the caudal region, and it contains numerous large
round corpuscles, though these do not seem to occur anterior to the liver (PI. XV. fig. 1).
Again the venous trunks immediately in front of the pectoral fins send prolongations
downward, and communicate with the venous end of the heart, which at this time shows
the broad auricle directed upward and backward, and a spacious sinus venosus (sv,
Pl. XII. fig. 8). The large venous tube thus passing to the sinus on each side is the ductus
Cuvieri, which, in addition to the posterior (cardinal) vein, also receives the anterior
(jugular) trunk. Around the two anterior veins the cellular tissue of the pronephros
grows (prn, Pl. XI. figs. 9, 11), and venous ramifications are developed in the midst of
the renal matrix. Before the end of the first week after hatching—generally on the
fourth or fifth day in Gadoids—a simple circulation can be detected. The anterior
bulbous end of the heart driving the blood upwards behind the eyes—probably by the
artery of the hyoid arch, whence it courses by the great subnotochordal trunk (dorsal
aorta) to a point a little posterior to the root of the tail, and, passing round by a minute
loop, returns by a large venous trunk which anteriorly divides into the two cardinals
already mentioned. The two subnotochordal trunks with the anterior branchial artery
constitute the simple vascular system in its earliest condition. A day or two later a
venous branch leaves the vena vertebralis at a point about midway along the trunk—
above the mesenteron, and passes down to the lower side of the alimentary canal—and
forward along the margin of the liver to the sinus venosus. This must be. the
subintestinal vein, which is, however, usually described as passing along the intestinal
portion of the alimentary canal. Its course, however, is at this stage very short. Not
so in the case of the intestinal artery (cceliaco-mesenteric) which leaves the dorsal
aorta in the pectoral region, traverses the mesenteron in descending, then courses
beneath the rectum, but ascends before reaching the anus, and passes along the anterior
margin of the urinary vesicle to join the caudal vein. The caudal vein is lengthening
simultaneously with the caudal artery; thus, in a cod on the seventh day both reached
barely a quarter the length of the caudal trunk, while on the fourteenth day they
extended almost to the tip of the tail. The force of the arterial current seems to hollow
out the yielding channel, and causes it to become longer, but the afferent venous trunk
has the appearance of a somewhat irregular ill-defined sinus. During the second week
great advances take place in the hemal circulation. LereBouLLer noticed, in Perca
about two weeks old, that blood was passing along two of the gill-arches; and in the
Gadoids and other forms described in this paper two arches likewise develop arterial
channels. There is considerable variation in the details of this development; thus a
haddock, on the fourteenth day after extrusion, showed arterial blood passing along
two (apparently the anterior) branchial arches, whereas another embryo of the same
species, on the eleventh day, showed three branchial arteries and a fourth artery, which
runs apparently within the opercular fold, possibly, however, the hyo-opercular. The
mandibular artery is a well-marked trunk coursing along the outer margin of the
780 PROFESSOR W. C. M‘SINTOSH AND MR E. E. PRINCE ON
mandible.* Both arteries meet in front of the symphysis, and return by a single median
vein along the floor of the mouth. The later developments of the hamal system at a
stage—in, say, Gadus morrhua—when the caudal artery extends along fully two-thirds
the length of the tail, are as follow :—Four branchial arteries can be made out, and
a submaxillary artery passes beneath the eyes, while a return-current is directed over
the eyes, along the supraocular vein. The coeliac artery, before described as leaving
the aorta in the pectoral region, passes over the liver, along the ventral surface of the
intestine, and sends an arterial branch upward, which, bifureating, supplies the walls of
the intestine,—the main trunk continuing its ventral course, and ascending in front of the
urinary vesicle,—over the walls of which it passes to the vena vertebralis. The venous
trunks form a more complex system—the simple subintestinal loop which breaks up into
an elaborate hepatie capillary network still continues, but it is joined by a large visceral
trunk on the posterior side of the liver. This latter vessel leaves the caudal vein at the
root of the tail, passes ventrally in front of the urinary vesicle and over the walls of the
rectal portion of the intestine to the termination of the mid gut. At this point a
large venous trunk branches off dorsally to join the posterior cardinals. Minor venous
branches run from the walls of the stomach and pyloric portion of the intestine, forming
the first indication of the portal system—all their blood finally passing in front of the
liver into the sinus venosus by the hepatic veins. The liver, the dorsal lobe of which
lies above the alimentary canal and behind the swim-bladder, is seen chiefly as a rounded
mass (the left and ventral lobe) projecting boldly into the surface of the yolk below, and
lying immediately in contact with the posterior pericardial wall. The proximity of the
liver with its rich vascular plexus, and of the large ductus Cuvieri pouring a stream into
the capacious sinus, suggest the possibility that it is at this point that the assimilation
of yolk-matter is most active. It is absorbed and conveyed to the heart by the venous
blood. The continuity of the wall, limiting the pericardial chamber (pd, Pl. VII. fig. 9),
appears to be unbroken, and roofs over a sub-pericardial space (ss) filled with a serous plasma
and disintegrated yolk. A suboral chamber in many cases seems also to be shut off by
this membrane (Pl. VIII. figs. 6, 7). The heart’s pulsations partake of a progressive
vermiform movement, the auricle, continuous with the sinus venosus, contracting first,
and the successive parts (of the auricle) contract in order, the ventricle dilating as the last
part of the auricle closes. As the ventricle contracts, the open end of the auricle dilates.
- The progressive systole being triple, : tee ol 2 3
B : ; a C)\ contract
= (See accompanying diagram,) : s , (4)—(B)—(f) dilates
L The diastole also is threefold, and D contracts ) (A)—(B)—(C) dilate
simultaneously with the dilatation of A, . ) (D) contracts.
The delicate pelagic forms chiefly considered in these pages present a great contrast to
* Gorre is certainly incorrect, as Batrour pointed out (No. 11, p. 645), in denying that a mandibular artery is
ever developed in Teleostei (No. 59).
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 781
the stronger and more robust Teleosteans, which are at a very early stage, often long before
extrusion from the egg, provided with a complex vitelline circulation. In such forms as
Salmo (Pl. XXII. figs. 4-9), Anarrhichas (Pl. XX. figs. 2, 4, 5), Gastrosteus, Cottus,
Liparis (Pl. XV. fig. 2), and Cyclopterus, the blood-corpuscles seem to be mainly
derived from the nucleated particles into which the surface of the yolk becomes broken
up, and, as already noted, TrumMAN found in Hsow that hemal channels appeared upon
the yolk, and corpuscles slowly moved towards the heart before this organ showed any
motion. No such blood-canals are excavated in the yolk of the pelagic forms here
treated of, indeed no yolk-circulation ever truly exists in the gurnard, cod, and allied
forms. Nevertheless, the yolk steadily diminishes, and in embryos, fourteen to twenty
days after hatching, it forms but a very slight projection, and at the end of the first
month would appear to be entirely absorbed (compare fig. 5, Pl. XIX. and fig. 1,
Pl. XVL). The surface of the yolk, however, shows during this time rapid disintegration
(vide Pl. VII. fig. 9), vesicles, granules, and nucleated particles appear in it (Pl. XI.
fig. 12), and are especially noticeable around the large oleaginous spheres (PI. XI.
fig. 13) in those forms, such as the gurnard, ling, and others, in which these striking
bodies occur. The protoplasmic envelope of the globule in such cases becomes richly
provided with large nuclei showing one or more nucleoli, and similar bodies occur
superficially over the yolk. In a young perch, eleven to fourteen days old, LEREBOULLET
observed, just as we have noticed in the Gadoids and other forms, the dorsal aorta, formed
by the union of the vessels of the branchial arches, sending a supply to the intestine and
adjacent viscera, and reaching to the extremity of the tail, while of venous trunks the
two anterior and two posterior cardinals and the subintestinal vein are common to both.
In Perea, in addition to the above trunks—developed no doubt in all Teleostean larvee,
a complex yolk-circulation arises, and is supplied by branches from the posterior cardinals
and from the subintestinal vein, These branches pass over the yolk as simple undulating
lacunze formed by the separation of the substance of the yolk-cortex, and meet on the
ventral side of the yolk in a pair of large veins, which form one large sinus, continuous
with the sinus venosus in the pericardial chamber. LEREBOULLET says of these vitelline
vessels, that they do not appear to have proper walls, and form an ill-defined and irregular
network; but on the third or fourth day after hatching the hamal canals acquire definite
walls, the network elongates, so that the main trunks show a parallel arrangement (No. 93,
p- 601). In Perca the development of this circulation over the yolk is much more rapid
than in Hsox, and LEREBOULLET connects this with the larger perivitelline space in Perca,
as there is a greater need for respiration; and for this reason, he says, in that species “ the
capsule is spacious, and holds so large a quantity of water” (No. 93, p. 610). The true
explanation, however, seems to be that the more complex and rapid the circulation the
more speedily the bulk of the yolk is reduced, and hence a large perivitelline space is
produced. It is remarkable, however, that in such forms as the gurnard, rockling, the
flat fishes, and Gadoids, in which no vitelline circulation ever develops, the yolk should
still show a very rapid disintegration (compare Pl. XII. figs. 1 and 3, with Pl. X.
782 PROFESSOR W. C. M‘INTOSH AND MR E, E. PRINCE ON
figs. 1, 2, and 3, and Pl. XVII. fig. 2). This does not take place, however, to any very
appreciable extent while the embryo is within the ovum, whereas the reduction is
very marked in Perca (No. 93, p. 610), Cyclopterus, and similar species. After the
embryo emerges in pelagic forms, and before any circulation of a corpusculated hemal
fluid exists, the yolk, which is very large and prominent in the newly hatched fish,
becomes speedily diminished. A process of absorption must be actively going on in
these forms (e.g., cod), and the presence of a transparent plasma hathing the tissues, and
filling the pulsating heart and lacunz of the trunk, is suggested.
The origin of the blood-corpuscles is an interesting point; but there is little
unanimity amongst observers on this matter respecting Teleosteans, and appearances seem
to support more than one suggested mode of origin. Ryprr, with Horrman and others,
as we have already said, holds “that the blood-cells are budded off directly” from the
periblast, the nuclei of which layer by division give rise to groups of granules, the form-
elements of the blood (No. 141, p. 543). C. Voer in 1842 distinguished a “ couche
hematogéne” (No. 155), as did also RatHKe and Von Bakr, their third or vascular layer
of the blastoderm being, however, derived from the “lower layer” or hypoblast-cells ;
and Van Bamsekg, while admitting that the periblast or “intermediary layer” has not
been proved to be this ‘ vascular layer,” appears to consider their homology very probable
(No. 20a, p. 9). Genscu’s researches support this view, the corpuscles arising from the
layer surrounding the yolk—‘ Kuprrer’s secondary entoderm.” In opposition to
Kurrrer’s affirmation that the outer mesodermal yolk-sac gives origin to the corpuscles,
Genscu found that in Hsow and Zoarces viviparus no mesoblast was present in the region
where they arose, the two-layered epiblast lying upon the granular periblast in which cells
were imbedded. These cells give out pseudopodial processes, which are constricted off to
form corpuscles, and these by subdivision produce blood-islands (vide No. 56). In Salmo,
Alosa (No. 141, p. 537), Gastrosteus (No. 122, p. 494), and other forms, the phenomenon
described by Grenscu has been observed, yet it is not conclusive that the primary
corpuscles are derived from the “ Dottersack.” That the periblast contributes to the
nutrient hemal fluid of the embryo there can be no question, but the point of chief
moment is, whence are the primary corpuscles derived? As LerEBouLLEer long ago
pointed out, the heart beats for some time before corpuscles appear in its lumen ; and he
added that the heemal trunks too are formed, as in the gurnard, before the corpuscles
(No. 93, p. 577). Werncxepacn, however, holds that in the process of formation the
blood-vessels give origin to the corpuscles, so that both originate contemporaneously.
This observer concludes that the blood-corpuscles appear to him to arise in a solid mass
of tissue in the region where the vena vertebralis is afterwards situated, the cells
constituting this mass being carried away by a hemal plasma, and acquire the colour
and character of blood-corpuseles subsequently (No. 157). The polyhedral cells which
Wenckepacu shows filling up the lumen of the subnotochordal vein (vide No. 157,
pl. viii. figs. 2, 3, &e.) are also found, in section, to fill up the aortic trunk, and there
is no reason why the derivation of these blood-cells should not be extended to all the
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 783
heemal vessels. The fact, however, seems to be that the form-elements of the blood are
for the most part derived from the periblast, the primary corpuscles alone being
moulded apparently from the detached cells of the subnotochordal trunks. In those forms
in which a vitelline circulation is developed, the removal of nucleated periblastie cells
and the formation of sinuous lacunze (primary hzmal trunks) has been repeatedly
observed, and may almost be taken as established. In those without such a yolk-circula-
tion (and to them reference is in these pages chiefly made), the periblast also is seen in
sections to break up into similar particles, and these doubtless pass into the sinus venosus,
though in what way is not decided. Certainly the liver and alimentary canal, as well
as the pericardial chamber itself, are, as already pointed out, in intimate relation to the
periblast beneath the embryonic-trunk (PI. VII. figs. 1, 2, 6, 9; also Pl. XII. fig. 8), and
the transmission of detached periblastic elements into the circulatory plasma may be
accomplished without difficulty. Ryprr, in Salmo and Tyloswrus, found such corpuscles
in the pericardial chamber (No. 141, p. 537). This further consideration favours the
latter derivation rather than the subnotochordal origin, viz., the rapid decrease in the
volume of the yolk, even in those which have no yolk-circulation. In such forms the
yolk protrudes as a very bulky appendage (y, Pl. XIV. fig. 1), but shortly before, and
especially after the blood-circulation is visible, it diminishes very rapidly (y, Pl. XVII.
fiz. 1). Now, if before the hemal fluid flows through its proper channels, it were
deriving its corpuscles from the yolk, and still more, if with the further development of
blood-vessels in the trunk a corresponding increase in the number of corpuscles takes
place, the rapid disappearance of the yolk is readily accounted for. It is noteworthy,
too, that while the subnotochordal trunks are the first to be developed, the formation of
the subintestinal vein and ceeliac artery quickly follows, and as these probably communi-
cate with hepatic lacune, the periblastic elements would find easy entrance into the vascular
system of the embryo. These nucleated cells, which make their way into the hemal
plasma, are originally colourless, and LerEBouLLer describes them as at first spherical,
afterwards becoming flattened and elongated. They rapidly acquire the characteristic
tint. In weak and sickly embryos the circulation is languid and the corpuscles few, a
feature LEREBOULLET also noted (No. 93, pp. 581-2). In monsters, especially double
embryos, the circulation presents interesting features, each having its own circulation,
though receiving nourishment from a common yolk. LEREBOULLET instances the case of
a trout (double monster) in which the artery divides into two vitelline trunks, each of
the two returning as veins to the corresponding embryo; while in another case of a
double-headed embryo, which possessed two hearts, one alone received blood from the
vitelline veins, the other heart received nothing (No. 94, p. 246).
Renal Organs.—The differentiation of a renal tract takes place at a very early stage.
We have seen that on each side of the notochord (PI. IV. fig. 10) cuboid masses of
mesoblast are serially marked off as protovertebra (my) soon after the separation of the
somatopleuric from the splanchnopleuric lamella. Just external to the protovertebre, a
little distance behind the otocysts, a rod of cells is budded off from the splanchnopleure
784 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
in close proximity to the intermediate cell-mass. LEREBOULLET observed that in Perca
this structure develops earliest posteriorly, for he failed to trace it anteriorly, though at
a later stage, about the time of hatching, he was able to follow its whole course (No. 93,
p. 633) anteriorly and posteriorly, In some species a fold is developed, not a solid rod.
RosENBERG seems to have been the first to speak of it as a diverticulum from the
somatopleure (No. 138), and OzLLacHER, HorrMaN, and others have confirmed this view.
Ryper asserts that “ the development of the renal organs in different genera of Teleosteans
differs greatly in detail” (No. 141, p. 533), and this would certainly appear to be so, for
in Salmonoids, which the observers named chiefly investigated, the origin of these ducts
as longitudinal diverticula pushed dorsally towards the epiblast, as a groove-like fold, in
fact, of the peritoneal cells, has been clearly shown (see OELLACHER, No, 114, fig. 18,,
Taf. iv.; Horrman, No. 69a, Taf. iii. fig. 3). Yet in Gadoids and Pleuronectids it is by
no means clear that this is the precise mode of origin. In the earliest condition yet
observed in these pelagic forms a longitudinal blastema or solid cylinder is formed on the
outer margin of the intermediate cell-mass, just as we find in the chick. Defined at
first in the region of the mid-trunk, this blastema rapidly extends forward to the pectoral
region, but posteriorly it develops more slowly and is ill defined. A lumen is formed by
the radiate arrangement of its cells, which separate at their common point of junction,
and it is now outlined throughout its whole length some days before the embryo emerges.
In an ovum (haddock) of the ninth day these structures are very distinctly seen as a pair
of simple ducts, with walls consisting of a single layer of columnar cells, and extending from
the pectoral region to the root of the tail, Anteriorly each tube is folded upon itself,
turns inward towards the notochord, and ends in a trumpet-shaped infundibular opening,
a condition exactly according with that described by Batrour and Parker in Lepidosteus
(No. 18, p. 415); but in that species the authors agree with RosENBERG and OELLACHER,
that it is a hollow outgrowth of the somatopleure, and freely communicates with the body-
cavity. The two ducts are widely separated, but as they pass backward gradually approach,
and, curving down in the anal region, they meet and unite beneath the notochord in an
unpaired common portion (wv, Pl. VIL. fig. 8, and in section fig. 6a), which is originally
of small capacity and provided with thick walls. At first the ducts are somewhat super-
ficial (prn, Pl. VII. figs. 1, 2, 3), as is implied in their mode of origin, being dorsally
directed outgrowths of the proximal somatopleure; but they undergo a change of position
similar to that exemplified in the chick, and lie ventro-laterally to the notochord (sg, PI.
VIL. fig. 4), and ultimately protrude into the peritoneal cavity (sg, Pl. XI. fig. 14).
Ryper did not make out the mode of termination in Gadus, and he supposed that the
urinary vesicle opens either directly into a cloaca or the terminal portion of the intestine.
The continuity of the walls of the ducts (sy) with the bilobed upper part of the urinary
vesicle (wv) is clearly demonstrated in section (Pl. VIL. figs. 7, 11), and the urimary
vesicle itself has an outlet in its early condition of an interesting nature. LEREBOULLET
described in Perca the first condition of the ducts, and says that each must be a secreting
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 785
organ solely, assuming the excretory function later, when the ovoid dilation (urinary
vesicle) establishes a communication with the lumen of the enteron (No. 93, p. 633).
Kuprrer draws attention to a strand of cylindrical cells connecting this receptacle and
the hind gut, “ uniting,” he says, “ with the epithelium of the gut” (No. 87, p. 224); but
he appears not to have made out, any more than LeREBoOULLET, an actual communica-
tion between the two. Yet such is the case. A distinct tubular connection exists; but
the walls of the vesicle (wv) as well as the enteron (ig) are extremely plastic and mobile,
vermiform movements being frequent, so that the lumen between the two becomes wider or
narrower, and at times appears to close up, though the communication is usually readily
seen (Pl. XX. fig. 13). Throughout their whole length, these excretory canals, including
the urinary vesicle, exhibit simply a wall of nucleated cubical cells—a single layer of
cylindrical epithelium. Such is the condition of the renal tract until the time of hatch-
ing, viz., a pair of cylindrical tubes, which pass along each side of the subnotochordal
heemal trunks, to terminate, after curving inward and downward in an infundibular
opening. In front of the crozier-shaped loop (prn, Pl. XI. fig. 11, and Pl. XXI.
fig. 6) a mass of trabecular tissue lies, into which tubules appear to enter to some
extent, but this loose connective is also penetrated from the front by the growing basilar
plate. The simple character of the embryonic renal organs in the Teleostei may be taken
as evidence of a primitive condition, in which no metamerism is seen, the simple duct,
which is truly an archinephric duct, forming a loop in front, and communicating with the
pleuroperitoneal cavity, while posteriorly it passes into the hind part—a cloacal section,
in fact—of the enteric tract.
During the greater part of embryonic life this simple condition continues, and the
infundibular openings do not seem to increase in number; whereas in Amphibians several
(three or four) are developed, and in Selachians they form a series. When the young
fish emerges, the anterior end of the kidney shows signs of growing complexity, the folds
of the loop increasing, and a vascular glomerulus being developed in front of the swim-
bladder near each nephrostome. A little later the nephrostome of each side and its
adjacent glomerulus are gradually enclosed in a capsule, this fibrous sac shutting off both
structures from the general body-cavity. A section just behind the occipital region
(Pl. XXVI. fig. 4) shows one of a pair of such capsules in the middle line and below the
median hemal trunks (ao and cv). On the lower and inner side of each capsule a
vascular meshwork (g/) is present, while the nephrostome of the head-kidney opens on the
outer side of the capsule. The rudiments of the single pair of glomeruli are seen in the
newly emerged embryo, and are not fully developed until some days later; but in
Gastrosteus and like forms, which issue from the ovum in a more advanced condition, the
later features are already exhibited. RypeEr states that in Clupea alosa there is no
evidence of the existence of a nephrostome or of the presence of median glomeruli until
long after hatching (No. 141, p. 534), and this is certainly remarkable, though in the
Gadoids and others great variations are observable, the renal organs being fairly advanced
in P. platessa a day or two before hatching, whereas in P. flesus and P. limanda they.
VOL. XXXV. PART III, (NO, 19). 6H
786 PROFESSOR W. C. M‘INTOSH AND MR E, E, PRINCE ON
are more rudimentary. The waste-products taken along the renal ducts originally pass
directly from the body-cavity, but they are by and by conveyed from the special excre-
tory Malpighian capsules into the urinary vesicle behind, a condition which remains
essentially unaltered in the adult. The archinephric duct does not really close early in em-
bryonic life, as has been stated (No. 48, p. 13), but opens into a special closed part of
the body-cavity. With the further development of the anal region, the unpaired enlarged
portion into which the ducts pass posteriorly communicates not with the rectum some
distance from the external orifice as in the figure before referred to, viz., Pl. XX. fig. 13,
but by a special passage with separate opening posterior to the anus, as in a cod the
third week after emerging—a condition also shown in the gurnard three weeks old
(Pl. VIL fig. 9). Of the series of segmental tubules and glomeruli seen in Elasmobranchs
there is no trace in Teleosteans; but though the renal organs are so simple in these
latter forms, the interpretation of the various parts is not devoid of uncertainty.
Teleosteans, it is generally held, agree with Cyclostomes, Amphibians, and Ganoids in
possessing a pronephros ; but, in all, it is a larval structure, and is supposed to disappear
in the adult. We have seen that in the embryos of the Gadoids, flat fishes, and
gurnards an anterior trabecular meshwork () lies in front of the archinephric duct, and
that this duct itself exhibits a much convoluted fore end (prn, Pl. XI. fig. 11), with a
nephrostome communicating with a glomerulus. The mid-portion of the duct becomes
more or less convoluted, while the posterior portion remains comparatively straight,
though on its dorsal side a large development of cellular tissue and small sinuous tubules
takes place at a late or post-larval stage (Pl. XXIII. fig. 2).
In the adult we usually find an enlarged anterior paired structure, the head-kidney or
pronephros succeeded by a pair of elongated bodies, indisputably renal, which are much
swollen terminally, often united, and traversed on their ventro-lateral margins by a pair
of excretory ducts. BaLrour examined various species of Teleosteans in the adult
condition, and came to the conclusion, in opposition to RosenBerc, that the so-called
head-kidney is not truly renal, though he did not deny the persistence of the larval
pronephros in the adult stage (No. 13, p. 15). In Osmerus eperlanus, Esox lucius, and
Anguilla, the fore part of the renal mass consisted in the main of vascular lymphatic
tissue, while the true kidney-substance extended posteriorly. In Lophius piscatorius,
which, according to Hyrvt, possesses a head-kidney only, lymphatic tissue, traversed by
tubules alone, was found. This lymphatic tissue may represent the convoluted enlarge-
ment of the archinephric duct, or merely a compact agglomeration of the loose cellular
tissue lying external to the ductus Cuvieri and cardinal veins. It would appear that
the latter is, in a large degree, true, the fore part being more emphatically trabecular,
while the hind part consists of degenerate kidney-substance, so that BALFour’s view most
probably represents the facts, viz., that the so-called head-kidney is really a large
lymphatic gland, concerned in the production of blood or lymph-corpuscles, while the
hind portion is a remnant of the embryonic head-kidney. Except for certain lymph-
spaces in the caudal region, the lymphatic system is but feebly represented in fishes, and
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 787
it is interesting to see a large glandular structure, such as the so-called head-kidney,
which may be made out in early embryos, and which is from the first closely associated
with the main hemal vessels of the trunk. The lymphatic system, with its plasma and
leucocytes, is really intermediate between a venous and an arterial system, and is
associated with the various serous membranes, pleural, peritoneal, pericardial, and others.
It is not surprising that large lymphatic masses should occur so near the centre of the
blood-system, and though BaLrour was not inclined to regard them as parts of the
true kidney at all, they cannot at any rate be regarded solely as degenerate pronephric
structures. WELDON, in his brief but interesting paper on Bdellostoma (No. 156),
suggests that such masses are represented in all vertebrates by the suprarenal bodies.
In Bdellostoma the archinephric or segmental duct is separated from this anterior mass,
though in some specimens, possibly younger, traces of the continuity of the two could be
made out. In embryonic Teleosteans the continuity is very patent, and in the adult
condition renal tubules still ramify amongst the lymphatic tissue, as BaLFour found in
Esox, Lophius, and Osmerus. In the last species a single tubule alone passes into the
vascular lymphatic mass. It would appear, indeed, as if the embryonic pronephros in the
process of degeneration were usurped by the antenephric lymphatic structures, the
proximity of both favouring this, while the persistence of stray tubules in the posterior
part indicates the pronephric portion. GROosGLIK’s researches upon various adult
Teleosteans (Cyprinus carpio, Esox lucius, Rhodeus amarus, Gastrosteus aculeatus) con-
firm BaLrour’s view, as he found coexisting in the region of the head-kidney lymphatic
tissue and remains of the atrophied pronephros surrounded to some extent by the cardinal
vein, while some pronephric tubules still pierced the lymphatic meshwork (No. 60,
pp. 605-611). Emery, however, maintains that the pronephros persists permanently in
such as Fierasfer and Zowrces; while in other forms, as Blennius, it is provided with
glomeruli and tubules, and in Merlucius esculentus it presents the peculiar structure of
the Wolffian body. In all it persists as a recognisable pronephros (No. 53a), a view which
Hyrtt held; while Raruxe and Sranntus concluded that in Cyprinus the head-kidney
is degenerate, and bereft of tubules, a view now generally adopted. The segmental duct
precedes the development of the Wolffian body, and cannot therefore be a mesonephric
duct, as BaLrour suggests (No. 11, p. 701); it is in fact a pronephrie duct, or more
truly it is archinephric, for the pronephros is secondarily developed as a convoluted
anterior portion. It is possible that this duct may not represent the primitive condition,
but rather a segmental canal bereft of its serial segmental tubules and nephrostomes,
save the single infundibulum at its anterior termination.* The view generally accepted
however, is that which interprets it as a primitive non-metameric renal duct. The ducts
retain their simple tubular character in the adult condition, and pass along the latero-
ventral margins of the fully-developed renal masses. In the last larval stages, within a
* The fact, however, that some segmental tubes, consisting of nephrostome, capsule, and convolutions, develop in
Elasmobranchs independently of the duct, and later connect by their originally blind end, may indicate that the serial
condition is secondary. It illustrates at any rate their separation and independent coexistence, whatever the explana-
tion may be.
788 PROFESSOR W. C. M‘SINTOSH AND MR E. E. PRINCE ON
month after hatching, mesoblastic cells become aggregated along the whole dorsal extent
of the two ducts, especially in the fore and hind regions, and they present a somewhat
glandular character, minute sinuous tubules appearing in their midst, which pass down
and open into the longitudinal ducts. Plate XXVI. fig. 3, shows this elongated renal
mass of segmental tubules, and presents largely the features of the permanent renal bodies.
Still better is the relation of the parts seen in the section (Pl. XXV. fig. 3). The
simple epithelial walls of the excretory ducts (sq) are fibrous and thickened, and become
in fact the permanent ureters. GEGENBAUR views the pronephros as the primitive excre-
tory gland of the Chordata, whose place has been taken by the mesonephros, and we see
that while the pronephric ducts persist the phylogenetic replacement of the pronephros by
the Wolffian body is ontogenetically repeated. It is noteworthy that the segmental ducts
become much convoluted along their course, but especially in the fore-portion. What-
ever this may signify, these primitive archinephric ducts are the same as those which in
Elasmobranchs and others connect the serial segmental tubes, but in Teleosteans they do
not appear to divide longitudinally into upper or Wolftian ducts and ventral generative
canals. The connective tissue which surrounds the renal organs becomes deeply
pigmented at a very early stage (PI. VII. figs. 1, 3, 4, and 7), the large black corpuscles
continuing to increase until their structure in later embryonic stages becomes obscured
on account of the profuse distribution of these bodies (vide Pl. XVII. figs. 1 and 2, and PI.
XXVI. figs. 3 and 4). The close connection of the early segmental ducts and the rudi-
ments of the pectoral fin has been pointed out, and it is interesting to note that the
black pigment, surrounding the renal organs at a later period, extends over and is con-
tinuous with the pigment-layer which passes to the base of the developed fin. The wall
of the urinary bladder at a subsequent stage presents a consistent connective-tissue layer
(conn), lined with columnar epithelium (epith), which in the upper portion forms pro-
minent folds (Pl. XXYV. fig. 5). These folds are continuous with the two excretory
ducts, which, as formerly stated, open into the wpper and anterior wall of the vesicle.
The Integument and Embryonic Pigment.—Throughout embryonic life the in-
tegument remains thin and transparent, so that the internal structure of the young fish
is readily seen. No cilia can be detected upon it. As already pointed out, a flattened
external layer or stratum corneum (ep, Pl. IV. figs. 5a—5d) is distinguished from the
subjacent layer, the neurodermis (ve). Soon after the notochord is defined these two
layers extend as a distinct integument, not only over the dorsum and flattened parietes
of the embryo, but as a yolk-sac, over the vitelline globe (Pl. VII. fig. 6). The
neurodermis, later in embryonic life, consists of several layers of pulpy rounded
cells, which gradually merge into the flattened epidermis above. The innermost part of
the two-layered epidermis constitutes a stratum Malpighii, and from it apparently exudes
a lymphatic plasma, which forms a distinct fluid layer (ss, Pl. VIL figs. 1, 3, 4, 6), such
a cutaneous sub-layer being found in Amphiowus and the Cyclostomes, though separated
from the epidermal layers by the dermis proper. In Teleosteans when the mesoblast
extends beneath the epidermis, to form the cutis proper, such a separation will be also
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 789
effected. There is, at an early stage, no true dermis beneath the Malpighian layer.
Poucuer speaks of this subepidermal tissue as a soft variety of laminated tissue, having
a very loose texture, and therefore little firmness (No. 119, p. 291), but in its earliest con-
dition it is simply a soft semifluid stratum in which amorphous matter abundantly occurs.
In this layer pigment develops (pt, Pl. IV. figs. 13, 20), and always appears as definite
amorphous corpuscles, not a mere diffused solution.
In different species the early coloration shows very distinctive features, the colour of
the pigment and its distribution being, in fact, so striking as to afford aid in diagnosis.
In some species the pigment is confined to the embryonic trunk (PI. V. fig. 2); in
others it extends over the extra-embryonic layer, 7.¢., the yolk-sac (Pl. XVI. figs. 2, 8).
Certain forms, again, exhibit one kind of pigment (Pl. XVII. fig. 1; Pl. XIX. fig. 8); others
show two or more colours in the larval stages (Pl. XVI. figs. 1, 3, 5-9). No generalisation
can be made, for in the same genus closely allied species show great diversity in these
respects. Usually the pigment occurs in the form of minute isolated spots scattered
upon the dorsum, and visible within one or two days after the closure of the blastopore ;
though it frequently forms superficial protuberances, evidently pushing out the epi-
dermal stratum at certain points. The form of the corpuscles undergoes rapid changes ;
thus in a larval cod under examination two spots at the anterior border of the liver were
seen to be finely branched, but before a sketch could be completed they visibly altered,
and presented a simple rounded aspect.
In the cod (Pl. XIX. fig. 8) and haddock (Pl. XVII. fig. 1) black spots only occur. In
the ova of the former species, seven days after fertilisation, these spots, amorphous or
rounded in form, were scattered sparsely over the dorsum and lateral regions, but in a
few days they multiplied and extended from the snout to the tip of the tail, without any
regular disposition. In larve of the cod, soon after emerging, however, a further change
in the distribution of the pigment takes place, for the spots, which are now elaborately
stellate, become aggregated in four distinct bands (Pl. XIX. fig. 8), two very dense
broad bands—a pectoral and an abdominal—occurring on the trunk proper; while
the tail exhibits two less dense bands, and often indications of a third. The haddock
never shows this regular series of dark bands, which seem to be so characteristic in the
newly emerged cod. In the ova of the haddock on the eighth day (two days after
closure of the blastopore), black spots are irregularly dotted over the dorso-lateral
regions, and subsequent changes chiefly affect the number and form of the spots. A
larva two days after emerging shows stellate spots of the most elaborate form, which
send out complex ramifying processes. These spots appear on the cranial region, and
very thickly in the post-otocystic and lateral regions of the trunk proper. Posteriorly
they are chiefly confined to the lower half of the caudal trunk, only two or three large
spots occurring above the level of the notochord. Occasionally one or two spots are
seen to send processes into the fin-membrane. The whiting offers a great contrast to the
foregoing Gadoids, since on the eighth day (three days after the closure of the blastopore)
very faint yellow spots appear, and are thickly distributed over the entire trunk, including
790 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
the tail. Not only so; but the fin-membranes and the yolk-sac exhibit similar spots in
abundance (Pl. XVI. fig. 2). They are very pale, and unless carefully looked for, readily
escape detection, but they are very characteristic of this fish, even in the late larval stages,
the pale yellow, with a distinctive greenish tinge rendering them important for diag-
nostic purposes. In this species one or more enucleate, elaborately stellate structures
frequently exist on each side of the mid-mesenteric region. Sometimes five or six of these
bodies appear upon the surface of the yolk near the trunk of the embryo. They have
the form of a “ bone-corpuscle,” but they are not pigmented, and their nature and meaning
are doubtful. In the ling, from the third to the fifth day (Pl. XIX. fig. 9), while the
blastopore is closing, neutral-tinted amorphous spots, apparently protoplasmic aggrega-
tions, which send out pseudopodial processes, and thus acquire a rudely stellate form, occur
over the yolk-surface (vide Pl. XIX. fig. 9). Two days later (when about thirty
protovertebree are segmented off) the trunk and fin-membranes are very richly supplied
with yellow pigment of a bright canary-tint (Pl. V. fig. 9). This consists of unbranched
corpuscles, and extends also over the yolk-membrane. Black pigment likewise appears,
a few rude spots at first behind the eyes, and similarly it is not confined to the trunk,
stray stellate spots extending over the yolk-surface, and especially over the protoplasmic
covering of the large oily sphere (og). On the trunk, from the otocysts (aw) to the tip
of the tail, a more or less regular linear series of stellate black spots passes, extending at
times over the dorsum. In Motella, as Mr Broox (No. 31, pl. ix. figs. 7, 8a; pl. x.
figs. 10, 11) has shown, black pigment occurs in definite patches; and after the embryo
has emerged, this definite aggregation of the spots produces a very remarkable appear-
ance (Pl. XVII. fig. 2).
In the few species of Pleuronectidee as yet investigated, certain common features are
noticeable, viz., the general occurrence of yellowish pigment (vide Pl. V. fig. 6; Pl. XVI.
figs. 1, 8, 5,6; Pl. XVIIL figs. 1, 2; Pl. XIX. fig. 5), and im later stages the presence
of two distinct colours (Pl. V. fig. 6; Pl. XVI. figs. 1, 3, 5; Pl. XVIII. figs. 1, 2).
On the fifth day (120th hour after fertilisation), when twenty-two to twenty-five
protovertebre in the common flounder are marked off, pigment of a pale brown tint,
yellow by transmitted light, occurs on the sides, especially along the median lateral line.
Twenty hours later, black spots, very minute in size, appear, intermingled with scat-
tered yellow spots over the trunk and tail. The yolk, however, is devoid of pigment.
Pl. XIX. fig. 5, shows the arrangement of the yellow pigment at the time of hatching.
In examples at an advanced stage, e.g., twelve or fourteen days after hatching, a
remarkable distribution of these spots is exhibited (Pl. XVI. fig. 1). The brownish
yellow spots extend above the mid-brain (mb), around the eyes, along the mandibles,
and over the abdominal region ; but are especially aggregated along the dorsum upon
each side of the median fin. The peculiar patches of radiate or stellate yellow spots which
appear midway along the embryonic caudal fin-membranes, dorsally and ventrally, will be
described in a subsequent page (see Median Fins). Radiate black spots also occur
amongst the yellow pigment.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 791
The dab (Pleuronectes limanda) has a distribution of pigment similar to that in the
flounder, though the yellow spots seem to take a more distinctive linear disposition, two
lines running along each side of the embryo, the upper line marking the dorso-lateral limits
of the neurochord (PI. V. fig. 11). This distribution is well seen when the embryo is viewed
from above. Pigment (yellow) appears when about thirty protovertebra are outlined
(i.e., about the seventh day after fertilisation). On the fourteenth day (two days after
emerging) the pigment-spots around the margin of the eyes and the otocysts coalesce to
form larger patches, irregular in form. A few days later, the upper lobe of the caudal
membrane is diversified by the development of an undulating line of yellow pigment, or
rather of a linear series of crescentic patches. Other spots occur thickly in the anal region,
but the yellow pigment of the trunk is confined for the most part to two lines, as above
described (Pl. XVI. fig. 6). In a more advanced embryo, thirteen days after extrusion,
the crescentic series of patches in the caudal fin is still more boldly marked, while two or
three irregular touches appear on its lower lobe. The stellate pigment-spots are now
meagre, occurring, as in the earlier stage just described, over the eyes, along the ventral
region, over the greatly diminished yolk-sac, and very sparsely on the tail. The eyes
have become darker, by increase of their black choroidal pigment, and about this time
they show a striking green lustre in oblique light (Pl. XVI. fig. 3).
In the plaice (Pl. V. fig. 6) black pigment-spots, mingled with finely stellate
bright canary-yellow corpuscles, develop, though comparatively late, and when the embryo
is freed it does not show the marked pigmentation of the cod or like forms. On the
third or fourth day after emerging yellow pigment appears as very minute amorphous
spots. In Pl. XVI. fig. 5, the peculiar distribution of the two tints is seen. The head
and trunk present very minute, scattered spots. The ventral margin of the alimentary
tract shows stellate black spots ; while the upper and lower contours of the caudal region
have bold lines of stellate spots, which extend to the caudal fin-membrane, though con-
fined to the lower lobe, and here the spots are simple and very minute. The yellow
pigment appears only as a narrow area towards the end of the tail, viz., the upper
margin of the posterior half of the caudal trunk. At the root of the tail a dense patch
of black spots occurs, extending obliquely just above the urinary vesicle.
Pigment appears in the gurnard at a slightly later stage than in the foregoing forms,
It consists of very pale yellow spots, which have a delicate sea-green tinge in certain
lights. They are sparsely scattered over the trunk proper, but form a rude line along
the dorsum, and an undulating line along the sides and around the eyes. Three or four
days later minute black spots occur, and both colours are sparsely distributed over the
yolk-sac, and around the large oil-globule. A more advanced embryo is seen in Pl. XVI.
fig. 8, at which stage irregular patches of yellow and black pigment exist upon the
dorsal and ventral portions of the caudal membrane. The spots send out branched
ramifying processes, and the pectoral fin exhibits distally a radial yellow and black
coloration. The eyes, however, are very slightly tinted with minute black spots. In
still later larval and post-larval stages the pigment diminishes, and only occurs very
792 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
-
sparsely in linear areas along the summit of the head, the opercular region, and on the
snout. In form the spots are amorphous or rudely stellate. Along the huge pectoral fins
and the ventrals similar minute corpuscles are developed, mingled in the former pair of
fins with yellow pigment-spots (Pl. XVII. fig. 5).
Certain features in the development of the pigment are noticeable, such as the fact that
in some Gadoids the spots are confined solely to the trunk (cod, haddock, and rockling),
(vide Pl. XVIL. figs. 1, 2); while in the whiting (PI. XVI. fig. 2), the sole and the ling
(Pl. V. fig. 9), the covering of the yolk (y) becomes richly pigmented. This pigmenta-
tion of the yolk-sac is a feature also in the gurnard (Pl. XVI. fig. 8), and in the latter and
the ling coloration is preceded by the appearance of colourless corpuscles, which are
scattered over the yolk-sac (wide Pl. XIX. fig. 9). Pale neutral tinted bodies, evidently
protoplasmic, and of various angular shapes, are distributed over the yolk-surface. They
send out pseudopodia, and become rudely stellate. In the ling this occurs on the fifth
day after fertilisation—about the time that the blastopore closes; and in the gurnard at
a similar stage these protoplasmic particles with short processes also appear. These
bodies are obviously only a cortical disposition of protoplasm—less delicate and complex
than the elaborate network of protoplasmic threads which extends over the yolk-sac in
the cod, haddock, flounder (Pl. XIX. fig. 5), dab (Pl. V. fig. 3), and other forms,
The pigment-spots which occur over the yolk-surface are beneath the cellular germ-
layer. They develop, as Ryprer has pointed out, in the non-cellular periblast ; and Cun-
NINGHAM, while noting this condition, viz., that ‘ they are situated at the surface of the
periblast,” in Plewronectes microcephalus and Scomber, states that in the latter species the
pigment is confined to the deep surface of the oil-globule and the sides of the embryo.
If the large multipolar corpuscles in the ling and gurnard be merely the nodes or
thickened points of intersection for the protoplasmic threads crossing over the whole yolk-
surface, it is remarkable that these points of intersection should not develop pigment in
the cod and dab, whereas they apparently become the pigment-spots of the yolk-sac in
the ling and gurnard. The actual transformation of the colourless corpuscles into
pigment-spots was not observed, but it is very probable.*
The pigment-spots of the embryonic trunk often form distinct papilliform projections,
the growth of the corpuscle pushing the epiblast out, and forming a small mound at that
point. If the development of a pigment-spot be followed in the ling or gurnard (vide PI.
V. fig. 2), we see a rounded or irregular particle of clear protoplasm superficially placed
upon the yolk-surface, which shows amceboid movements, and sends out blunt processes
(Pl. I. figs. 8a, 8b). These processes become bifurcate, and assume a more or less elabo-
rate ramose disposition—a stellate corpuscle being the result (PI. V. fig. 2b). In the
* In Gastrosteus Kuprrer speaks of the appearance on the yolk-surface of small nuclear bodies, from which he says
not only pigment, but blood-corpuscles are formed. These nuclei, probably the nuclear bodies already referred to in
the allied marine species (p. 55), which become radiate in form, develop pigment-particles, the others keep their
original shape until they are set in motion by the establishment of a blood-circulation (No, 88, 1868). In Gastrosteus
spinachia, the yolk-cortex, even before the blastopore closes, presents a striking appearance on account of the large
translucent nuclei which are scattered all over it. These nuclei often show many nucleoli (vide No. 124, p. 493), and
in the freshwater species, (, aculeatus, a reticulation is also present, but this has not been observed in G@. spinachia.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 793
centre a nuclear portion (7) can be made out, and this usually remains clear and un-
changed, while around it very minute particles of black pigment (pt) develop. These
particles increase so rapidly that the bases of the pseudopodia become much darkened,
and a centrifugal transference commences, the minute particles flowing along the ramify-
ing arms, until a pale steel-tinted stelliform body becomes distinctly outlined. The tint
grows in intensity, and finally shows the dense black colour characteristic of the completely
developed corpuscle. In many cases by their extension these black corpuscles intermingle
so as to interlace their arms in a complex manner, and even coalesce, as was noticed by
LEREBOULLET, who also observed the persistence of the central pale nucleus in each
corpuscle (No. 93, p. 579).
The variations in the disposition of the pigment in different forms is noteworthy, and
its diagnostic utility has been already mentioned. The time at which pigment appears is
also remarkable. LeEREBoULLET found in Perce that it develops earlier and more abund-
antly than in sox, though in both forms it overspreads the yolk-sac (No. 98,
pp. 579-586, 610). It is very precociously developed in the flounder, and comparatively
late in the whiting.
During the later larval stages the epidermis becomes very irregular—rounded pro-
tuberances appearing especially over the cranial and facial regions (Pl. IX. fig. 3; PI.
XVII. fig. 4). Many of these are sensory enlargements, and described elsewhere, but
enlarged mucous cells develop, especially in the region of the snout. These open
superficially, and doubtless are protective in function—bathing the young embryo exter-
nally with a gelatinous secretion. The contents of these large mucous cells stain very
deeply, and are especially noticeable in sections of the plaice, though in Cyclopterus and
others they also form a noteworthy feature.
No cilia are apparently developed upon the embryonic integument, nor do fine
immovable hairs occur as in Petromyzon and its young stage—Ammocates. The serial
sensory papille (Pl. VI. figs. 8, 87) send out fine filiform processes (plp), but they are
local, and probably pushed through from the neurodermis below. The development of
scales as protrusions from the corium which burst through the epiblastic integument, as
well as the formation of iridescent plates in the stratum Malpighii, belong to a late post-
larval stage. In some young forms, it is true, a brilliant iridescent appearance is seen in
the abdominal region ; but this is occasionally due to the enlarged swim-bladder, the fishes
in certain cases remaining translucent, and almost colourless in the post-larval stages, when
all the more important structural features of the adult are assumed. In such forms, again,
as the post-larval Anarrhichas, the whole abdomen is iridescent.
Ova and Generative Organs.—As soon as the segmental ducts have reached their
final position on each side of the dorsal aorta, a strand of peritoneal (splanchnopleuric)
cells passes below them. They thus become grouped on the inner side close to the
mesentery (Pl. VII. fig. 1). These cells become aggregated, and produce an irregular
contour especially in the posterior region—where the alimentary canal is more distant
from the notochord, and the median mesenteric membrane is better developed. They
VOL. XXXV. PART III. (NO. 19). 61
794 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
form, in fact, the germinal epithelium, but a definite germinal ridge cannot be made out.
Indeed, in the haddock, it is not until the second or third week after extrusion that this
germinal portion becomes distinctively marked (Pl. XI. fig. 14). Some of these cells
(po) are seen to enlarge and protrude from the surface of the mesentery (msn) into the
abdominal cavity as large primitive ova, and they occur, almost solely, slightly anterior
to the urinary vesicle, especially above the region of the small intestine. In short, their
appearance and distribution precisely accords with Batrour’s description of the early
Elasmobranch ovum (No. 15, vol. xi. p. 161). The ova are most closely grouped on
the roof of the abdominal cavity, and especially in the median niches formed by the
projection of the suspensory septum or mesentery (msn). They are also grouped upon
the mesentery, and some develop upon or have migrated to the peritoneal envelope of the
intestine itself (hg). They are very irregularly distributed, and show great variation in
size ; large spherical ova projecting from a mass of small undeveloped cells, and all
loosely held together by the delicate connective tissue of the peritoneum. The ova
appear to be like the cells adjacent, and differ only in their larger size and more active
development. Each consists of a mass of minute nucleated spheres enclosed in a thin
membrane ; but are quite unlike the primitive ova of Elasmobranchs, as described by
Batrour (No. 13, p. 164), for these latter are uninucleate, one or two nucleoli, stain-
ing deeply, occurring in the nucleus, which is large, and surrounded by a granular
protoplasmic matrix. Along each side of this region of the abdomen, external to the
abdominal cavity, a mass of cells may occur, not unlike, but less in dimensions than, the
primitive ova described above. The lateral niche in which they are aggregated is defined
by richly pigmented peritoneum, and this pair of lateral sacs strongly suggests the
ovaries of the adult. The largest ova are those, however, which are free, and project
boldly from the mesentery and roof of the abdomen. Ba.rour speaks of a thickened
germinal epithelium in the Teleosteans, into which the adjacent stroma sends ingrowths—
the cells of the epithelial layer increasing by the growth of the clear protoplasmic
contents. But this does not correspond with the condition seen in the young haddock,
each ovum being a more or less perfect sphere, and enclosing numerous minute
nucleated bodies. Later stages were not observed, and it was not made out whether the
lateral peritoneal sacs finally became the ovaries with their continuous genital ducts, or
whether an epithelial layer grew over the freely suspended primitive ova, and enclosed
them in an ovarian sac, depending from the abdominal roof.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 795
IX. Tae Fins.
Median Unpaired Fins.—The development of a median epidermal crest (ef, Pl. V.
fig. 11; Pl. XIIL fig. 3; Pl. XIX. fig. 10), extending along the median dorsal line from
the cephalic region round the end of the tail, and along a portion of the under surface of
the caudal trunk, is an early and noticeable feature in the embryos of Teleostean fishes,
with probably few exceptions (e.g., Hippocampus). Soon after the tail is detached from
the yolk-surface, within a day or two after the closure of the blastopore, a minute fold of
epiblast projects as a ridge along the whole course just indicated. It grows in vertical
breadth, being pushed out in the form of an epiblastic fold, and shortly before the extrusion
of the embryo is quite a broad membrane, especially well developed in the hind trunk and
caudal region. On account of its superficial extent—while the embryo is within the egg
—it is creased and much folded about the body; but on the embryo issuing from the
ovum the membrane rapidly straightens out and becomes erect. It apparently continues
to grow after extrusion, a newly hatched embryo having a much less extensive median
membrane than one a few days old (compare Pl. XIX. fig. 5; Pl. XIII. fig. 6; Pl. XVI.
fig. 1). The extent covered by this fin (ef) varies in different species, thus in the young
of Trigla gurnardus (Pl. XII. fig. 1) it never extends quite so far forward as in the forms,
e.g., Gadus eglefinus (Pl. XIV. fig. 1), G. morrhua, G. merlangus (Pl. XVI. fig. 2), and
Motella (Pl. XVII. fig. 2); its wider portion in fact reaching only to the otocystic region,
in front of which its height gradually diminishes, and the fin disappears above the
occipital region (P]. XVI. fig. 8). In such examples as the Gadoids just mentioned, it is
broad and prominent as far forward as the mid-brain, in which region it gradually
slopes toa mere ridge. The thinness and transparency of this structure is remarkable.
It is so delicate that as the fish progresses through the water it is flexed and waved
about with every movement, and on removal from the water the fin collapses at once,
and lies like a film on the body. Slight contact with a hard substance immediately
injures it, and while in healthy larve it stands out erect and even, and is _per-
fectly translucent, it appears crumpled and in many parts opaque when the fish is
in a sickly or dying condition, ultimately dissipating or breaking up into needle-like
fragments.
In certain forms, e.g., Gadus merlangus (Pl. XVI. fig. 2), Molva vulgaris (Pl. XVIL.
fig. 9), and Solea vulgaris (Pl. XVIL fig. 13), the pigment, which extends not only over
the body, but over the yolk-sac, appears also upon the embryonic fin (ef) ; whereas in
Gadus morrhua, G. eglefinus, &c., no such pigment-corpuscles occur save on the trunk
of the fish—the yolk-sac as well as the membrane being destitute of them. It was men-
tioned previously that in Plewronides limanda (P). XVI. figs. 3, 6) and Trigla gurnardus
(Pl. XVI. fig. 8) the fin shows during the later larval stages remarkable coloration
—in the former species crescentic particles of yellow pigment appearing in regular series
along the membrane above and below the caudal trunk during the second week after
796 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
hatching, while in the gurnard a third-day embryo shows irregular patches of yellow pig-
ment, with which black spots are also mingled (Pl. XVI. fig. 8). The coloration in other
species will be noticed on a following page.
In transverse section this fin-membrane (ef) consists merely of a simple median fold
of the double-layered epiblast—the outer flattened corneous layer, and the inner sensory
layer, which proceeds into the narrow fissure separating the two lamellae of the fin
(Pl. VIL. figs. 3,6). This fissure enlarges close to the trunk, and is continuous with a
spacious subepidermal chamber which extends all round the latter, and is well seen in
late larval stages in section (PI. VII. fig. 6) and surface view (PI. XVI. figs. 1, 3). A jelly-
like lymph fills up this cavity, which, as already pointed out, becomes extraordinarily
enlarged in the cephalic region. All along the trunk such a space exists in a modified
degree, and delicate nerve-strands pass across it from the spinal cord to the sensory
papille in the skin. Along the tail the interspace is narrowest (ss, Pl. XI. figs. 15, 17),
but on the ventral side, as the root of the tail is approached, it enlarges and forms a
spacious fissure in the anal region (ss, Pl. XI. fig. 14). It is in this chamber, limited
on each side by the epiblastic fin-fold, that the rectum (ig) pushes its way, and before
the anus is formed sends out a strand of loose cells, extending from the base of the
urinary vesicle to a point midway down the expanse of the fin-membrane.
The hind gut, as already indicated, ends blindly, and does so for a period varying
very much according to the species. The anal column of cells, before and after a
lumen is formed, passes down the centre of the fissure (ss), and is apparently held in
place by the tenacious plasma (, Pl. VII. figs. 12, 13), in which granules subsequently
appear, and forms a matrix surrounding this part of the intestinal tract. As formerly
mentioned, the anus does not extend to the ventral margin of the fin, but opens at the
side about midway (a, Pl. VII. figs. 14, 15). In this continuous embryonic fold the
permanent unpaired fins of the adult fish are formed—arising, as Barour said, by local
hypertrophy (No. 11, p. 78), though no less by atrophy of the parts between the
ultimate fins. LEREBOULLET refers to this atrophy in Perca, when he says the margin
becomes indented where the three vertical fins in that species will finally remain
(No. 98, p. 634). These local indentations mark the atrophy of parts of the embryonic
membrane, which finally disappear, leaving the prominent and strengthened remnants
of the once continuous fin to form the permanent unpaired fins. Before this atrophy
of the transient portions and the hypertrophy of the permanents parts, the sites of the
ultimate fins often appear to be indicated by remarkable aggregations of pigment. Thus,
in the advanced embryo of Plewronectes flesus, a striking development of pigment-
corpuscles takes place in the dorsal and ventral portions of the embryonic fin. Scattered
pigment occurs along its whole extent behind the pectoral region, though it is sparse ;
but certain parts in an early stage are distinguished by more abundant coloration, and
in the thirteenth-day flounder, referred to, a patch of brownish-yellow pigment-spots,
arranged in a radiate manner, is seen with black spots intermingled (Pl. XVI. fig. 1), as
also in the undetermined Pleuronectid figured on Pl. XVIII. fig. 1, and in Agonus on the
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 797
same plate, fig. 11. A similar dorsal and ventral arrangement of caudal pigment-spots
occurs in the advanced embryo of the ling (Pl. XVIL. fig. 10), black pigment-spots
diverging upward and downward from the caudal trunk in a characteristic manner. In
this way the sites, so to speak, of the future median fins are indicated by radiate
coloration before the continuity of the embryonic membrane (ef) is to any appreciable
extent destroyed. Later, however, the developing fin-rays (embryonic) are more clearly
indicated by granular striations which pass across the membrane (vide Pl. XIII.
figs. 2, 6a; Pl. XV. figs. 4, 5), still very thin and transparent (though a fine reticulation
of a superficial character often appears in it), no mesoblast having as yet insinuated
itself into the interlamellar fissure, as shown in a section of the haddock on the
third day after hatching (Pl. VII. figs. 3, 4). or even so late as the seventeenth day
(Pl. XI. fig. 14). LeresouLLer noticed similar indications in the still persisting
membrane of the embryo of Pevca when twelve to fifteen days old. He describes along
its whole length small irregular transparent structures like oil-tracts, and he found that
they accumulate where the permanent fins will be developed (No. 93, p. 640). These
are either the homologues of the pigment-corpuscles mentioned above, or aggregations of
the external reticulation. Later, he says, he noticed these disappear in Leuciscus eury-
ophthalmus as if by absorption, and striations inclined in a backward direction take their
place. They form successive pairs, the rudimentary rays, in fact, of the unpaired fins,
which he remarks are double at the time of origin (p. 640). Ryper speaks of the
mesoblast as entering the fold at an early stage (No. 114, p. 517),* but this does not
apply to many forms, for a section through an advanced embryo of the haddock, as just
mentioned (PI. XI. fig. 14), still shows a mere epiblastic fold (ep) little altered from its
primitive condition. While the membrane still remains thin and translucent, ray-like
thickenings are frequent—apparently aggregations of a horny or chitinous nature, usually
regarded as epiblastic thickenings, which develop, as LEREBOULLET observed, centri-
petally, and grow towards the trunk (No. 93, p. 637). He describes them as transparent
strips, distant from, but directed towards the body, and appearing simultaneously in the
three parts which subsequently form the three vertical fins in Leuciscus ewryophthalmus.
These rays LEREBOULLET describes as formed by a “condensation of a plastic material
without any grouping of cells,” and he regards them as connected with the vertebral
column below from which they are separated, subsequently, by the interspinous bones
(p. 630). In reality, however, the early rays are merely dermal thickenings, and appear at
first as narrow granular tracts indefinite in outline, and extending dorsally and ventrally,
and therefore unconnected with the axial skeleton below. LereBouLLet’s view applies
to the dense permanent rays which develop in the post-larval stages, for these rods
are paired, and arise under the epiblast—beneath the pigment, which appears in the
Malpighian layer of the ectoderm, and are most probably aggregations of mesoblastic cells
which grow up into the median fin-fold from the axial (skeletal) mesoblast below. In
* Ryper now holds that even the embryonic fin-rays are mesoblastic (Rep. U.S. Comm, Fish and Fisheries, 1884).
As fast as they appear, they are preceded or accompanied by outgrowths of mesoblastic cells.
798 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
the embryos of species with pelagic ova, eg., Gadus morrhua, G. eglefinus, G. mer-
langus, Molva vulgaris, Trigla gurnardus, and the Pleuronectide, such median fin-
rays do not appear even in the late larval condition (ef, Pl. X. figs. 1, 4; Pl. XVII.
figs. 2, 10, 12); and Ryper instances other examples, some having demersal ova, e.g.,
Alosa, Pomolobus, Cybium, Parehippus, and Idus, in which this is so (No. 141,
p. 518), the original transparent membranous condition of the embryonic fin persisting
to a late stage. Ryper adds that in Gambusia and certain Lophobranchs no embryonic
fin-fold is formed at all—the single dorsal fin arising later as a local dermal excrescence
with a core of intruding mesoblast (No. 141, p. 518). In some Cyprinoids (Jdus and
Carassius), which also possess a single dorsal only, the continuous embryonic membrane
nevertheless appears. Pl. XVIL. fig. 5, represents a young gurnard in which the two
dorsals and the single anal fin (af) are indicated; but the former are still continuous
with the tail-membrane (cf), while a remnant passes forward to the anal fin. The stage
figured is post-larval, and in Pl. XVII. fig. 7, the fins have really reached the adult
condition, and are completely differentiated, all trace of the continuous embryonic mem-
brane having disappeared. In Pl. XV. fig. 6, representing Cyclopterus lumpus, these
intermediate connections are still discernible, though the two dorsals (df) and the
anal are almost wholly separated. These unpaired fins have become conspicuous
by hypertrophy at three points, and by the atrophy of the membrane in front and
behind (see also fig. 5). The ventral median fin is broken up into two by the anus (a),
which, e.g. in Gastrosteus, has pushed its way down and terminates at the apex of an angular
bay marking off a pre-anal from a true anal fin (PI. XV. fig. 5). LereBouLter describes such
a bay in the newly emerged embryo of Perca, while the body is still encircled by the con-
tinuous fin, “ the lower edge,” he says, “ exhibits an indentation where the anus will appear ”
(No. 93, p. 616). This condition differs very much, it is unnecessary to point out, from
that in the newly hatched embryos of the species here described. A post-larval flounder,
5°8 mm. in length, which is perfectly translucent and colourless, but has lost almost every
embryonic trace, still retains a membranous vestige connecting the dorsal above and the
anal below with the caudal fin. The three fins thus connected have otherwise attained
all the characters seen in the adult.
The unpaired fins in Teleosteans, therefore, do not arise as two apposed, independent
epiblastic plates, but as a median fold or crest.
Prof. Humpury first broached the idea, from an examination of the adult anal fin,
that it might be double in its origin, 7.e., 2 union of two lateral fins ; and he suggested
that the other median fins might have thus originated, and that the paired and unpaired
fins were alike double primitively (No. 72), a view supported by the fact that the dorsal
fins, in addition to their (spinal) motor nerves, are supplied by a pair of sensory nerves
which branch off from the trigeminal soon after it emerges from the roof of the skull.
The study of their development, however, would seem to yield an opposite conclusion—
the median fins are single at their origin,* and their bilateral strueture—muscular and
* LEREBOULLET's statement that the dorsal fin is double at its origin is likewise misleading (No. 93, p. 630).
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 799
skeletal—is subsequently assumed, and it must be added the paired sensory (nerve) con-
nection, above mentioned, is probably also secondary, for in Selachians and Dipnoans no
trace of it is seen. It is remarkable that in some forms, e.g., Apeltes, vascular loops are
formed in the median fin-folds at the time of hatching, whereas in none of the species
specially referred to in this paper is this the case—the membranes remaining transparent
and non-vascular for some time after extrusion.
The Caudal Fin.—It is plain from the foregoing observations that the tail of the
embryo is not by any means distinctly marked off from the trunk. The tail is indeed
the tapered portion of the trunk, which gradually diminishes, ending posteriorly as a thin
rod (the notochord with the muscle-plates on each side), and the neurochord above (cf. Pl.
XIII. figs. 1, 2, 4, 6a, 7). A strand of connective tissue passes along beneath the rod,
and in this tissue the hzemal trunks of the tail are by and by formed (vs., Pl. VIL. fig. 6a;
Pl. XI. figs. 15, 17). The whole is encircled by the embryonic fin-membrane (ef)
which passes along the median dorsal, terminal, and ventral line, so that the tail is at
this early stage of the typical protocercal type, showing no division into lobes. In the
early ling, about the time that the eyes are fairly complete, two peculiar folds are sent off
below the muscle-plates in the caudal region. While within the ovum the caudal trunk
lies for some time as a flattened process upon the yolk, its greatest breadth being at right
angles to the caudal plane of symmetry, and when first it buds out from the trunk it
is ina state of torsion, the developing fin-membrane being folded in a complicated manner
at the root of the tail, and passing as a horizontal ridge round its termination (PI. II.
fig. 11). This state of torsion, which is very marked in the earliest condition of the tail,
does not continue, and shortly before hatching the enlargement of the preivitelline space
not only gives the caudal trunk more freedom, but even permits active movements on
the part of the embryo.
Usually, as pointed out above, the trunk terminates in a more or less accuminate
process (Pl. XIII. figs. 1, 2, 4, 60,7); but in Pl. XV. fig. 4, a remarkable terminal
enlargement is seen, the neurochord swelling to form a lobe, while the notochord ends in
an irregular bulbous structure. In the figure just referred to (Pl. XV. fig. 4) the tail-
fin proper is marked by a radial structure (embryonic fin-rays), apparently a mere
dermal thickening, such as we see in a late stage of Pleuronectes limanda (Pl. XVI. fig.
3). In PL XIII. figs. 6, 6a, the embryonic membrane is diminished between the ter-
minal caudal and anterior portions, and a mass of granules is forming around the end of
the notochord, which assume a radial disposition. ‘These diverging granular tracts are
better defined, and form, in fact, rays in the dorsal and ventral lobes of the membranous
fin of the same embryo (PI. XIII. fig. 7). The formation of fin-rays, without the
intervention of special cellular prolongations from the vertebral arches, was observed by
LEREBOULLET, who speaks of them as produced probably by “ the deposit of a cartilaginous
cytoblastema” (No. 93, p. 634). The appearance of these rays does not suggest a
cartilaginous character, the fine granular tracts (PI. XV. fig. 5), as they become defined,
form clear translucent rods (Pl. XIX. figs. 2-4), not unlike the “spicular substance,”
800 PROFESSOR W. C. M‘SINTOSH AND MR E. E. PRINCE ON
which appears in certain parts of the axial and appendicular skeleton (e.g., vertebral
bodies and pectoral arch). Most probably they are of a resistent horny (?) nature, and
they are developed at first in the distal or mid-part of the fin-membrane, approaching,
as before pointed out, the trunk by the growth of the proximal end of each ray, “ their
development being in conformity with M. Serres’ law of centripetal formation” (No. 93,
p. 634; also vide Serres’ Principes dorganogénie, Paris, 1842, p. 212). As the rays thus
develop, the aboral end of the cellular notochord (nc) curves upward (Pl. XVIII. fig. 3), the
upper lobe (opisthure of RyprEr) diminishes, while a new and larger lobe expands on the
ventral side of the chorda. A notch, however, separates this new growth from the lower
lobe of the primary protocercal tail (PI. XIX. fig. 4).* AGassiz describes this development
of the secondary caudal membrane as an atrophy of the upper lobe, and a rapid
development of the lower lobe which becomes bifid. The lower lobe does not really
become bifid, but a new lower or rather anterior ventral lobe grows out, and by its
rapid development leaves a notch separating it from the primary lower lobe. The two
original lobes of the protocercal tail are gradually pushed further up and almost entirely
disappear, the tail of the adult being for the most part a wholly new growth on the
ventral side of the notochord, and slightly anterior to its termination (compare figs. 3 and
5, Pl. XVIIL). The stages of this atrophy of the primary fin-lobes and the growth of the
secondary tail-fin, mainly as a new product, can be seen by comparing Pl. XVII. fig. 3,
which shows the original protocercal outline, with fig. 6 on Pl. XV., in which the
secondary tail-fin is formed as a large ventral lobe supplanting the primary tail.
In fig. 5, Pl. XVIL, the new tail-fin has completely taken the place of the primary
membrane. Pl XVIIL, figs. 3, 4, 5, and 7, show these stages well. The embryonic tail with
its dermal rays is transitory, and the permanent tail with its hypural elements (Pl. XV.
fic. 3) belongs to a stage which is post-larval. LEREBOULLET says the materials out of which
these later skeletal elements are developed are furnished by a rich caudal plexus of blood-
vessels. This complex vascular development, he says, ‘precedes and announces the
formation of the tail,” and it consists of a system of elongated loops in the pike, perch,
trout, and roach (No. 95, p. 26). No such subnotochordal terminal plexus is formed in the
Gadoid and other forms studied at St Andrews. Thus the gurnard, even at so advanced
a larval stage as Pl. XVII. fig. 5, shows no such network; yet the hypural plate is well
developed and the fin rays fully defined.
The Paired Fins.—When the embryo is first outlined in the blastoderm, an alar
expansion stretches away on each side of the trunk of the young fish. This expansion
consists of epiblast and hypoblast resting upon the stratum of periblast below. No
* Ryper (“ Evolut. of Fins of Fishes,” Report of Com. Fish and Fisheries for 1884-1886) states that there is evidence
of the degeneration of the caudal region, as in Chimera and Stylephorus there is a permanent archicereal opisthure, a large
temporary one in Lepidosteus; and, moreover, there is the evidence of the concrescence of the hypural pieces; the
ventrally diplacanthous and even triplacanthous caudal vertebra, or their coalesced representative, the urostyle ; the
existence of hypaxial opisthural elements ; the abortion of the epaxial spines of the caudal vertebra ; and finally, the
abortion or extreme modification of the last muscular somites of the caudal region. Ryper (op. ectt., from an examina-
tion of the eel) holds that the hypurals are partly heemal and partly interspinous.
+ See Lorz on “Tail of Salmon,” &c., Zeitschr. f. wiss. Zool., 1864, p. 260.
+
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 801
mesoblast apparently extends into it (a/, Pl. II. figs. 11-13; Pl. IV. figs. 4, 10),
though this layer is ill-defined laterally at this stage. A pair of lateral horizontal ale
(a/), indeed, stretch along the whole trunk—from the pectoral to the post-mesenteric
region. It is in reality the elongated and narrowed blastodermic scutum (Pl. XXVIII.
fig. 5), and extends in front and behind the two points mentioned, though it is there
thinner and hardly distinguishable. In Pl. III. fig. 19, such a pair of lateral horizontal
fin-expansions are present extending from the trunk-region proper, and their limits
are very definite when viewed from above. Just as in the case of the median vertical
fins, certain areas in these horizontal alze become defined, as special fin-regions by a
visible thickening, apparently from the folding under of the epiblast. Thus two flattened
oval pads consisting of a double epiblastic fold like the double median fin-fold, are
disengaged from the rest of the alar expanse. Before and behind this pair of pads the
lateral membrane thins away and atrophies, while the special portions continue to increase
in density as a pair of pectoral limbs (pf, Pl. V. figs. 6,9; Pl. XIV. fig. 1). LereBouLLer
apparently did not notice that the pectoral fins emerge from the lengthy lateral mem-
brane or alar expanse on each side, and speaks of a gradual accumulation of cells from
the inferior lateral portions of the trunk as a pair of tubercular processes protruding
some distance behind the ears. In Perca he found that these fin-pads became detached
on the seventh day (No. 95, p. 10; No. 93, p. 583). The increasing density of the fin-
pads is due to the entrance of mesoblast into the interstice, separating the upper from
the lower epiblastic lamella. This mesoblast spreads out radially, but does not reach
quite to the distal margin, and the peripheral portion remains more transparent, though
the epiblastic cells which solely constitute it become columnar, and form a thickened
ridge from which the fin-rays doubtless subsequently develop centripetally.* Such a
mode of development as that above sketched has theoretical bearings of considerable
interest. These were briefly treated in a former note (vide No. 124a, p. 697), and need
not be discussed in this place further than to point out that the fin develops as a
horizontal ridge, in accordance with Barour’s theory of a primitive horizontal lateral
fin, and that it is independent of and prior to the formation of a girdle-rudiment. Prof.
CLELAND, in a paper on the Limbs of Vertebrates (No. 40), emphasised this latter point,
and further showed that a limb involves two distinct elements—a radiation (7.e., an
appendix) and an arch, which is not a radiation, but a cincture, which always circles more
or less round the body, and may be complete above or below. Prof. CLeLanp further
stated that neither appendage nor limb-arch is the property of one particular segment,—
their position being variable and their nervous supply multisegmental,—points which are
* Kinestey and Cony, in the cunner (Zautogolabrus adspersus, Gill), and other authors in various forms, have
recognised only the lateral fins when they were defined as tubercular pads. The observers named speak of these fins
as only developed when the embryo is ready to emerge—the tail being free and the capsule loosely surrounding the
fish (vide No. 78, fig. 51, pl. xvi.). No trace of a continuous lateral fold could be seen, the fins protruding as simple
outgrowths (p. 210). The extension of the thickened epiblast and hypoblast laterally is, however, a feature common
to all Teleostean embryos, and a portion of this becomes defined in all the forms studied at St Andrews, and out of
this defined epiblastic fold the pectoral fins arise.
VOL. XXXV. PART III. (NO. 19). 6K
802 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
supported most clearly by the development and early condition of these structures in
Teleosteans.
From the primary horizontal position (pf, Pl. V. figs. 4, 6, 9; Pl. XIX. fig. 7),
the fins change to a more vertical situation (pf, Pl. XIII. figs. 1, 6; Pl. XVI. figs.
6, 8), though still connected by a lengthy attachment to the side of the embryo. The
mesoblast of the fin-plate may be traced to a mass of cells in which the Wolffian ducts
Jie, and out of which they are developed (Pl. VII. figs. 1, 2). If these ducts, as appears
to be the case, arise as lateral ridges or diverticula of the somatopleure, then the meso-
blastic cells of the fins must be pronounced somatopleuric. But no ridge of somatopleuric
cells, comparable to the Wolffian ridge of higher forms, has been recognised in fishes, and
we must regard this mesoblast as indifferent, and forming an “intermediate cell-mass”
adjacent to the excretory system. The proximity of the Wolftian duct and the base of
the pectoral fin is very noticeable (Pl. VII. fig. 7). The fins gradually become dis-
connected from the blastodermic yolk-sac, and about the time that they are free a median
stratum in their mesoblast assumes a columnar character, and is seen as a transversely
striated central bar in cross-section (x, P]. VII. fig. 2). This plate (@) is gradually con-
verted into cartilage, and extends from the base of the fin, where it is thickened almost to
the distal border, at which it thins out and ceases (Pl. VII. figs. 1-3). Around this fan-like
cartilaginous plate the adjacent mesoblast develops rapidly, especially near the proximal
attachment to the trunk, so that a stout peduncle is formed (Pl. VII. figs. 1, 2).
Viewed from above, in the living embryo, the fin appears as in Pl. VII. fig. 10, the outer
and anterior margin presenting many protoplasmic processes, which seem to bind it to
the epiblast over the yolk. The pigment-corpuscles, moreover, may be regularly disposed
on the fin. Each fin, therefore, consists of a thickened stalk and an outspread distal
expansion (pf, Pl. XII. fig. 6a), traversed from the base almost to the summit by a
flattened plate of cartilage which is imbedded in a mass of indifferent mesoblastic cells,
destined to become the muscles of the limb, and forming the main mass of the peduncle
(Pl. VIL. fig. 7). The basal part continues to become thicker, and later is disproportion-
ately enlarged, while at the same time the more distal parts expand like a fan, and
become thinner and more transparent, save where the delicate radial striations pass.
The part towards the distal border in many forms quickly exhibits pigmentation, e.g., in
T. gurnardus (Pl. XII. fig. 1), Molva vulgaris, Cottus, and Liparis, radially disposed
yellow and black pigment-spots being intermingled in the distal parts of the fin in the
first-named species (Pl. X. figs. 2,3; Pl. XVI. fig. 8), or again, rich orange stripes in
Liparis (Pl. XVI. fig. 7).
During the third week after hatching the “rotation” of the fin has reached a stage
at which its position is seen to be wholly altered, the original horizontal position (PI.
XII. fig. 1) being now exchanged for an oblique vertical attachment (Pl. XIII. fig.
1; Pl. XVL. figs. 3, 4, 7). The rotation continues until its basal attachment is almost
perfectly dorso-ventral, and therefore at right angles to its primary position (Pl. X. figs.
2, 3; Pl. XV. fig. 2; Pl. XVIII. figs. 2,10, 11). Meanwhile a pectoral bar appears
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 803
on each side of the thoracic region, extending dorsally and ventrally, forming in fact two
halves of the pectoral girdle as yet disjoined below. RypeEr distinguishes, before the
development of the cartilaginous girdle, an oblique pectoral fold (No. 141, p. 520), con-
sisting of a band of mesoblast, out of which, he states, the girdle develops. There
appears on each side, therefore, a clear yellowish rod, tapering at its upper and lower
extremities, and curved like an //—as in the gurnard on the eighteenth day (cl, Pl. X.
figs. 2, 3; also Pl. XIII. figs. 5, 6, 7). In- Pl. XI. fig. 18, this bar is figured as removed
from a larval Pleuronectid about three weeks old. The species was not determined. The
small triangular element attached, though not unlike the post-temporal, is probably the
coracoid bone. This secondary bar may be readily recognised by its form and position
as the clavicular element (c/), and it develops in certain species, as in the gurnard,
the Gadoids, and others, without being preceded by a bar of cartilage-cells, and in these
forms the basal part of the fin-cartilage is greatly developed, as if preparatory to inclusion
as a posterior part of the girdle. If the homogeneous, translucent, brittle rod, strongly
suggestive of chitin, be the clavicle, then the elements behind, which become attached to
it, must be the scapular and coracoidal portions of the permanent girdle. By the
breaking-up of the basal portion of the cartilaginous fin-plate the system of basilar
pieces is formed (Pl. XVII. fig. 5). Kinestey and Conn speak of this proximal car-
tilaginous thickening as parallel to the axis of the trunk, and as preceding the distal
rays. ‘This basal skeleton,” they say (No. 78, p. 210), “instead of appearing as a pair
of rods as described by Ryprer, was rather a broad plate with a central opening, as if
his rods had united at their extremities.” The same feature was also seen in Loplhius.
There is much obscurity in regard to the development of the ultimate elements of the
paired fins, and their relation to the axial girdles. The details of this further develop-
ment, with the theoretical considerations involved in their interpretation, have been
dealt with by one of us in a special paper.*
Ventral Fins.—The development of the ventrals will be alluded to when describing
the post-larval stages (vide Pl. IX. figs. 2,3; and Pl. XVIII. fig. 3). They are late in
making their appearance in the pelagic forms.
X. Mernops AnD TECHNIQUE.
I. MernHops.—The ova and embryos are treated according to the usual methods of killing,
fixing, staining, and cutting. Notwithstanding the large number of methods recommended by
various embryologists, the ova and early embryos of Teleosteans may still be counted amongst the
most difficult objects subjected to the microtomist’s processes. The recommendations of various
investigators are most conflicting, and a perfectly efficient and reliable killing, staining, and
imbedding process continues to be a desideratum. WuiTMAN, after trial of the usual hardening
agents, “failed to find any completely satisfactory method of preserving the vitellus; even the
germinal dise cannot well be preserved by any of the ordinary hardening fluids ” (No. 159a, p. 152),
and this agrees with the common experience of investigators.
* E. E. Prixce “On the Development and Morphology of the Limbs of the Teleosts,” Elizabeth Thompson
Fund, U.S.A.
804 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
The plan followed by Kuprrer (His and Braune’s Archiv Anat. Abth., 1882), HENNEGUY (Bull.
de la Soc, Philom., Paris, 1879, pp. 75-77), and others involve too many processes to be adopted when
the species studied are numerous, and the quantity of material is large.
Various circumstances conduce to render Teleostean eggs difficult objects for treatment—not
only on account of their small size, pelagic ova being rarely more than a millimetre in diameter—
but the tough nature of the capsule and fluidity of the contents render the removal of the former a
most delicate and hazardous task. If hardened before the capsule is removed, shrinking results ;
and if the capsule be removed before hardening, the egg is more or less disorganised, unless the
operator be very fortunate. The best sections are those gained by leaving the egg almost intact,
and by hardening, staining, and imbedding in toto, but this plan is beset by many dangers. On
removing the egg from the sea-water, and reference is made here to marine ova solely, the capsule
is carefully pierced in order to facilitate the admission of the various media into which it is to be
transferred. Save for this puncture, the egg is left entire, and thus it is passed through all the
processes of killing, hardening, staining, clearing, and imbedding.
The paraffin method proved to be the only practical one, other methods, such as imbedding
in pith, which might serve for large eggs, such as those of the Salmonide, were unsuitable
for eggs so small and frail as those of the Gadoids, Plewronectide, &c.* Various forms of the
microtome were used in preparing the extensive series of sections of the various Teleosteans
considered in these pages—the rocking microtome of the Cambridge Scientific Instrument Company
being found very useful. The large Caldwell microtome, used in the classes of zoology at the
United College, and kindly lent by the authorities of the University of St Andrews, was of great
service; while the Jung (Thoma’s) microtome was found to be well adapted for older stages of the
embryos, and for adult ovaries—a series of sections being eut by Dr Scuarrr. The sweeping
motion of the last-named instrument proved very efficient in cutting through the more mature
skeletal and other tissues of young fishes, to which task the fixed razor of the English microtomes
proved unequal—refusing, in fact, to pass through the firm connective and cartilaginous elements.
Il. Kiniie, Frxine, anp Harpentnc—Corrosive Sublimate.-—The saturated solution is one of
the most efficient killing and fixing fluids available in the laboratory, and it kills, fixes, and hardens
so rapidly that Teleostean ova require to be left in it for a very short time. As soon as the
penetration of the fluid is complete, they are removed and washed in dilute alcohol, rather than in
distilled water, Washing must be well done, in order to prevent subsequent deposition of crystals
in the tissues. The desirability of staining, clearing, and cutting after treatment with this fluid is
too well known to require any explanation—the best preparations being found to be those in
which, after killing and fixing, the subsequent operations are immediately proceeded with. A mix-
ture of two parts corrosive sublimate and one part acetic acid was found to be most serviceable. It
is a powerful killing and fixing fluid, and produces the best results. For killing, two or three
minutes usually suffice, and washing is then done in very weak alecohol—the alcohol being
frequently changed until the killing medium is wholly extracted, and graduated alcohols follow,
viz., 30, 40, 50, and 60 per cent.
Picro-sulphurie Acid (KLEINENBERG). This useful killing and fixing fluid does not produce
the best results, since it frequently causes the blastomeres in early stages to expand and burst the
capsule, thus entirely disorganising the embryonic structures. WHITMAN experienced the same
results (op. cit., p. 152), but occasionally this effect is not produced, and, if successfully killed and
hardened in this fluid, ova are often found to produce most satisfactory sections. It is, however, not
reliable. Creosote is added on KLEINENBERG’S suggestion, but apparently without much effect. If the
ova placed in picro-sulphurie acid maintain their normal shape, they remain four or five hours, and
then are transferred into 70 per cent. alcohol, which is frequently changed, as it becomes stained by
the yellow picrie acid. When the alcohol is seen to be uncoloured, the ova are then ready to
be transferred to absolute alcohol, preparatory to clearing. Emery recommends this fluid for
* Hennecovy used elder-pith soaked in alcohol and covered with a layer of collodion.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 805
hatched embryos, and it is certainly one of the best that can be used for killing and hardening
them.
Perenyi’'s Fluid (Chrom-nitrie Solution)—This fluid kills instantaneously, and preserves
Teleostean ova better than any other medium tried; but in the processes subsequent to hardening,
its action proves defective. The staining fluid is best added during the fixing process, borax-
carmine being mingled with the solution. Pelagic eggs preserved their form admirably, and
fixation was apparently most satisfactory, but staining was not very successful, and in the clearing
and imbedding processes the ova shrunk, and good sections were found to be impossible. With
some change in the mode of imbedding, this fluid would be most efficient. WHITMAN, however,
states that he obtained good sections “more instructive than any obtained from eggs hardened in
other fluids” (op. cit., p. 154).
Chromic Acid—The merits of this fluid for killing and fixing Teleostean eggs need not be
insisted on. It acts perfectly; but the long washing and difficulty of subsequent staining are
objections.
Osmie Acid.—Alone and in various combinations osmic acid is much recommended. The fatty
elements in Teleostean eggs, however, render it a doubtful medium, and no good results were ob-
tained. MArsHALL used it for the embryos of Seylliwm, which were placed in } per cent. sol. chromic
acid and a few drops of 1 per cent. osmic acid for twenty-four hours—thence into alcohol.
Chrom-Platinum.—This mixture is said to be admirable for fixing, but Wairman found that
embryos are often rendered brittle, and contours are indistinct. It is very slow in action, but after
washing in alcohol, staining is said to be easy and successful.
Alcohol-Method—A great number of ova and embryos were not subjected to special treatment,
but were simply transferred from the tanks (sea-water) to 60 per cent. alcohol. In this they were
lulled and hardened, as ordinary museum-specimens are. Much distortion often resulted, yet some
good sections were made of blastoderms thus simply prepared. The capsule of the egg was
usually pierced with a fine needle to ensure entrance of the alcohol, stain, &e.
The graduated series of alcohols was tried, and, producing less distortion, gave fair results,
The objects were transferred from the sea-water into dilute alcohol, “ Dritteraleohol,” iz., 33°3 per
cent. ; thence in 40, 50, and 60 per cent. On account of the small size of the ova, five or six hours
in each sufficed, extended in the stronger alcohols to ten or twelve hours.
IIL. Sramie.—Only alcoholic stains were used, and Beale’s solution, if not too newly made,
gave very satisfactory results. It requires long immersion, rarely less than twenty to thirty hours,
and is apt to be diffuse, but acidulated alcohol in a short time makes it markedly nuclear. Diluted
with alcohol, the penetrative power of this stain is increased.
Borax Carmine (NAPLES formula) is one of the most successful stains—penetrating and nuclear,
and sections are additionally valuable if, after overstaining, the eggs are placed in acidulated alcohol
until the surplus is removed.
Hematoxylin (KLEINENBERG’S)—This proved less useful than might have been supposed; no
good sections of early blastoderms were obtained after the employment of this stain, but more mature
tissues were very satisfactorily treated, the stain being of the most pronounced nuclear character.
On the whole, the carmine stains are found to be the best.
IV. ImbBeppING.—Prior to imbedding, the ova were finally dehydrated by an immersion for two
or three hours in absolute alcohol, and transferred thence either into benzine, oil of bergamot,
or chloroform—clove-oil, creosote, &e., not being found to act well. The transference was made
gradual by the method of GriksBrecHT. Turpentine succeeded the bergamot, in other cases
a mixture of the clearing agent and paraffin followed, fragments of paraffin being added until
finally the objects were transferred to pure melted paraffin in the usual way. Mixtures of the
hard and soft paraffin, supplied by the Cambridge Instrument Company, were used—the proportions
varying according to the temperature of the laboratory. Before transferring from the final absolute
806 PROFESSOR W. C. M‘INTOSH AND MR E. E, PRINCE ON
alcohol, it was found necessary in the case of certain embryos to remove the yolk. In such com-
paratively large forms as Cyclopterus, Cottus, Anarrhichas, and Gastrosteus, the yolk became so dense
in the hardening process that the razor of the microtome would not pass through it; hence, by
dissecting off a portion of the yolk-sac, the enclosed yolk could with care be removed en masse.
WHITMAN (op. cit., p. 178) recommends (rastrosteus as especially suitable for sections, forgetful of the
fact that the yolk-mass presents peculiar difficulty to the microtomist*—in contrast to the yolk-mass
of more delicate ova, such as the cod, whose yolk is cut with ease by the razor. Ova which contain
large oil-globules, eg., Trigla and Molva, are not reliable for cutting, the alcohol removing their
constituent fluid, and leaving large empty cavities in place of the globules,
XI. Empryonic, Larvat, AND Post-LARvAL CoNnDITIONS OF THE Foop FisHes.t
Trigla gurnardus,t L.—In dealing with the ova of this species, it has as a rule
been found at St Andrews that the ripe females are considerably larger than the males,
but whether this is due to the fact that the males, as in some other fishes, e.g., the
salmon, become earlier mature, or to other circumstances, is at present undetermined.
The rate of development of the embryo depends much on the temperature, thus ova
fertilised on the 6th May hatched on the 13th day, while the embryos escaped from the
eggs on the 6th day, respectively on 17th June and 5th July 1885. The spawning
period of this form is thus considerable, viz., from April to June.§
The young gurnard, on emergence (Pl. XII. fig. 1), is a glassy transparent
form with a considerable yolk-sac, the oil-globule (egy) in which is conspicuous at
the posterior angle, and is surrounded by a thickened layer of protoplasm (p).
Numerous round pigment-corpuscles of a dull yellow or olive colour, often apparently
dull greenish, are scattered over the head, dorsum, and latero-ventral region, but
they do not extend to the tip of the tail. The dorsal margin of the embryonic
fin has finely ramose, dull yellow, pigment-spots, with a few intermingled black
corpuscles. These proceed within the dorsal edge, and may be traced down to the body
line, a short distance in front of the tail, finally intermingling with the branched pigment
on that portion of the animal. A similar pigmented area occurs along the ventral fin for
a short distance. The coloration of the pectoral fin (pf) is very striking, an arch of
pigment-corpuscles passing across the base of the organ, which, as in the young cod, is
now erect. Over the yolk, as already noted, many stellate yellowish and a few
black corpuscles occur, and they often anastomose. We have seen that this
colouration of the yolk-envelope is characteristic of certain species, the gurnard being
one, while in others, e.g., cod and haddock, this feature is absent. Besides the opercular
aperture, a single gill slit (?) at this stage occurs above the heart (Pl. VIII. fig. 8, poe),
* WencKEBACH, who killed the embryos of Perca in corrosive sublimate, and stained in picro-carmine, alludes to
this character of the yolk—* the embryos being very small, and the yolk extremely hard in the preserving reagents . . .
satisfactory sections are difficult” (No. 157).
+ The order of convenience only has been followed in this section.
t Day (Commercial Fishes of Brit., p. 77) states that the gurnard probably spawns twice a year, viz., in mid-winter
and mid-summer, If he means that each individual fish spawns twice, there would seem to be no struetural grounds
for the remark. § Mr Scorr found ova of this species in the Moray Firth in January.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 807
and the epidermis of the cephalic region is very uneven. The heart (4) has the siphonal
shape, and the dilated venous end is curved to the right. In some examples a large
space—RyDEr's segmentation-cavity—is present below and in front of the heart (PI. VIIL.
fig. 6, pd), while in others this space is either much reduced or is not present. In some,
again, the pigment is less developed than in others, the former possibly having emerged
at an earlier stage than the latter. The larva at this time hangs in the water with
the yolk uppermost, the head being often directed downward.
2nd day.—On the second day the pericardial wall has, in front, shifted downward, so
that its attachment terminates anteriorly some distance below the junction of the throat
and the yolk-sac. The latter is diminishing, and has already receded from the rectal
bend of the intestine. A large lumen is present in the oesophagus, and it distinetly
passes beneath the eye. ‘The pigment-corpuscles at the margin of the dorsal fin, which
were at first amorphous, are now finely branched. A very remarkable phenomenon is
the shortening of the region between the pectorals and the otocysts, coincident with the
great growth of the pectoral fins. Three branchial arches are distinctly visible, and
have an oblique dorso-ventral direction, but the slits do not appear to open externally
at this stage.
3rd day.—On the third day (Pl. XIV. fig. 2) the chief changes are the increased
prominence of the snout, which now projects in front of the yolk-sac, the general
shrinking of the latter, and the very finely branched condition of the pigment-corpuscles
in the marginal fin, pectorals, and on the yolk-sac (PI. V. fig. 2a). More pigment, of
a yellowish colour, now occurs over the mid-brain and round the eye. The reticulation
of the peculiar pigment-corpuscles of the yolk-sac is conspicuous (PI. V. fig. 2a), these
bodies wholly differing in shape from those of the embryonic fin and other parts (PI.
XVI. fig. 8, those of the trunk being figured on Pl. V. fig. 2). The pectoral fin has
acquired greater prominence, and its distal margin is rounded. Little change has
occurred in the outline of the marginal fin. Surface-views still show that the oral
region is impervious from the widely open mouth to the eye, but the lumen of the
alimentary canal posteriorly is very distinct. The liver projects prominently opposite
the posterior border of the pectoral fin. The urinary vesicle (wv) is elongated from above
downward, and the segmental ducts often appear to enlarge before opening into it. The
larve at this time show increased activity, and jerk or dart about at intervals,
apparently for respiratory purposes. In certain cases the well formed and active
larvee keep near the bottom of the vessel, while the deformed examples float helplessly
on the surface. They occasionally remain still, hanging obliquely with the head down-
ward, and gradually descend to rest quietly on the bottom. The fine yellow pigment and
shining oil-globule in the yolk are diagnostic features. The dead sometimes float as
minute white objects on the surface, though generally they sink to the bottom.
5th day.—When five days old the gurnard measures *165 of an inch. The eyes
have a greenish lustre, with black pigment. The ochre-yellow pigment is now chiefly
confined to the head, yolk-sac—where the corpuscles are finely ramose, the pectorals, the
808 PROFESSOR W. C. MSINTOSH AND MR E. E. PRINCE ON
anterior dorsal region, and the base of the mandible, but they are very sparse on the
opercular and abdominal surfaces. In the region at the base of the abdomen black
pigment-spots are numerous, while one or two occur on the tip of the snout and along the
ventral margin of the myotomes. ‘The pectoral fins form a pair of great fan-like organs
dotted with yellowish pigment and very minute black spots, while delicately branched
yellow corpuscles occur towards the free margin. No feature is more striking than the
great development of the pectorals; they project almost at right angles to the body, their
concavity being directed backward (Pl. X. figs. 2, 2a). They actively move with a
vigorous paddle-like motion, and aid effectively in progression.
The tail now shows dorsally and ventrally three ridges which slope in the former
ease upward and backward, and ventrally downward and backward. The mandible
remains stiff, or is very slightly movable, and as the upper jaw projects, and the mouth
is wide open, the appearance produced is remarkable and diagnostic. Aeration is sufhi-
ciently provided for by this wide and rigid oral aperture, and the energetic forward
movements of the fish. Ina deformed specimen at this stage the urinary vesicle was
large, and distended with a large number of minute highly refracting granules. More-
over, the dorsal blood-vessel (vs) was in course of formation, since rows of comparatively
large cells formed a definite tract beneath the notochord (7), as was also plainly seen in ,
the larval ling (PI. XV. fig. 1). This specimen was apparently affected by hydrops
pericardii, for the heart was directed at right angles from the pre-hyoidean region, and
the venous portion formed a spindle-shaped process attached by a narrow neck to the
ventral pericardial wall. At this latter end of the heart large rounded globules occurred,
while the arterial portion was attached in front to the posterior part of the branchial
framework. Probably by the dragging down of the membranous attachment of the
venous end, its spindle-like form was acquired. The yolk is now very much reduced.
On the following (the sixth) day, the rapid development of pigment greatly obscured
the internal structure of the young fish. On the eighth day the premaxillary region
sends out a pair of prominent knobs, theprecursors of the spinous ridge which is subse-
quently formed. The anus, which has probably been open a day or two, now shows a
distinct corrugated aperture. The rectum is often swollen, apparently with a watery
fluid, and its strongly folded walls contract powerfully—expelling a riband of translucent
mucus containing minute refracting (fatty ?) granules similar to that discharged in the
tanks by the adult Cyclopterus. The mouth (m, Pl. IX. fig. 5) is still gid, but widely
open, and the gullet leads into a pendulous, sacculated stomach immediately behind the
liver. Thus the course of the cesophagus behind the otocysts is backward and downward,
The gut leaves the upper border of the stomach, passes along the roof of the abdominal
eavity, and bends downward to the anus at an angle slightly less than a nght angle.
The whole alimentary canal behind the short cesophagus is thrown into complex rug,
which constantly vary with the peristaltic movements of the walls. Above the cardiac
end of the stomach, and surrounded by the hepatic folds, is the translucent rounded gall-
bladder.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 809
During the following days the black pigment continues to increase, especially at the
base of the abdomen. At first the radiate corpuscles are separate, but they subsequently
anastomose and form dense patches.
16th day (Pl. X. fig. 2)—The great size of the pectoral fins (pf) is the most
prominent feature at this stage. They are in constant motion, flapping to and fro like a
pair of fans, and the pigment (pt) on their surface is largely developed. The yellowish
yolk has shrunk very much, and forms an irregular mass in the pectoral region, the oil-
globule, apparently undiminished in size, still occupying a posterior position. A large
vacant space (ss) is left in front of the rectal tract, and a similar large space (ss) occurs in
front of the yolk. The snout is much elongated, and viewed from above is like a
truncated cone just as in the adult gurnard. A feature of moment is the comparatively
motionless condition of the mandible (mn). The marginal fin (ef) shows no differentia-
tion into definite fin-areas; it is, as compared with the breadth of the body, now
proportionately narrower. As above noted, the pectorals (pf, Pl. X. fig. 2a) are the
most noteworthy feature, standing out almost at right angles to the trunk, and so well
developed that, viewed obliquely, the young fish resembles very strikingly Pegasus natans.
Under a lens the yellowish pigment is seen to be confined chiefly to the head, pectorals,
and yolk-area. A few corpuscles occur along the margin of the dorsal fin in front, and
a few also on the tail; but the body has fewer of them than previously, finely branched
black corpuscles alone being present. A later stage (Pl. X. fig. 3), about three weeks
after emerging from the egg, exhibits much the same features—a chitinous bar being
prominent in the premaxillary region. The next stage under observation was procured,
along with a large number of others, while in the Fishery Board tender “ Garland,” and
the specimens were slightly larger than the last stage described, viz., about 6 mm. in
length. They clearly were the young of the same year, as they were obtained at the close
of summer, viz., 3lst August. The great size of the head generally, as well as of the
eyes and brain, was characteristic, and especially the broad scoop-shaped snout with the
median “bite.” Behind the head the pendulous abdomen projected like the yolk-sac
(now almost wholly absorbed) of the earlier stages. The stomach, in fact, was found to be
greatly distended with minute Copepoda, which form the staple food at this time. The
pectorals are even larger than in the previous stage; while the marginal fin with its
embryonic rays continues into the tail fin, which shows the notochord as a median
slightly tapered axis. From this axis the rays below slant downward and backward,
while those above lean upward and backward. Those coming from the tip of the
notochord are short. The ventral rays are larger, and a granular opaque tract below the
chorda probably indicates the site of the future hypurals. No cartilagmous rays are
present. The marked downward projection of the angle of the jaw, and the lean tapering
body behind the massive abdominal region are noteworthy features. As the specimens,
on account of their extreme delicacy, were injured by the pressure of the water against the
net, it was necessary at once to consign them to alcohol, and their colours were thus
more or less lost. Large stellate pigment-spots could, however, be distinguished along
VOL. XXXV. PART III. (No, 19). oi
810 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
the dorsal line of the abdomen, and a linear series also passed along the ventral line of
the body posteriorly. These tiny, though active and vigorous, forms, had already left the
surface where their early larval life is spent, and consorted with their older brethren
in the still water of the open sea at 25 fathoms. The next stage, as shown in these spirit-
preparations, is about 7-5 mm. long, and the chief changes noted are as follow :—The size
of the head has further increased, and the snout is longer ; moreover, several sharp spinous
processes project from the occipital area, though those on the operculum are not yet much
developed. The translucency of the head permits the brain to be fairly seen, and the
nasal organs are clearly outlined, as well as the facial and branchial cartilages. The
pectorals form large fan-like organs with pigment-corpuscles thinly sprinkled towards the
tip. The rays (thirteen in number) are all united by membrane, so that the three
filaments which are free in the adult must be separated later. While the proportions of
this anterior pair of fins are great, the upper rays being nearly half the length of the
body, the ventral fins project as mere buds, so that their use in progression is trifling
when compared with the same organs in such a form as the young ling (see p. 829).
Along the ventral margin at the tip of the notochord, which is not yet bent upward,
three hypural elements are visible, the first being large and prominent, the last merely a
thin band below the termination of the chorda. Cartilaginous rays now appear in the
ventral division of the caudal, but are absent in the median and upper portions of the
fin, in which embryonic fin-rays still occur. In the next stage, one or two millimetres
longer (z.e., 8 mm. or 9 mm.), the hypural elements have assumed a broad wedge-shape—
with an even edge posteriorly and slanting from above downward and forward. Only
a short process of the notochord is free, and this part is slightly flexed upward. The
marginal fin still continues from the dorsum to the tail, and the inferior lobe of the latter,
with its cartilaginous rays, has increased so as to constitute its greater part ; while the
upper lobe, with its embryonic fin-rays, has decreased in size. The great pectorals seem
to be growing, while the ventrals are also larger, and their rays are variegated with
black pigment. Upon the head the spinous processes are more distinct.
When the young gurnard has reached the length of 10 mm., spines not only appear
on the operculum, the angle of the jaw, and the facial surface, but attain some size, two
upon the occiput being especially prominent. The long upper rays of the wing-like
pectorals reach nearly half the length of the fish, while the ventrals show considerable
growth, and project freely as small fins thickly pigmented with black corpuscles. Their
length is not quite equal to that of the basal part of the pectorals, which are, compara-
tively speaking, enormous. The posterior border of the hypurals is nearly straight (in a
vertical direction), and the free portion of the tip of the notochord has diminished. The
small upper lobe of the tail continues to decrease, though the delicate embryonic rays are
still visible in it. The remnant of the marginal fin fringing the trunk shows no carti-
laginous rays.
When 15 mm. long, specimens present much the same features as the last stage
(Pl. XVII. fig. 5), but the nuchal spines upon the occiput are characteristically promi-
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 811
nent. The head is large, and the body shows an evident increase in size. The first and
second dorsal fins are still continuous, though their separation is indicated by an indenta-
tion. Embryonic fin-rays alone are present, those of the anterior moiety or first dorsal
being short, while the longest rays occur about the posterior third of the second dorsal.
This is a marked feature when contrasted with the adult, the anterior rays of whose first
dorsal fin far exceed the others in length and strength. The caudal fin is more distinctly
separated from the dorsal above and the anal below. Dorsally the marginal fin at the
base of the caudal almost ceases behind the second dorsal, but ventrally it is broader
and less distinctly separable from the anal. It still exhibits merely embryonic fin-rays.
The caudal fin is somewhat conical in shape, being broad at the base and sloping
to the projecting median rays, and thus very different from the slightly emarginate
adult fin.
The hypurals form an almost vertical border from edge to edge, z.e., dorso-ventrally,
and the notochord now barely projects from the superior angle. Above the latter several
linear (opaque) tracts indicate the superior accessory fin-rays, and inferiorly shorter rays
appear next the hypurals. The anal fin shows fin-rays similar to those in the dorsal
fin. The pectorals are still of large size, the upper rays being about double the length of
the lower. The three lowermost rays that ultimately become free filaments are webbed to
the tip. Black pigment has greatly increased over the fin, especially distally, and a black
margin passes a considerable distance posteriorly. The ventrals now extend slightly
beyond the anus. Black pigment-corpuscles have increased over the head, cheeks,
abdomen, and ventral line of the body.
Frequently in this and the earlier stages specimens of a Crustacean (resembling the
young of Caligus) are found fixed to the head or other regions by the long central
process.
When the gurnard attains a length of 17 mm., the caudal fin is separate from the
second dorsal, and has several accessory fin-rays. It is also free inferiorly, but the
separation is marked by a gap behind which a portion of the marginal fin runs on to join
the caudal, where the accessory fin-rays begin. The most prominent part of the caudal
fin is still the median border; but the complete separation of the anal and dorsal fins,
and the growth of the superior and inferior fin-rays, produce a great change in its
appearance. ‘The first dorsal is not quite wholly separated from the second, and its rays
are considerably longer than in the foregoing stages, while the posterior rays of both
second dorsal and anal are longer than the remaining rays in these fins. Black pigment
is scattered over the entire surface of the pectoral fins, extending, indeed, as far forward
as the border of the branchiostegal region. The lengthening of the body beyond the tips
of the pectoral fins causes the latter to appear somewhat shorter. No separation of the
three anterior filaments of these fins has yet occurred. The ventrals have grown slightly,
and extend a little further beyond the anus. The branchiz are now much more definitely
pinnate than hitherto, and resemble the barbs of a growing feather.
At the next stage demanding special notice, the young fish measures about 21 mm.
812 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
in length, and in form closely approaches the general appearance of the adult.* The
spines on the head are, however, proportionately larger. The first dorsal is appreciably
larger, its supporting spines stronger, and their tips project beyond the connecting
membrane, while a deposit of pigment has appeared in its median region. The
posterior fin-rays of both dorsal and anal fins have increased in length, so as to cover,
when depressed, most of the space intervening between the second dorsal and the caudal.
A row of prominent conical papilla, larger posteriorly, extends along each side of both
dorsal fins. A series of more minute papillae marks the lateral line. By a further
development of the parts of the tail-fin at the dorsal and ventral accessory fin-rays, the
outline of the tail becomes less conical, and the posterior border is now, indeed,
distinctly truncated. The caudal fin is, in fact, much longer than broad at this stage.
The pectoral fins, though still large, appear of less size on account of the continued
growth of the trunk, as well, probably, as from atrophy of the upper or long rays.
The pigment-corpuscles are, moreover, definitely grouped upon the pectorals—forming
a basal and two distal bands, the latter conspicuously colouring the expanded fin. The
three inferior rays are larger than the others, but still connected by membrane. The
ventrals now extend considerably beyond the shorter pectoral rays. In some examples
several of the parasites (Chalimus-stage of Caligus) occur on the cephalic and hyoidean
regions. The pinnately fringed branchix show greatly increased complexity.
A specimen, 22 mm. in length, procured in St Andrews Bay, Aug. 23, 1886 (Pl. XVI.
fig. 7), presents considerable increase in the pigment of the various parts, a feature
probably connected with its life in the shallower waters of the bay, where the sunlight
has more direct access. The pectoral and dorsal fins, and general surface of the trunk
and head, are boldly marked; indeed, the little fish is most vividly tinted. Moreover,
it is important to note that the three stronger radial filaments of the lower anterior
border of the pectorals are now separated, and during confinement, for a short period,
the connecting membrane was observed still further to disappear, as shown in the figure.
Though very slightly longer than in the preceding stage, the pectoral fins are propor-
tionately shorter, while the first dorsal and ventral are somewhat longer. The appear-
ance of the fish, viewed from above, is shown in Pl. XVII. fig. 6.
When a few millimetres longer (e.g., 24 mm.), the spines on each side of the dorsal
fins, and along the lateral line, are very distinct, A trace of the connecting membrane
still remains at the bases of the three free filaments of the pectoral.
Next season the young gurnards appear to reach the length of 24 to 3 inches in
June, though others range to 4} and 64, but whether the latter and those reaching
41 and 64 inches in May are older forms of the same season, or belong to a previous
one, has not yet been determined. It is probable that all may be included in the
season’s growth.
Gadus morrhua, l.—The ova of the cod are very abundant in many parts of the
* In a specimen whose total length was 20°5 mm. the following proportional measurements occurred :—Head,
‘5 mm.; tail, 5 mm.; longest feeler, 5 mm.; trunk, 10°5 mm.; pectoral, 6°2 mm.; breadth of head, 3 mm.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 815
sea at both surface and bottom from March to May,* and have a diameter of ‘0551 inches
or 1375 mm. The embryo emerges from the 8th to the 10th day in April, and in
May somewhat earlier.
Thus those which on the 16th April presented the multicelled lenticular stage with
the nucleated periblast surrounding the disc, next day, at 9.30 a.m., showed a still
larger number of nuclei in this zone, which, however, at 1 p.m. had all but disappeared,
while the blastodermic ring had increased in size. On the 18th April the blastodermic
ring extended over a third of the surface of the ovum, and two hours later it had gained
the equator. At3 p.m. the keel of the embryo had deepened, and faint indications of the
optic enlargements were visible, while at 4 p.m. they were completed.t At 10 A.M. on
the 19th the embryo was fully outlined, with five or six protovertebree. The blastopore
had closed, and there were traces of Kuprrsr’s vesicle. At 12 noon the protovertebre
had doubled, and Kuprrsr’s vesicle was more distinct. The invagination of the lens had
commenced, and the alar membrane of the embryo was distinct.
20th April.—tThe eyes, otocysts, and mesenteron (which turns to the right) had all
made progress, and the heart showed a double-celled appearance at 3 p.m. The otoliths,
at first very small, occurred at 4 p.m., and the pectorals were outlined. 21st April.
The body of the embryo jerks from side to side, and the heart pulsates languidly and
nregularly (about 3 p.m.), the contractions, however, sometimes ceasing for fifteen or
twenty seconds. The trunk has lengthened and the caudal extremity is flexed. The
pectorals are more distinct, and the delicate processes anterior to the fins (observed in
most forms) still persist. The mesenteric lumen extends as far as the heart, and
enlarges in the mid-region. The notochord is now completely crossed by intermingling
ares.
22nd April—the posterior region of the trunk and tail are now flexed, and the yolk
appears to have decreased. The pectorals are well defined and pointed posteriorly,
while the anterior margin is rounded. The liver forms a rounded process, the heart
shows a venous end, and the pulsations are more regular (twenty-five per minute).
Round chromatophores (black) have appeared on the head and dorso-lateral regions of
the trunk, but they have no regular linear disposition.
23rd April.—tThe eyes show pigment, and that over the body has increased. Three
branchial clefts and the nasal pits are visible. The violent motions of the embryos
indicate their advancement, and a few issued from the eggs. The empty capsules retain
their spherical shape, though a rent passes two-thirds across their diameter.
24th April.—Five-sixths of the embryos are still in the eggs. They present a similar
appearance to the previous day, though the increasing complexity of the branchial region
is evident, and four clefts are visible. Some of the chromatophores on the head are
stellate.
* Méprus and Herncxe state that the cod in Kiel Bay spawns from January to the end of March, but in other
parts of the Baltic, ¢.g. Gothland, in April; op., cit. p. 233 (1883).
+ The temperature of the laboratory was 59° F.
814 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
25th April.—Further changes occur in the pectorals which are bluntly lanceolate,
and in the pigment which in the eye has a bright bronze-like hue. The urinary, vesicle
and other viscera are advancing.
The newly hatched cod float on the surface of still water. When a current of air is
directed against them some wriggle aimlessly about, others, probably less robust
specimens, float helplessly in the water. The yolk-mass is often uppermost, though some
of the stronger carry it inferiorly. In many abnormal forms, which have a slightly
distorted or curved appearance, the yolk lies laterally on the surface of the water.
Four pigment-patches diversify the transparent body of the young larva, one behind
the pectorals, one towards the posterior border of the yolk, and two on the tail. The
disposition of these bands of pigment is well seen when the larve are placed in sea-
water in a white porcelain vessel (Pl. XIX. fig. 8). The larval coloration is temporary,
and differs in arrangement from that in the next and subsequent stages.
27th April—the free larvee are very active, swimming forward in a straight course
with considerable speed. When at rest, however, they often lie on the side, or float with
the yolk uppermost. The snout has become free from the yolk-sac to some extent, and
the oral aperture has burst through. The otocysts have approached the eyes. The yolk-
sac is still large, but the breathing chamber anteriorly has expanded. The distinctive
patches of pigment can now be made out on the trunk. In several advanced specimens
the circulation was visible, the corpuscles passing along the dorsal aorta and returning
after traversing about a quarter of the length of the tail.
28th April.—The circulation can be traced two-thirds along the tail, and though a
definite branchial circulation cannot be made out, a confused movement of corpuscles
having the appearance of a plexus occurs posterior to the otocysts. The larval cod swims
in straight lines, and now keeps the yolk-sac inferior.
29th April.—The general outline is altered, the upper jaw projects beneath the eye,
and a depression divides it from the olfactory enlargement superiorly. The mandible
extends a little beyond the upper jaw. The yolk-sac has much diminished, the folds of
the mesenteron have increased, and the branchial system become more complex, while
the aorta proceeds almost to the tip of the tail.
30th April.—tThe dorsal median fin now begins over the mid-mesenteric region, and
the cuticular tissues in front form an expanded cap over the head, covered with papille.
This is the “integumentary vesicle” or ‘lymph-space” of Ryprer, who mentions
homologous structures in the Spanish mackerel and other forms. He does not now
consider this as an extension of the median dorsal fin-fold, which is never carried to the
front of the head. It is very characteristic of the gadoids as well as of several
pleuronectids.
1st May.—The development of the pectorals is marked, and they are slightly angular
in front, rounded posteriorly. They are brought to the sides, and by a wriggle of the tail
the fish progresses.
2nd May.—The larval cod are now about 4°5 mm. long, and though their dis-
——
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 815
advantageous surroundings have diminished their vigour, they still make active forward
movements, and often rest on the bottom. The yolk-sac has almost disappeared. An
almond-shaped mass lies along the floor of the abdominal cavity. The alimentary canal
appears to be shortened, and still shows the constriction at the pylorus. No anus has
yet appeared. The urinary vesicle is unaltered.
Ryper* states that the larval cod has the integument raised above the head, and that
a large serous cavity or supra-cephalic chamber is formed, which appears to serve as a
float, but the latter interpretation is doubtful. The fish swims horizontally, but when at
rest has an oblique position, the tail pointing backward and downward. The sub-
epidermal space is very prominent in older specimens three or four weeks after emerging,
and they are then very strong and vigorous, usually frequenting the bottom of the tank, a
habit inconsistent with Ryprr’s view just stated, and shooting rapidly through the
water, the large iridescent silvery eyes being the feature most readily seen. They
dexterously escape from the forceps or other instrument used for their capture, and do so
with considerable intelligence. The pectorals are large and strong, and the larval cod
can direct its course with great agility and speed. The mandible and hyoidean apparatus
project considerably, and the abdomen is hollow and shrunken (PI. X. figs. 5, 5a).
The lateral view resembles a Chinese caricature of a fish, or a malformed trout, such
as indicated by Acassiz and Vocr,t this effect being produced by the curvature and
size of the head. The anus is lateral in position, and has not yet reached the ventral
margin.
It occasionally happened that favourable circumstances enabled us to rear an example
to a somewhat later stage. Thus, for instance, one in which the yolk had wholly dis-
appeared on the 31st May, though the length was only about 4 mm., presented a marked
enlargement of the head, chiefly from the great increase of the hyomandibular apparatus
and the projection of the angle of the jaw. Moreover, the upward slope of the mandible,
so marked at a later stage, was now characteristic. When viewed ventrally, indeed, this
formed a high wall on each side of the hyoidean region. The body was comparatively
massive. The cephalic “vesicle” had disappeared, but the broad marginal fin still
surrounded the fish, and in the tail fine embryonic fin-rays occurred inferiorly. A few
also were indicated at other parts of the fin both dorsally and ventrally. Behind the now
open vent a rounded margin appears in the ventral fin. The pectoral fins are very large,
and show a finely radiate basal (mesoblastic) region, and a fan-like membranous distal
portion. The snout in a lateral view is prominent, with a deep hollow above the pre-
maxillary region. The eyes are large, deeply pigmented, and with the bluish silvery
sheen so well known at a later stage. Close behind the eyes are the large otocysts with
the otoliths. One of the most interesting features at this stage is the evolution of the
coloration of the early post-larval stage out of the four dark bands so characteristic of
the larval form. At the stage now under consideration the little cod has only two
* Science, vii. 1886, pp. 26-29 (fig. 1).
+ Hist. Nat. des Poissons @eau douce, taf. 3b.
816 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
well-defined bars behind the abdomen—by a partial coalescence of the dorsal and ventral
masses of pigment; the others have been modified into a band of black pigment, which
passes along the roof of the abdomen, and if somewhat younger forms be examined
the steps leading to the coalition of the two pigment-touches are clearly demonstrated.
Various black chromatophores occur on the head, at the angle of the mandible, and on
the ventral surface of the abdomen. There is thus already a change of pigment, and it
is easily seen how the post-larval colouration develops normally from the condition just
described.
The scanty supply of suitable nourishment and the indifferent nature of the
surroundings (for the water in tanks is very different from the freely aerated and
healthy oceanic water) probably retarded growth to a considerable extent. Those
of 4°5 mm. in length, however, were brought within a very brief distance of the forms,
6 mm. long, caught by the mid-water net in the bay.
Between the stage above mentioned and the appearance of the young cod in shoals at
the margin of the tidal rocks, there has been in this country till now a blank more or less
complete, only a stray specimen or two—half an inch long—having been captured
in the tow-net near the surface. The observations of the last two seasons, and
this with the large mid-water net,* have, however, advanced the inquiry within a
measurable distance of completion. By employing the net during the winter, as well
as during the spring, summer, and autumn, most of the intermediate stages were pro-
cured.
For some years the efforts of one of us have been directed specially to the
elucidation of the history of the present species in its young condition, as the account
given by Professor G. O. Sars for Norway was not applicable in all respects to the
British Seas. In 1886, indeed, some remarks were made on the young stages of the
cod, which Professor Sars had captured, at the surface of the sea, some years ago,
in April amidst quantities of the “herring-food,” viz., Calanide, e.g., Calanus fin-
marchicus and Temora longicornis, species which abound under similar circumstances
in our own seas. Besides the points indicated in the paper just mentioned it may
be noted that on the 12th of June Sars found “that the clear and undivided
embryonic fin surrounding the whole body had already in part dissolved into the
first and second dorsal, and a small barbel was present.” On the 5th of July, again,
they were discovered along with young haddock, shorter and stouter in shape, under
Aurelia aurita and Cyanea capillata, as well as under pieces of Alow; and he con-
sidered that they associated with the Meduse for the sake of the benumbed animals
and the parasitic Hyperiz. It must, however, be borne in mind that in our seas
Hyperiz (e.g. Parathemisto) are frequently found in a free condition and in very great
numbers. Similar young cod were found at Lofoten in the stomachs of pollack
(Gadus pollachius), shoals of which surrounded them, chased them to the surface,
* Vide Ann. Nat. Hist., Oct. 1886, p. 310.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 817
where they were thus put within reach of the gulls as well as the pollack themselves.
On the 38rd August the shoals of young cod, 2 inches and upwards in length, presented
the following external colouration :—Three or four parallel lines of square spots, reddish-
brown and more or less bright, extended along the sides, which with the head showed
an alternating silvery or golden gloss. Sars thinks that they are driven shorewards
when 2 or 3 inches long, by wind and currents, and seek protection from the pollack
among the Algz at the bottom. Moreover, it would appear that the shoals succeeded
each other, since they went off as they grew older. In the beginning of October,
having attained the length of 4 or 5 inches, they grow more rapidly, reaching in
the middle of November the length of 6 inches, while on the 10th of December they
measure 6 inches to 8 inches. Towards the end of winter they decrease in numbers.
Sars states that the last fishes to appear amongst the Algz were no larger than the
first, and that there must of necessity be a succession of shoals. Indeed, he describes
two varieties, viz., the thickish, reddish-yellow kind, living chiefly amongst the Algz,
and swallowing large numbers of reddish crustaceans, and a second kind of a light
ereen or greyish shade frequenting sandy ground, where the Crustacea mentioned were
rare—these thinner fishes living on Annelids and young Cott. Towards the end of
February he followed them further out to sea, and found them measure on an average
12 inches, and he was of opinion that the “ Alow-fish” were one year old. The
greatest number of these “ Algv-fish” (1 foot long) are caught, it may be noted, in
summer; but towards autumn their numbers are fewer. Accordingly, Sars concluded
that the “going out” takes place in the second year, and that three years, or at most
four years, hardly elapse before the fishes return to their native sites as full-grown
cod, ready to reproduce their species. Considerably larger fishes than the forms found
in February (1 foot long) he estimated at two years old, and in these the generative
elements were found at Lofoten not to be fully developed, the smallest breeding fish
being nearly 1 yard in length. On the other hand, he had seen young cod 1 foot in
length in the fish-market of Christiania, which had mature roe and milt.
Hitherto no very young gadoids have been captured in January, February, or March,
and it is the end of April before such appear; indeed, they are more surely obtained in
May in St Andrews Bay. Moreover, it does not follow that the smallest always occur in
the earliest months, for some are found in May as small as any in April. The least of
those hitherto secured was about 5 mm., several having been captured on the 30th April,
and others of the same size on the 19th of May and Ist June. Now the little cod reared
in the laboratory to a certain stage are about three-fourths the length of this on the 9th
May, and though we cannot antedate the spawning period of the cod from personal
observation sooner than March, there is no reason to doubt the occurrence of an earlier
issue of ova and spermatozoa in some cases; indeed, the general variability would hold.
This, and the differences in the rate of growth known to occur even in those spawned
at the same moment, give us the somewhat wide range in size with which we are familiar
in the group.
VOL. XXXV. PART III. (NO. 19), 6 M
818 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
A fortunate sweep of the trawl-like tow-net on the 1st June gave a complete series
of fresh specimens, from the form just described to other stages formerly seen. The
smallest cod were 5 mm. in length, but they were even younger than the somewhat
stunted specimens reared in confinement. They had the two post-anal bars, the sub-
notochordal black band, and the scattered spots on the head and jaws; and they were
further characterised by the greenish-yellow colouration on the head and snout, as well as
along the dorsal region of the body, a feature so marked at a somewhat later stage; the
swim-bladder (which appeared to have a short or rounded form) was distinct. The tail
and marginal fin did not differ from the stage mentioned on the previous page. Almost
the same remarks apply to those 6 mm. in length, some of this size presenting a
pinkish abdomen from the oil of the minute copepods they had swallowed. At 7 mm.
the marginal fin has many embryonic rays ; moveover, the two post-anal pigment-spots
have spread out, so that they form a dorsal and a ventral band, though two denser regions
indicate their former condition ; a median line also occurs laterally. The yellowish-green
tinge is better marked.
In small forms 6 mm. long in spirit, and probably corresponding to the stage last
mentioned (7 mm. when fresh), the marginal fin is quite continuous, commencing
ventrally behind the well-formed anus and passing round the tail to a point on the
dorsum a little in front of a vertical line from the vent, though in front of this a
membranous margin projects a short distance, indicating probably a further extension of
the fin. Fine embryonic rays are present throughout, except in the caudal region, where
slight linear thickenings dorsally and ventrally indicate the commencement of the
permanent rays. The pectorals are large, with a chimeeroid base and a fan-like membrane
with embryonic rays. No trace of ventrals is visible. The mandible is bent upward
when closed at a little more than a right angle to the body, and the angle of the jaw is
very prominent. The eye shows a notch dorsally, and a well-marked choroidal fissure
inferiorly. A little black pigment exists on the snout and the top of head, and along each
side of the dorsal and ventral marginal fin, while a streak also occurs in the middle line
laterally in front of the tail. The same pigment appears in touches on the prominent
edges of the mandible, and along the ventral surface of the abdomen.
In the beginning of May again, and also the Ist of June, similar forms are
encountered, ranging from 8 to 10 mm. and upwards. The youngest of these, 8 mm.
in length in spirit (Pl. XIX. fig. 2), still presents the embryonic fin from a point on the
dorsum distinctly behind the vertical from the pectorals all round to the vent, the tail
as yet showing no special differentiation. At points, however, corresponding to the two
posterior dorsals and the two anal fins, thickenings—indications of the adult fins just
mentioned—beyond the body-line are noticed, at the base of the embryonic fin. Beyond
these rudiments the embryonic fin is unaltered. The tail forms a perfectly symmetrical
organ, convex posteriorly, and having the notochord as a straight, tapering, and translucent
streak in its centre, with the hypural and epiural elements disposed ventrally and dorsally,
and so equally that the whole presents a lancet-like figure in the middle of the tail.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 819
A little pigment exists in the interspaces of the rays over a limited area dorsally and
ventrally. The pectorals have a large—almost semicireular—basal region, and a fan-
shaped series of rays distally, so that they are still powerful, but the ventrals are visible
only as two minute ventral papillee on the throat in front of the former. The body and
tail have increased considerably in bulk, but the head and anterior region still remain of
great proportional size. The angle of the mandible is prominent, and the jaw has the
larval slope upward and forward. The eye retains its great size. The black pigment
occurs on the top of the head—on which the chromatophores are now larger, along the
base of the dorsal, and less distinctly along the base of the ventral marginal fin, with a
streak in the middle line of the body towards the caudal region. The only other pigment
is in the abdominal region—from the top of the pectoral in a line downward and _ back-
ward to the anus, and this for the most part is internal. Yellowish-green pigment also
occurs here and there all over the surface, so that the animal when living presents a
greenish translucent aspect, and it is also noteworthy that the dorsal pigment is in two
sections on each side, thus indicating the two original spots. The eyes at this stage are
proportionally large, as in others of the group, of a bluish silvery aspect, and with
a dark arch of pigment superiorly. The bluish sheen is probably due to interference,
and not to any special pigment. The abdomen has a slightly pinkish hue from the
Crustacean food which filled both stomach and intestines. The branchiz show simple
papillee.
At a somewhat older stage (Pl. XIX. fig 3) the three dorsal fins are distinct, as also
are the two anal. It may be noted also that the first dorsal develops somewhat later than
even the two succeeding fins, that is to say, it presents only a thickening, while they
have rudimentary rays—for instance at a leneth of 10 mm. and 13 mm. In the latter
the swim-bladder assumes a more elongate aspect. The ventrals show more evident rays,
the growth of the body and head diminishes the proportional size of the eye. The snout
is longer, so that the mandible bends less obliquely upward than in the previous stage.
The blackish pigment has increased on the lines formerly mentioned, and also at the base
of the abdomen, While in the earlier stages the tail of the young cod presents a straight
notochordal process posteriorly, it now (at and near three-eighths of an inch in length)
shows a distinet upward bend apparently from the development of the hypural elements
inferiorly. The tapering tip of the notochord issues therefore from the upper part of
the pointed central mass, the shape of the region, however, marking the usual
transformation caused by the shifting of the ventral margin to the posterior region of
the tail.*
A month later, viz., on the 1st June, considerable progress had been made in the
growth of the young cod, which were caught both in the trawl and in the mid-water
net, sunk 3 or 4 fathoms in 6 or 7 fathoms of water, showing that these fishes gene-
rally seek the lower regions of the water. The length of the smallest was about 4%
* The great length of the notochordal tip (embryonic tail) in Lepidosteus is noteworthy (BALrour and Parker,
op. cit., p. 874).
820 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
inch. The pigment is not yet arranged in transverse bars, but has the character
described in the earlier stages, being chiefly grouped on the head, along the dorsum, and
on a lateral line. Stellate pigment-spots are somewhat thinly dotted here and there on
the sides. Moreover, in several, after preservation in spirit, the pigment-corpuscles on
the head show a central nucleus, then a pale area, and externally a ring or border of
black pigment, the whole presenting the appearance of minute mosaic work. The
abdomen in all is tinted of a pale orange hue from the Crustacean food which distends
both stomach and intestines. The same food is eaten by the small sand-eels, young
armed bullheads, and other fishes captured with them. The ventrals are now well formed,
and show the elongated outer rays, though these are less developed than in a subsequent
stage. Glancing generally at the contour of the fish the origins of these fins (ventral)
also appear somewhat further forward than in the later stages. The barbel is now
distinct, though it is less conspicuous from length than thickness.
As the fishes get larger (? older) there is a distinct aggregation of the black pigment
along the sides, and the appearance of a brownish tinge in the skin on which these
pigment-specks rest. These young cod are paler than the young green cod, from which
they are also distinguished by the size of the barbel (which is very small in the green
cod), and the longer snout in front of the eye; while the appearance of the pigment-spots
along the sides at once removes any ambiguity. Moreover, the eye of the green cod
is somewhat larger, proportionally, than that of the cod, probably from the shorter snout,
and the mandible in the former is longer, when each is about 14 inch in length. The cod
also soon shows a series of pale dots, from 4 to 6 in number on each side, along the
dorsum, and the general habit of the fish differs quite from that of the green cod, as
formerly mentioned.* Spirit-specimens, about 13 inch long, are readily discriminated
from the green cod by the pigment-bars and pale areas, and the barbel, as well as by the
general sprinkling of pigment-corpuscles over the entire area in the green cod. The fins
in the young cod vary considerably in regard to pigment, many presenting at this stage
a slight marginal black band, but as a rule they have much less pigment than in the
green cod, which, moreover, shows grains of yellow pigment in the dorsal fins, and to
a less extent in the first anal.
ALEXANDER AGASSIZ mentions and figurest two specimens, probably of the common
cod, 20 and 28 mm. in length respectively, the former without the pigment-bars, devoid
of a barbel, and with the median fins still somewhat continuous, the latter with long
ventral fins, pigment-bars, and the general feature of the adult. As a rule the cod of our
eastern shores show the characters of the adult before reaching so great a length. More-
over, instead of simple ventral pigment-bars, the dice-like pattern of the pigment is
diagnostic. {
The young cod which, in company with the green cod (Gadus virens), frequents the
* Ann. Nat. Hist., Oct. 1886, p. 307.
t+ Proc. Amer. Acad. Arts and Sci., vol. xvii. p. 286, pl. viii. figs. 4, 5, 1882.
t Vide Fourth Report, Fishery Board for Scotland, and Ann. Nat. Hist.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 821
rock-pools of St Andrews in June and July, often hang in the water obliquely with their
heads downward against the current. Their food at this time, when they measure 13
inch to 1¥ inch in length, consists of copepods, larval cirripedes, sessile-eyed crustaceans
(larval), small annelids, and Campontia, while the green cod, in addition to that food,
feeds upon minute Mollusca, e.g., Homalogyra rotata, and various species of Ostracoda.
The cod is less shy at this stage than the young green cod, and it is captured with less
difficulty.
Viewed from the dorsum they have a general pale olive-green colour. The sides
are iridescent, with a pretty pinkish pearly lustre. The upper surface and sides of the
head to a level with the eyes are studded with dark pigment. A regular series of dark
pigment-spots runs along each side of the median dorsal line to the tip of the tail.
About eight dark blotches occur on looking at the median lateral line, and as these are
flanked by other dark patches in the upper lateral region, they give a very characteristic
appearance to the fish (Pl. XVII. fig 8). This upper lateral region, just below the lateral
line, shows behind the operculum nine dark spots. The first three are continued on the
silvery belly, and then cease. The rest have connections with a series of median spots
(five in number) in the middle line—bands, in several instances, passing from two upper
spots to one lower median, or again bifurcating inferiorly. The ventral median line has
on each side a band of pigment, continuous with the bars just described ; but the pig-
ment-corpuscles are less distinct than along the dorsal lines, except opposite the base of
the vertical fins, where the pigment is quite regular, and corresponds with the base of each
ray. The first two dorsals have the blackish pigment towards the tip best developed on
the membrane between the rays, the basal region being pale. The third dorsal has only
a little black pigment. A trace of pigment also occurs towards the commencement of the
anal fin. Blackish pigment is scattered on the sides and under surface of the mandible,
and a thin dark streak passes backward in the middle line. The eyes are of a pale
olive-green hue, with dark specks of pigment. The upper opercular region, and the
surface above the cerebellum, are of a pale pinkish colour, due to the blood-vessels
and the brain beneath. The vascularity of the latter seems to be considerable. The
opercular region and the body are silvery. The pointed teeth are very evident in the
jaws.
The later stages have been dealt with in former papers, and need not be alluded
to at present, except in regard to Ermur’s* notion that the markings in animals are
primitively longitudinal. Now the young cod is conspicuously speckled in its earliest
stage, and is rather pale and translucent in its next condition, the pigment which forms
the transverse bars gradually grouping themselves on a somewhat pale surface, without a
trace of longitudinal bands. In many other fishes, both round and flat (Pleuronectids),
the same arrangement obtains, so that Haake had good grounds for demurring to this
view from the study of the Australian fish Helotes scotus, which in the adult is marked
by eight longitudinal bands, while young specimens have in addition a row of clear
* Zoolog. Anzeiger., Viii., 1885, pp. 507-8.
9: gery > PI
822 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
transverse bands which disappear when they attain maturity. In one fish, viz., the ling,
the post-larval stage is uniformly tinted, the next stage longitudinally striped, the third
transversely barred, while in the adult it is uniformly tinted as in the older post-larval
condition. No rigid rule can thus be held.
Gadus aeglefinus, L.—The ova of the haddock are about ‘058 in., varying a little, e.g.
from 1°65 mm. to 1°5 mm. The development of the embryo ranges from six days in
June to twenty in March.* Thus a series received from Granton presented on the
second day (22nd March 1885) a blastodermic cap ‘4 mm. in diameter. It reached the
equator on the fourth day. While the keel of the embryo indents the yolk, the head is
defined, and everywhere shows further progress. On the fifth day the optic enlarge-
ments are distinctly outlined. Faint indications of protovertebree (four to five in number)
appear in the anterior caudal region, and scattered black pigment-specks show on the
sides and dorsum. On the seventh day, at 9 a.m., the blastopore had closed, but
Kuprrer’s vesicle was not apparent till next day. The lenses of the eye are fully
formed, and the heart is represented by a granular patch. On the tenth day the various
regions of the brain were defined, with the nasal pits, the otocysts, and an opercular
cleft ; the liver is indicated on the ventral aspect of the alimentary canal. No cavity is
visible in the heart; the latter pulsates on the eleventh day about ten times per
minute, though occasionally a little more rapidly, and shows a somewhat triangular
cavity.
The pigment-spots are more numerous and more elaborately stellate on the twelfth
day, especially on the dorso-lateral regions above the pectorals. A lateral fold arises
behind the latter and passes along each side. The lumen of the mesenteron has notably
enlarged next day on the dorsal side of the liver, but it diminishes very much as it
approaches the cephalic region. On the fifteenth day the cephalic region has increased
in size, and the body has considerably lengthened. Embryonic rays have appeared
in the marginal fin. The heart pulsates on the seventeenth day about thirty times
per minute. The eyes have a punctate appearance from the development of pigment,
and the first branchial cleft is distinct. On the eighteenth day the eyes have black
pigment. A second branchial cleft occurs on the ventral side of each otocyst. The
liver has largely increased and projects into the yolk-sac. The pectorals show a distinet
rim. The alimentary canal is filamentary anteriorly, and ends blindly in an enlarge-
ment posteriorly. Three branchial clefts are visible on the nineteenth day, and the
pulsations of the heart are forty per minute. A buccal chamber is continuous with the
mesenteron, which has a flexure to the right of the embryo. The segmental ducts and
the urinary vesicle are well advanced.
The embryos emerged on the twentieth day 3 mm. in length, and with a yolk-sac
‘5 mm. in its long diameter. They attempt to progress with the yolk-sac downward,
but at rest are inverted. The black pigment-corpuscles are grouped somewhat densely
behind the otocysts, and extend backward a little beyond the commencement of the
.* In contrast with the ova fertilised on the 24th April, and hatched on the 3rd May—that is, in nine days.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 823
intestine. A line of the chromatophores passes along the infero-lateral region from the
beginning of the mesenteron to near the caudal tip, and a few exist on the dorsal part of
the abdominal region. A fourth branchial arch is visible. A delicate polygonal proto-
plasmic meshwork occurs over the surface of the yolk, as in the flounder. The walls of
the heart are thinner, and cellular strands pass backward to the liver. There is neither
mouth nor anus. ‘The alimentary, renal, and other organs have been further developed
on the third day (of freedom), and the urinary vesicle sends down a fine strand of cells,
the precursor of the urino-genital tube. On the fifth day rapid elongation of the
skeletal elements of the mandible has occurred, the head has been raised, and the cranial
flexure diminished. The point of the snout is now in the same line as the ventral
margin of the liver. The abdominal pigment has increased, but there is little change
in the rest. The oral chamber has now burst through. The otocyst presents a ridge
growing up from the floor, and a chamber descending from the roof, the otoliths lying
on each side of the former. A lenticular mark indicates the anterior nares. The
mouth gapes, but only erratic movements of the parts take place. Next day the
mandible protrudes further, and the branchial and hyoidean arches are prominent. The
yolk-sac is oval and much diminished. On the seventh day blood began to pass into
the heart, but the death of the embryos arrested further examination.
The newly hatched larvee of this species are very small, about 3 mm. in length,
and irregularly pigmented with black. They emerged in June, in about six days after
fertilisation, and are very active when free. In a week they are difficult to see when
resting on the bottom, and if stimulated they glide rapidly, seldom rising above the
bottom, or at any rate rising very little, and progressing with a jerking motion, the yolk-
sac being inferior. When at rest in the water, the head hangs slightly downward as in
other young fishes, and in descending they wriggle a little and elevate the anterior region.
They are chiefly recognised by the eyes, which are large and pigmented, and also by the
pigment passing along the dorsal edge of the abdomen as well as a faint line below the
muscle-plates of the same region.
The post-larval stages of the haddock have hitherto escaped detection, and it is only
when the fish reaches the length of upwards of 2 inches, with the characters of the adult
fully displayed, that it has come under notice. Few authors allude to the very young
stages of this form, though G. O. Sars thought he could distinguish them amongst
other young gadoids by their shorter and stouter form. CoLLErr again states that he
found the young haddocks 7 em. long under Cyanea capillata.*
Gadus virens, L.—The ova of this species have not been recognised in the ripe
condition. It is stated by Kroyer to spawn in January. In its earlier stages the green
cod probably resembles the cod very closely, and follows similar habits. When 1% inch
in length they come in large numbers to the margins of the tidal rocks about the end of
* Vide Mosrus and Heincxe, who quote without criticism the remark of Mau that the haddock spawns in shells
on the west coast of Sweden from January to March ; and that in the museum at Kiel is a shell-fish on which are
ripe eggs.
824 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
May and beginning of June, preceding the arrival of the young cod of the stage formerly
mentioned, though perhaps not always. The characteristic features of the species, as
distinguished from the cod of the same size (14 inch), have already been indicated.
They consist of a deeper green hue all over, but especially anteriorly, and a much greater
development of black pigment-corpuscles both on the body, head, and fins. The eyes
also have a greenish hue, and these are proportionally larger than in the cod. The fins
throughout are duskier from the black pigment, and the three dorsal and anterior anal
are often marked by yellow pigment-grains. The pectorals in some show traces of two
broad arches of pigment, after the manner of other larval forms, such as the gurnard and
armed bullhead, though much less distinctly. The ventrals are well formed but small,
and show no special elongation of the outer rays. When specimens of this and the cod
are viewed side by side from the dorsum the difference in regard to pigment is striking,
the green cod being almost uniformly pigmented from the tip of the snout backward,
whereas the cod shows such chiefly on the tip of the snout and over the brain. More-
over, the snout in the young cod is decidedly longer and narrower, so that with the
distinction already noted in regard to the size of the eyes the whole facies differs. In
profile the gape of the cod is the longer, the mandible apparently being longer, and the
angle more pronounced.
A curious feature was observed in those killed by a few drops of corrosive sublimate
(in acetic acid), viz., the closely adpressed condition of the first dorsal fin.
In somewhat older forms, which are abundant in the rock-pools in July and
August, two varieties oceur, viz., one of a pale though dull green along the dorsum and
upper lateral regions, the other of a dark olive-green in the same parts.*
Gadus merlangus, L.—The eggs of the whiting abound in April and May, and
probably later.t They measure 0476 in., or about 1°125 mm. In an instance
in which they were fertilised at 3.30 p.m. on April 15, 1885, the germinal cap was
found at 6 p.M., and forty minutes afterwards the first furrow had appeared. At 9 P.M.
segmentation had proceeded beyond the eight-cell stage, and soon sixteen were outlined,
the nuclei in these being apparent at 9.40 p.m. On the second day, they were in the
multicelled stage, but no well-defined nuclear zone was visible, the latter being very
distinct on the third day, The blastoderm had largely extended on the fourth day, and
on the sixth the blastopore had closed, though Kuprrer’s vesicle had not yet appeared.
Lenses and otocysts were present. No pulsations of the heart occurred early on the
seventh day, but later intermittent contractions took place. Finely stellate chromato-
phores develop on the yolk-sae.{ On the eighth day yellowish chromatophores appeared on
* Report on Trawling (1884), p. 360.
+ Day says the whiting “spawns in March not far from the shore,” though what advantage the latter situation
gives is not stated. Mosrus and Herncke observe that, according to BENKCKE, it spawns on the Prussian coast from
December to February, and in the Cattegat, according to Mam, from March to May.
t Mr Cunniycuam considers that in the larval whiting the chromatophores are confined to the body of the
fish, and are absent from the marginal fin and the surface of the yolk. His diagnosis rests on specimens captured in
the tow-net (Jour. Mar. Soc. Biol. Assoc., N.S., i.) In our experience the whiting is a form very early characterised by
its yellowish pigment, which invades the marginal fin.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 825
the dorsal region, and on the yolk-sac, near the trunk. The cardiac pulsations were
vigorous and regular. The pectorals were distinct. Next day the movements of the
contained embryos were active, and some emerged at 5 P.M., most however issuing next
day (tenth after fertilisation, viz., 24th April): they are delicate, translucent forms,
and swim vigorously near the surface. The pigment is characteristic (see p. 126).
The oldest larva reared in the laboratory is shown in Pl. XVII. fig. 12. It is
distinguished by its black pigment-spots arranged in a double series along the edges
of the muscle-plates, the inner row in each case being somewhat fainter. Dorsally the
outer row reaches forward to the mid-brain. A dense pigment-band exists in the
subnotochordal region of the abdomen. Scattered spots of considerable size occur on the
mandible, over the cardiac region, and on the ventral surface of the abdomen. As in
many other forms the dark pigment abruptly ceases in front of the caudal region. The
yellow chromatophores are distributed generally over the head, trunk, and fin-mem-
branes. The eyes are bluish silvery, the snout is still blunt, and the mandible is stout
and prominent. The subepidermal serous space over the head is well marked, and
extends as far as the anal region. ‘Three sensory organs are present in it. The otocysts
are comparatively large. The blood-corpuscles are distinct. This example nearly bridges
the gap to the post-larval forms. At this stage the great translucency of the species is
noteworthy, all the organs being most clearly observed.
The earlier post-larval stages of the whiting, viz., those immediately following larve
reared in the laboratory, are still somewhat obscure, though they probably closely approach
those of allied forms, such as the cod and haddock. The characteristic nature of the
larval pigment, however, would lead to the belief that in the brighter colours (e.g., yellow)
early differences may occur. Such, as a rule, were lost before they came under observa-
tion ; for all these delicate forms are dead and considerably altered before reaching the
deck, and the same remark applies still more decidedly to those immersed in spirit. The
pressure to which they are subjected in the large mid-water net, by the currents, and by
the weight of crowds of Appendicularians, Medusze, and Hydromedusee, as well as Cteno-
phores, would alone sufficiently explain this; nor are these dangers obviated by the use
of large wide bottles at the extremity of the net.
So far as present observations go, the young whiting appears to be recognisable as
such when from 9 to 12 mm. in length, examples of these stages occurring in August
(1886). The dorsal, anal, and caudal fins have permanent rays, and the several parts of
the two former are all outlined but not separated from each other. The pectorals form
large fan-shaped organs, but the ventrals are minute. Groups of black pigment-
corpuscles occur on the brain and along the sides of the dorsal and anal fins, while a line
runs in the median ventral region of the abdomen. The sides of the body posteriorly have
a more general sprinkling of black pigment than in the cod, which, however, it closely
approaches. No barbel is noticeable.
When about 15 mm. long the species is distinguished by a more abundant covering
of minute black pigment-specks along the sides of the body and on the fins than in the
VOL. XXXV. PART III. (NO. 19). 6.N
826 PROFESSOR W. C. MINTOSH AND MR E. E. PRINCE ON
cod, and by the greater length and diminished depth of the first anal fin. The pigment-
specks are still present in the median ventral line of the abdomen. These characters are
better marked at 18 mm., the black pigment-lines at the bases of the anal fin-rays being
especially characteristic when contrasted with the young cod, in which a median line of
black pigment proceeds from the centre of the tail forward to a point above the middle
of the first anal. No barbel is present, and the myotomes are more closely arranged than
in the cod.
At the length of 20 mm. the first anal of the young fish assumes the adult characters,
and a small papilla now indicates a barbel. The pigment along the dorsal edges is much
more developed than along the ventral. The general and minute flecks of black pigment
are very characteristic at 24 mm., and the barbel has increased in size. The denser
dorsal pigment, moreover, has spread downward over the sides, but in the preparations is
uniform; and no dappled condition was noticed when fresh.
Between the foregoing and a length of 28 mm., a decided change takes place in the
region of the pigment last mentioned, viz., a tendency to form separate touches along
the dorsum, somewhat after the manner of those in the cod. These dark touches are con-
fined to the dorsal region, though in some a few bars occur at the base of the tail. The
fish is now minutely flecked with black pigment all over the sides, head, snout, and fins,
a few large corpuscles appearing in the dorsal and the hyoidean regions—the silvery sides
and under surface of the abdomen alone being free from them. In general outline it
approaches the adult. The shortness of the snout readily separates it from the cod—
without reference to the first anal fin. A slight duskiness exists above the base of the
pectoral, but no definite spot. The tips of the ventrals reach fully to the vent. The row
of pigment-spots usually disappears from the median ventral line at the length of 30 mm.
The barbel is small but distinct at this stage.
The young whiting at 34 mm. presents the following features when contrasted with
a cod of the same length (in spirit). Externally parasitic Caligi are generally more
abundant in the cod. The median dorsal fin is less abruptly elevated than in the cod,
and the first anals diverge widely. The body of the whiting is more neatly rounded and
more plump than that of the cod, which often has a protuberant abdomen. This outline
in the whiting is probably due to its earlier maturity. Though a smaller fish it issues
from an egg somewhat larger than that of the cod. The pigment-specks closely cover
the sides of the body of the whiting and the membranous webs of the dorsal fins. The same
pigment is continued forward on the head. The pigment at the bases of the caudal rays
is more distinct in the whiting, and the lancet-like caudal termination of the body is
longer in this species. Moreover, the myotomes are coarser in the cod, and the surface
has little of the dappled silvery sheen of the whiting, apparently from the somewhat
more advanced condition of the scales in the latter. The finely stellate black pigment-
corpuscles are larger in the cod, and instead of the general specks of the whiting, they
are grouped in blotches over the surface, with intermediate pale regions, and the head
and neck are much less covered with pigment. Both pectoral and ventral fins of the
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 827
cod are shorter than those of the whiting, the tips of the latter leaving a considerable
interval between them and the anus. This abbreviation of the abdomen coincides with
the very long first anal fin, and is as characteristic of the adult as the young. The snout
of the whiting is shorter and broader than that of the cod, and its depth is greater. The
long barbel of the cod contrasts with the short process in the whiting.
At 54 mm. the pigment has increased, and the elongate tips of the ventrals pass
beyond the anus. The barbel is distinct but small. It is interesting that no young
whiting of this and previous stages has been seen without a barbel, yet Mr Day and
other authors do not allude to the subject, apparently considering that the young agree
with the adult forms in this respect. Young whiting, between 3 and 4 inches in length,
have more than once been observed with a distinct barbel, indeed, a stronger statement
may safely be made, viz., that at 34 inches some present the barbel, others do not.
The Ling (Molva vulgaris, Flem.).—The ova of the ling measure ‘066 to ‘0916 in.,
or about 1°08 mm., the oil-globule being 45 of that size. They were fertilised at sea
on the 27th April,* at 12 noon. When received at the laboratory at the forty-eighth
hour, they were in the biconvex morula-stage. They appear to be more delicate than
the ova of the cod and haddock, and many were collapsed, the contracted globe of
yolk carrying the oil-globule in its wall of protoplasm away from the inner surface
of the zona radiata. The nuclei of the periblast were about one-third the diameter
of the blastodermic cells. The zona is not so soft and tough as in the cod and
haddock, but shows greater resistance, bursting rather than collapsing under pressure.
Third Day.—About a fourth of the yolk is covered by the blastoderm, and the
rim is broad and distinct. On the following day three-fourths of the yolk are en-
veloped, and the shield is outlined ; some show metameric segmentation in the middle
region of the trunk. In the median line of the body are a number of clear protoplasmic
vesicles between the embryo and the yolk-surface. In many, the blastopore is closing,
the optic vesicles are contracted off, and the notochord ends abruptly in the pectoral
region, but terminates indefinitely at the caudal end; fifteen or sixteen somites can be
observed, but the three regions of the brain can barely be discerned. The envelope of
the yolk (blastoderm) is dotted with pale neutral-tinted corpuscles of various angular
shapes which send out processes. The blastoderm shows a double contour (probably
epiblast and hypoblast) as it passes off on each side of the embryo.
On the sixth day the lenses are in process of formation, but cannot be fully made
out. The neurula is well defined in the cranial region and has a marked keel. The
large cells of the closed rim of the blastopore persist at the posterior end of the fissure
between the embryo and the yolk. In other Gadoids, these have generally disappeared
at this stage. The blastodermie shield is reduced to a mere film on each side, but the
peculiar fan-like mass of cells and protoplasmic threads in front of the pectoral region
(as in other species) has larger and more definite cells than usual. The clear
corpuscles of a neutral tint scattered over the yolk near the oil-globule are still present.
* The ling is said to spawn on the Skagerrack in May.
828 PROFESSOR W. C. MINTOSH AND MR E. E. PRINCE ON
Rudely stellate (¢.e., with short rays) black chromatophores appear on the seventh
day (May 4), on the dorsal surface of the trunk. The vesicles on the ventral surface
still persist along with Kuprrer’s vesicle. About thirty somites are visible, and the
caudal plate rises prominently upon the yolk. The otocysts are also present and have
a circular outline. The heart is being differentiated from a protruding mass of cells
below the otocysts, and folds immediately behind indicate the mesenteron. ‘The oil-
globule projects from its pocket in the yolk, externally having a covering of blastoderm.
A central fissure occurs in each eye.
Eighth Day.—Vhe tail is well formed and is laterally flexed on the yolk. The finely
branched chromatophores form two somewhat regular dorsal lines, and five or six solitary
spots also occur over the yolk, in its outer envelope. The cardiac pulsations are faint.
The nasal bulbs are distinct, and the lenses of the eyes fully formed. Very delicate
round pigment-spots of a pale greenish-yellow colour appeared about noon, giving the
ovum a slightly greenish tint to the naked eye. These greenish-yellow corpuscles were
thickly scattered at the ventral margin, and especially on the marginal fin, almost to
the tip of the tail. Each segmental duct ends in a space above the end of the intestine,
and the anal tract sends a protoplasmic tube partially across the tail-fin, The lumen
has an external opening on one side of the caudal fin-membrane.
Next day (6th May) the embryos (PI. XIII. fig. 4) emerged, though some which
had been isolated in a small quantity of sea-water in a room escaped the previous day.
They measured about 3 mm., the yolk being 1 mm. in its long diameter. They appeared
to be delicate, many lying on the bottom, while the more active floated in the reversed
position near the surface, and were able to wriggle a little. The liver appears to be
further back than in the other Gadoids examined, the distance being nearly one-fifth the
length of the head and trunk (excluding the tail). The fine lumen of the mesenteron
extends to the opening formerly indicated. Anteriorly it ends as a fine fissure behind
the heart. About fifty myotomes are marked off, and the caudal trunk terminates in a
slight enlargement. The otocysts have thick walls, and just in front of them are two
clefts. The heart slowly pulsates. The finely stellate chromatophores in the caudal
region seem to correspond in number to the lines of the metameres.
The larvee on the 7th May presented certain peculiarities at the tip of the
notochord very distinctly, viz., a slight enlargement followed by a constriction, then a
large swelling in front of the terminal knob. The lumen of the intestine was slightly
increased, though still smaller than the mesenteron proper. The urinary vesicle (which
communicated with the rectal portion of the canal) showed continual movement of its
walls. The yolk-cortex has receded considerably from the outer envelope (blastoderm)
leaving a large extra-vitelline space, and the oil-globule (og) is also lifted away from
the outer layer. The distance of the heart and the oral region from the liver is still
marked. The heart, on the 8th May (Pl. XVII. fig. 9), was much flexed, asuming an
S shape, but no definite wall to the pericardial chamber was visible. The yolk has
diminished. On the 10th May large ramifying chromatophores occur over the yolk,
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 829
their long zig-zag processes being characteristic. Two or three extend over the whole
yolk-surface. The larva now measures 3! mm.; from the snout to the anus 1,45 mm.,
the tail being thus very long, viz., 2;4; mm. The lower lobe of the caudal fin appears
to be larger than the upper. The envelope of the oil-globule is thickened, and pigment
appears in it. The greenish-yellow pigment-corpuscles are more numerous, and have
a well-defined oval outline. These corpuscles are clear and homogeneous in vigorous
examples, but they become granular in moribund and decaying forms ; moreover, while
the black chromatophores are elaborately stellate these remain amorphous or rounded.
The larval fishes shoot upward from the bottom of the vessel, and strive to reach the
surface with more or less success, then, hanging head downward, sink slowly to the bottom.
In their upward course the yolk-sac is inferior, but when the fish is motionless it turns
uppermost and the fish descends.
On the sixth day after emergence (12th May), an indentation passes across the
nasal region, but in the earlier part of the day the mouth is not yet open, though a
fold of epiblast hangs like a curtain on each side. Later in the day the mouth appears
as a lenticular slit, cells defining its upper and lower margins.
At the end of the first week of freedom (13th May) the larval fish measures 3,3,
mm. (Pl. XVII. fig. 10). The mouth is freely open. The eyes are deeply coloured
with black pigment. An opercular fold has grown over the cleft, leaving a fissure
behind and below the otocysts, which are now spacious and thin walled. The pectorals
still have a horizontal attachment, but can be elevated and depressed; and they show
radial thickenings (fin-rays). The yolk has much diminished, and has five or six large
stellate black chromatophores, but these do not extend beyond the yolk proper (in the
cortex), whereas the yellow spots occur all over the integument. A pericardial wall
appears, and the endocardial surface is rugose. The anus now opens (?) on the lower
margin of the fin, and the space between the anus and the oil-globule is large, as the
latter has been dragged forward by the wall of the diminishing yolk, but the globuie itself
does not appear to be much smaller. Large black chromatophores occur over the mid-
brain, and a row of them begins near the root of the pectoral, and extends along the
dorsal region, ceasing above the anus. At the latter a line commences along the upper
margin of the notochord and ends a short distance from the tail, extending over 3 of the
caudal trunk. At its termination, a confused mass of elongated chromatophores trends
from the margin of the muscles outward over the tail-fin. A similar mass passes ven-
trally. A concentration of black pigment also occurs on the dorsal surface, behind and
above the otocysts.
On the 30th August 1886 very young examples of the ling (Pl. XVIII. fig. 3), about
8°5 mm. to 9 mm. in length—resembling Phycis, were captured. Along the dorsum a
slightly greenish tint was observable, with minute scattered black pigment-spots. Two
well-marked black bars pass behind the abdomen, one a short distance posterior to the
latter, and another in front of the base of the tail. They are best developed ventrally,
and do not reach to the dorsum, while a pale brownish hue surrounds them. Under the
830 PROFESSOR W. C. M‘SINTOSH AND MR E. E. PRINCE ON
anterior end of the mandible as well as on the summit of the head black spots occur. A
most striking feature is the extraordinary length of the ventral fins (vf), three of the fin-
rays in each being very long, while the fourth is shorter. The fins are of an ochre-yellow
colour along the rays, with specks of black pigment scattered over the inter-radial mem-
brane. The iris, like that of the eye of the whiting, is of a pale sky-blue. The notochord
passes almost in a straight line backward to the tip of the tail, and the caudal fin is con-
tinuous with the unbroken marginal fin dorsally and ventrally. The great development
of the ventral or permanent rays, however, slightly pushes the tip with the embryonic
radial striations upward. The hypurals, two of which are very distinct, are developing
inferiorly, and the epiurals dorsally, but they have only slightly affected the direction of
the notochord. The early development of the upper caudal rays in this form is of interest,
as it is in marked contrast with such forms as the Pleuronectidze in which the inferior fin-
rays alone appear.
The head and the eyes are disproportionately large, and the prominence of the
hyomandibular apparatus, as well as the size of the mandible, gives to the Jaws a massive
character, Just as in the cod. The angle of the jaw is especially marked, projecting
prominently inferiorly—rather behind a vertical line drawn from the centre of the lens.
The hyoidean apparatus, and subsequently the whole facies, the opercular structures, and
branchiostegal rays, are remarkably developed. The pectorals (pf) have short fleshy
bases with fan-like expansions of fin-rays of moderate length, not unlike the condition in
the adult. The barbel can barely be distinguished. The alimentary canal has a com-
paratively simple course, the capacious stomach bending to the right, whence a wide and
straight intestine passes backward nearly to the anus, then bends forward, doubling again
behind the stomach on the left side, before proceeding straight to the anal opening.
The next observed (on 21st July 1887) was about 15 mm. in length, three occurring
in the mid-water net in a haul at 22 fathoms. The pigment and other characters of
these do not require special mention. The yellow pigment is at once removed by
alcohol, but the black remains.
On 31st August 1886 examples of the next older stage (Pl. XVIII. fig. 4) were
obtained off the Isle of May. The dorsum again was greenish, and a similar pale tint
existed over the trunk and tail, while along the sides of the latter black pigment occurred.
The long ventrals extended more than one-quarter the length of the body, three rays
being especially distinguishable for their size, while three rudimentary rays were present
at the base. Their colour is similar to that of the last stage. The pigment of the
body, especially that of the two black bars above described, is now more diffuse and
continuous, the bars being however indicated by two isolated dorsal bands. The
blackish pigment in front of the ventrals is more definite, forming a broad arrow or
A-shaped figure, and at the tip of the mandible, on each side of the symphysis, a band
occurs, and a trace also is distinguishable in front of the barbel. Dorsally, a slender
stripe exists along the premaxillze, and the pigment on the cranium is better defined.
All these external features were, however, already indicated in the younger examples.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 831
At this stage the ling measures about 20 mm. in length, and the differentiation of
the first dorsal is complete, its position being as in the adult. The relations of the
second dorsal fin are similar, as is also the case with the anal and caudal, the
approach to the adult condition being marked. The tail, however, is more ovoid in
shape than in the adult. The pectorals (pf) are broad dorso-ventrally, while the ventrals
appear to be less advanced, that is, more directly under the pectorals than in the adult.
The development of the hyoidean and opercular structures alters the outline of the
angle of the mandible. At this stage the parasitic young Caligi also occur on the ling.
The next stage observed was a specimen 34 inches long, which had been stranded in a
pool on the sands in the middle of December.* The fish is now boldly striped longi-
tudinally ; thus an olive-brown band passes from the tip of the snout in a line with the
middle of the eye straight backward to the base of the caudal fin-rays. The pale ventral
surface bounds it inferiorly, while dorsally a stripe with a beautiful opaline lustre runs
from the tip of the snout over the eye backward to the base of the caudal rays. The latter
band is opaque white on the tail, and it gives the fish a characteristic appearance. The dorsal
fins are well marked, the first presenting a distinct black speck posteriorly, and another
black pigment-patch oceurs at the end of the last division. The dorsal line from the
brain backward is distinguished by a narrow edge of dull orange or pale olive, and this
brings out in relief the colours formerly mentioned. The little ling is thus a longi-
tudinally striped form, and in strong contrast with the tessellated condition of the young
cod, The barbel is proportionally large, and is borne by the fish horizontally, @e.,
projecting in front of the snout.
At a later stage, viz, from 8 to 9 inches in length, when it abundantly
frequents the rocky margins, the ventrals show three free filaments, the first shorter
than the second and third—which are nearly equal. These filaments in the previous
stage (3 inches) are worn off in confinement, indeed all the fins are frayed. The
change which ensues at this advanced stage has been formerly described by one
of us,f and may be summarised in a specimen 7# inches long as follows :—The
fish is now boldly and irregularly blotched with brown, both dorsally and_ laterally,
the region of the white stripe being indicated by the pale and somewhat scalloped area
dividing the lateral from the dorsal blotches. Fourteen or fifteen of the latter occur
between the pectorals and the base of the tail; they are separated by the whitish areas,
which thus assume a reticulated appearance over the anterior dorsal and lateral regions,
and both kinds of pigment invade the dorsal fins. The original dark greenish band is
more or less evident from the tip of the snout to the posterior part of the operculum, but
thereafter it is lost. The tail has a pale border, with a dark brownish belt of consider-
able breadth, and a few black touches in it. A broad white streak exists in the upper half
within this, but is feebly marked inferiorly. The black pigment is largely developed in the
* Third Annual Report, Fishery Board for Scotland, p. 62, 1885. Another example of the same size has since
oceurred in March.
+ Fourth Annual Report, Fishery Board for Scotland, p. 209.
832 PROFESSOR W. C. M‘IINTOSH AND MR E. E. PRINCE ON
brownish belt along the inferior margin. The black spots on the posterior part of the
first and second dorsals are very distinct, and the dark belt of the anal is densest at the
posterior end. In life the whitish streaks often have a bluish appearance.
The remarkable length of the ventrals in the post-larval ling resembles the condition
described by ALex. Acassiz, in Onus,* and in Motella.
Motella mustela, L.t-—The ova of this species abound in the sea from March to May,
and those in the tanks shed their ova freely in April. The unimpregnated egg on its
escape has a diameter} of ‘73 mm., the measurements given by Mr Brook (No. 31) ranging
from °655 to°731 mm. ‘The hyaline capsule is slightly corrugated, and the entire yolk-
surface presents a series of minute oleaginous particles. Mr Broox’s larvee emerged
on the fifth or sixth day, but at the laboratory the development was less rapid at the
beginning of May, probably from the much colder surroundings. Thus ova, in which
the blastoderm had enveloped two-thirds of the yolk (probably more than three days
after impregnation) on the 4th May did not emerge till the 11th May. Nine proto-
vertebrae were visible on the 5th, and the blastopore closed on the 6th May. The
optic vesicles were well defined, but the otocysts did not appear till 5 p.m. of this day,
the first sign of their cavity being a very fine slit. Brook gives the length of the
newly hatched larvee at 2°25 mm. About the sixth or seventh day after hatching the
mouth resembles that in the young plaice, the lower jaw projecting very much
(Pl. XVII. fig. 2). An oil-globule occurs in the small portion of the yolk still remaining.
The marginal fin is finely fibrous, and in the caudal region fine threads stand out
in the moribund animal. The notochord shows very large cells, those in the tail
being rounded and forming a single linear series, while the anterior are smaller, more
numerous, and irregular. An interesting condition of the termination of the neurochord
is seen at this time, for it exhibits a distinct lobular dilatation (ne) having a fine central
canal (mc) which can be traced a long way forward. This terminal nervous enlargement
(ne) projects beyond the end of the notochord (nc) (Pl. XV. fig. 4). The skin has a very
irregular surface many from granular papille. Three days later (May 11th) most of the
embryos had died, as they are somewhat delicate forms; but the survivors (see fig. 2,
Pl. XVII.) show a beautiful iridescent area behind the pectoral fins, probably from the
swim-bladder. The yolk-mass has been absorbed and the median dorsal fin has diminished.
The mandible (mn) is still prominent.
Proceeding to consider what may be called the post-larval stages, procured in St
Andrews Bay, we note that ALex. AGassiz,{ in one of his papers on the young stages
of “ Osseous Fishes,” in which he made known the remarkable development of the ventrals
in a form doubtfully regarded by him as a Motella, speaks of it as Motella argentea,
Rhein., though he added that it might be a species of Onus described by Court.
* Op. cit., p. 273.
+ The egg and larval form figured by Mr Cunninauam (op. cit., p. 105, pl. vii. figs. 3, 4) evidently belong to
Motella.
+ In parts of an inch their diameter is 0283, and the oil-globule ‘0033 or less.
§ Proc. Amer. Acad. Sci. and Arts, voi. xvii., July 1882.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 833
There is no uncertainty, however, with regard to the genus of the form about to be
described. It is clearly a Motella, though more probably M. tricirrata than M.
mustela,
The youngest stage captured in the large mid-water net at the end of August is
6 mm. in length (Pl. XVIII. fig. 6), and the embryonic fin (ef) is still connected with
the base of the tail both dorsally and ventrally, the specimen being apparently about
the stage of Acassiz’s, pl. vu. fig. 6. The body of the British fish is, however,
proportionally shorter and deeper. The head is large and the snout blunt, the high
arch formed by the gape being noteworthy. The mandible is large, prominent, and
protrudes somewhat in front of the snout. The hyoidean region is well developed,
though the branchiostegals are indistinct. The abdomen (abd) is very prominent and
large, and has a silvery iridescent sheen superiorly. A trace of the choroidal fissure
persists beneath each eye. Numerous blackish pigment-corpuscles occur over the
brain; but only an interrupted line extends along each side of the anterior half of the
dorsal fin. The pectorals (py) form large fan-shaped structures directed upward, and
the ventrals (vf), which are blackish in hue, are of great size; but instead of arising
considerably in front of the pectorals, as in the adult, they spring by a pale base only
a very short distance in front of the pectorals. These long black fins are about one-
third the length of the fish, and when first seen with the naked eye they resembled a
pair of powerful black spines, for the protection of the tumid abdomen. Four of the
rays, as in the American form, are largely developed. The body is of a general pale or
slightly silvery hue in the preparation studied, and the stomach contained minute
copepods. A somewhat silvery form, only 2 mm. longer (viz., 8 mm.), shows the dorsal
and anal fins almost separated from the tail. The head is now better developed, and
the delicate branchiostegals are very evident. The pigment over the brain is very dark,
and a dotted band proceeds from this region backward for some distance on each side
of the middle line. A group of pigment-specks also occurs laterally below the posterior
part of the dorsal fin. From the elongation of the body, the ventrals do not seem to
be so long. This example was procured on the 21st July at 22 fathoms, but the same
stage has been seen at the surface. In young forms, apparently pertaining to Motella
mustela, the dark ventrals show dull yellowish rays.
The next stage (Pl. XVIII. fig. 5) reaches a leneth of 10 mm., and the examples seem-
ingly belong to the same species. A silvery hue predominates over the cheeks, abdomen,
and partially on the posterior region of the trunk. | Over the brain and along the dorso-
lateral Ime the black pigment is more abundant, while a blackish spot occurs a short
distance in front of the tail. The continuity of the dorsal (df) and caudal fin (¢f) is
less prominent though still present, and the tail is more elongated—tapering slightly
towards the tip. The arch of the mouth is still high, though the forward growth of the
premaxillary region renders it less conspicuous. The black coloration of the ventrals (v/)
is confined to rather less than the distal half of each fin, and the length of these organs
is proportionally shorter in relation to the body of the fish. The eyes are really larger;
VOL. XXXV. PART III. (NO. 19.) 60
834 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
but the abdomen is less tumid than in the last stage. Specimens slightly older than
this are represented by Mr Coucn (Brit. Fishes, vol. iii. pl. eli. and p. 118) as
THompson’s midge, and were referred by the late Dr Gray to the genus Coryphena,
probably from the remarkable development of the ventrals.
Specimens 24 mm. longer than the last described, viz, 12°5 mm. in length, show a
large increase in the amount of black pigment on the dorsum, where it now gives rise
to a mottled appearance, extending over the sides and tail. Only a few corpuscles exist
near the ventral line behind the abdomen. The pectorals have increased in size and
strength, whereas the ventrals, though still of extraordinary dimensions, are now only
about one-fourth the length of the body, and are tipped with deep black, while the
remainder (#) of each fin is very pale in colour. The sides are silvery almost to the base
of the tail. In many of the specimens a parasite like a young Caligus projected from the
branchiostegal region. The youngest examples of Motel/a above described occurred in
32 fathoms water off the Isle of May, about 7 fathoms from the bottom, the others
were obtained in the same region in 25 fathoms water and about the same distance from
the bottom.
When M. mustela reaches 24 or 25 mm. in length, the general silvery hue is marked,
only the dorsum of the head and body being brownish. The five barbels are distinct,
and the tips of the ventral fins do not project behind the pectorals, though their bases
have now advanced considerably in front of the former. The eye remains comparatively
large. The specimens of this size were obtained by the surface-net in Lochmaddy.
At 29 or 30 mm. many of the adult characters have been assumed, the brownish-
black pigment having spread over the upper lateral regions. The tips of the ventrals
scarcely reach those of the pectorals, the three anterior rays being furnished with long
sensitive tips. The abdomen and lower lateral regions are silvery.
The older Motelle obtained are characterised, as Mr Day observes,* by their very
bright silvery sides and dark bluish-black dorsum. The black axillary pigment occurs
in most of these, but it varies in intensity. They range from 26 to 40 mm. That
which most nearly resembles M. tricirrata possesses a pair of very short barbels or
papillee in the premaxillary region, but sometimes one is indistinct, and they probably
disappear during the subsequent stages. The ventrals extend about as far back as the
tips of the pectorals, but their bases are considerably in front of the latter, the second
ray being the longest of the three specially developed. All the black pigment has now
disappeared. Contrasted with M. mustela of the same length, the eye is somewhat
larger, and the space between them narrower, while the barbels are shorter. The first
dorsal appears also to be somewhat shorter (from before backward). The free rays of this
fin are characteristic in all the species.
Two examples from the surface of the sea, south-east of the Isle of May, present
only a single median barbel on the upper lip. Both show axillary black pigment, and
in other respects correspond with the foregoing, except that the median barbel on the
* Op. cit., p. 312.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 835
upper lip is longer, as also is the barbel on the mandible, while the snout is less pro-
longed, the latter character being indicated by Mr Day. These examples measured
27 and 38 mm. respectively, and corresponded with Motella cimbria.
Unknown Egg with Oil-Globule (e).—A small egg, measuring 034 by ‘035, with a
single oil-globule, and in the earlier stages agreeing with Motella, was captured by the
trawl-like tow-net on the bottom in the early part of May and for some time thereafter.
As soon, however, as the pigment appeared in the embryos its distinction from the
common species (J. mustela) was evident (Pl. V. fig. 4). The reticulated cellular
appearance of the contained embyro and yolk was another marked feature.
After extrusion the larva (Pl. XVIL. fig. 4) measured about +5th of an inch, and was
characterised by the presence of yellowish pigment along the marginal fin dorsally and
ventrally, blackish chromatophores occurring amongst the rest. The tip of the tail, how-
ever, remains uncoloured, ‘The general surface of the body, head, and yolk-sac is dotted
with yellowish pigment, and a few black chromatophores are present on the yolk and oil-
globule. No pigment appears in the eyes. The oil-globule is situated inferiorly distinctly
behind the middle of the yolk-sac, but a considerable interval exists between it and the
posterior border of the latter, thus distinguishing it at once from the egg of Motella
mustela. Moreover, the entire surface of the larva is covered with a somewhat coarse
reticulation of cells with nuclei, which do not occur in the centre of the cells, but at their
margins. On the third day after hatching the mouth had not yet opened, and the only
new feature was the more general distribution of the yellowish pigment.
This larva was kept until the yolk and oil-globule had wholly disappeared. The
chief change was the more conspicuous nature of the yellow chromatophores along the
margin of the dorsal fin. The head is of a deeper yellow from the pigment over the
brain, and the body has many minute yellow chromatophores mingled with black. The
pectorals are tipped with yellow, and have the streaked mesoblastic basal region. The
eyes are greenish silvery. The mouth is widely open. At this stage it somewhat
resembles a pleuronectid.
An unknown larval fish (z) procured in February, and elsewhere* described and
figured, approaches the preceding group (Gadoids) in the large size of the silvery eyes,
which abut close on the maxillary border. At 10 mm. the notochord is straight, and
embryonic rays occur in the tail. A marginal fin occurs along the ventral edge of the
abdomen, which has a small yellowish oil-globule beneath the liver in front. Five black
chromatophores occur over the head.
YounG PLEURONECTID-®.
Hippoglossoides limandoides.—The long rough dab seems to spawn early in the
season, for during the trawling expeditions ripe specimens occurred towards the end of
March ; and some seemed to have discharged all their ova on the 21st March. Com-
* “Pelagic Fauna,” Seventh Annual Report, Fishery Board for Scotland, 1889, p. 263, pl. iii. figs. 5-7.
836 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
paratively small specimens are productive. Northern writers give the end of winter as
the spawning period,
After the stage in which the young of this species and Pleuronectids generally re-
semble the larval condition of other fishes, they begin to exhibit an increasing depth of
the body, disproportionate to their length. In the earlier stages, when about 4°5 mm. in
length, this flattening and depth of the body are diagnostic. ‘Towards the tail an
abrupt narrowing occurs, and the slender embryonic tail proceeds therefrom as a tapering
straight process bordered by the embryonic fin, which runs from the head dorsally all
round to the anus. The rays are longest at the base of the slender caudal process.
Another feature of moment is the ventral projection of the abdomen, for it extends much
beyond the line of the body as a prominent swelling. As aids in diagnosing the mutilated
young flounders of this stage are the proportionally larger eyes in the young round fishes,
and the structure of the tail; the depression of the snout between the eyes is also a
noteworthy feature. The eyes, it need scarcely be mentioned, are quite symmetrical, as
in other fishes.
The most prominent feature in the next stage is the thrusting upward of the terminal
caudal ‘‘ whip” by the development of the hypural elements and the inferior true fin-
rays. The ventral margin is also often finely dotted on each side with black pigment.
The hypural cartilages so largely increase that they form a deep vertical boundary to
the tail, the terminal (notochordal) process being bent upwards, and appearing, when
viewed externally, as a slight filament. The depth of the body at the base of the tail
has greatly increased. The left eye now shows a tendency to move forward and upward,
and a slight twisting of the frontal region is discernible, so that the symmetry of the head
is no longer perfect. Small lateral buds indicate the ventral fins.
The most advanced specimens measured about 13 mm., and when one was placed
on its side a small part of the left eye was visible above the margin of the head.
Moreover, that eye was slightly anterior to the right eye, and its axis was directed
somewhat forward. On the right side four black pigment-spots were situated at the base
of the interspinous bones, and the same number, besides specks on the body posteriorly,
occurred along the ventral region. On the left side only two were visible along the dorsal
line, and a few scattered specks along the ventral, as well as on the posterior part of
the body. The general outline of the body strongly suggested that the species was no
other than the long rough dab, but the mouth seemed to be similar to the common dab.
This latter feature may, however, readily alter afterwards. The dorsal and anal fins are still
joined to the caudal by a marginal membrane without rays. This form ranged from 5 mm.
to about 13 mm., and was captured in the mid-water net at the end of August. Next
year (1887), however, similar specimens were procured towards the end of July, and one
reached 14 mm. in length. Their distance from the shore, and the depth of water,
besides their structural features, gave grounds for connecting them with the species
mentioned. The young of the common flounder at other stages appear to approach it
very closely,
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 837
Pleuronectes limanda, L. (Dab).—The ripe forms at St Andrews have generally been
procured in April and May, but there is no reason to suppose that, as in other marine
fishes, they do not overlap these limits considerably. The diameter of the egg is
‘033 inch, or about *825 mm.
As an example we may take a series fertilised on April 30 (1885) at 2 p.m. In
these ova the perivitelline space is very small. At 4 p.m. the blastodise was formed at
one pole, and the nuclear zone covered it. At 5.30 p.m. the dise was in the four-celled
stage, each sphere with a nucleus. Scattered granules, moreover, occurred on the
margin. The morula-stage was reached at 10 a.m. on the second day (1st May), and
the granular periblastic zone surrounded the disc, the nuclei being two or three deep.
At 12.30 the disc had increased in diameter, showing finer cells in the centre, and
larger at the margin. The periblast was broader, and nuclei could be seen under the
margin of the dise by tilting the ovum. The disc had still further extended at 3 P.m.,
and the cells resembled large irregular nuclei embedded in a narrow protoplasmic
envelope. On the third day the blastoderm had reached the equator, and the em-
bryonic shield was well defined. On the fifth day (4th May) the embryo is fully
outlined, and Kuprrrr’s vesicle appears. The cephalic region has increased, but the
optic enlargements are not outlined. In certain aspects indications of metameres are
observed anterior to Kuprrer’s vesicle.
On the morning of the sixth day Kuprrer’s vesicle had considerably diminished,
and about sixteen metameres were indicated, and they extended almost to the head.
At 12.30 Kuprrer’s vesicle had sunk into the tissues of the trunk. The metameres
have a rounded dorsal outline. The notochord is distinct from Kuprrer’s vesicle
almost to the pectoral region, and slightly indicated in front of the latter. The lenses of
the eyes were faintly outlined at 1 P.M.
On the seventh day (6th May) about thirty protovertebre are clearly outlined.
The otocysts are small, but well defined, and the cavity is ovoid and limited. The lumen
of the mesenteron extends almost to the otocysts, and posteriorly it expands con-
siderably, becoming attenuated, however, before ending blindly. The neurula is cleft in
the middle line, and rises anteriorly as two bold ridges. Yellow chromatophores (round)
are scattered over the head dorsally, and extend almost to the caudal termination.
On the eighth day the eyes are boldly outlined, and the otocysts have expanded, the
oval chamber having increased in length and breath. The lumen of the mesenteron
anteriorly appears to be bifid, an arm passing towards each otocyst, but ceasing before
reaching the eyes. The protoplasm (periblast) enveloping the yolk has formed many
reticulations. At 12 noon the notchord shows lens-shaped cells or vacuoles—
partially alternate in arrangment, while at 6 P.M. it is completely segmented by bold
fissures. The yellow chromatophores are more distinct, and though iregularly dis-
tributed may roughly be described as forming a double lateral line on each side, viz., a
dorsal and a ventral. The surface in the cephalic region is rough from papillee on the
dorsal and lateral regions. The pectorals are rudely outlined, and the heart appears as
838 PROFESSOR W. C, M‘INTOSH AND MR E. E. PRINCE ON
a solid transverse column, showing, however, a core when viewed on end. Active
movements occur, so that the tail is sometimes drawn from left to right.
On the ninth day the trunk has lengthened, and the tranverse chambers of the
notochord are much longer, leaving narrow intervening bars of the original tissue. The
otocysts are larger, and show two otoliths. The cavity of the mesenteron stretches from
the otocysts to the anal region.
The heart pulsates faintly and irregularly at intervals on the tenth day (9th May).
The notochord is broken up into large and somewhat angular compartments. The
pigment-spots show further development.
By vigorous movements the embryos, measuring about y4jth of an inch in length,*
emerged on the twelfth day ; but it has to be stated that in other instances, somewhat
later in the season, and when the temperature was higher, they issued (e.g., on June 2)
seven days after impregnation. They were. carried about by the slightest surface-
currents, gently descending head foremost and again ascending by the usual wriggling
motion. The pigment-spots are very distinct, of a lemon-yellow colour as already
deseribed,t and are grouped in two lateral bands. The liver forms a pouch-like prominence
on the anterior portion of the alimentary canal. On the second day the pigment had
increased anteriorly, forming irregular blotches on the cephalic region. On the fourth
day the pectorals are about twice as large as on emergence, and an anal tract is
forming, while in many the upward flexure of the caudal region is marked. They are
about 4th of an inch longer, and swim in small groups at the margin of the vessel.
On the seventh and eighth days the chromatophores are finely stellate, and the
eye has much black pigment. The larvee are very active, though when descending they
often assume the reversed position. The snout is rounded and prominent; an oral
aperture has appeared, and the mandible slightly projects. The basal process of the
pectorals is marked, and radial thickenings are formed on the fin. The anus is not yet
open, and no circulation is visible though the heart beats actively. The hyoid is well
developed, and four branchial bars are distinct.
On the tenth day after emergence the survivors swam actively when disturbed,
using their large pectorals like flippers, but they often lay on the bottom. The dark
pigment of the eyes presents a greenish iridescence. The increase of the pigment over
the surface, the opening of the anus behind the scarcely visible yolk-sac, the great
angular development of the mandible, and the membranous opercular covering, are the
chief changes. The stomach shows tranverse folds, but posteriorly longitudinal rug
pass to the anal region. A dorsal elevation covered with papille gives a peculiar outline
to the head. The embryos survived only a few days longer. t
* Mr ConnrInGHAM (op. cit., p. 100) gives the length of the newly hatched larva at 2°66 mm. He does not allude
to the characteristic lemon-yellow coloration.
+ Page 791.
t The stages intermediate between the foregoing and the succeeding are at present no doubt confused with those
of the flounder and other forms, especially as when brought to the surface they are generally injured, or as yet have
oniy been examined in spirit.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 839
Specimens 28 mm. in length are occasionally thrown on the west sands. They are
distinguished from the flounders by their larger eyes and more elongated outline, even
when the lateral line is invisible. Others 14 inch long occurred in the trawl on June 7,
while somewhat smaller forms were found in the stomach of a gurnard on the 20th of
April.
Pleuronectes cynoglossus, L. (Witch).—Another form characterised by its com-
parative thinness, narrowness of body, great breadth of the embryonic fin, and the
conspicuous character of the dark olive pigment, was obtained abundantly. It is distin-
guished from the young of the long rough dab, by the translucency of the body even
after immersion in spirit, and by the nature of the pigment, which is finely dotted
along the ventral edge in the young dab, whereas in this form only a few (about
five) large isolated patches, blackish in spirit-preparations, occur along the dorsal
and ventral margins of the body (Pl. XVIII. fig. 7). The depth of the embryonic fin
exceeds that of the body, and the abdomen is prominent; the urinary vesicle being
very visible posteriorly. A little pigment also occurs on the surface of the abodmen,
and the marginal fin is of a faint dull yellow in life. Both sides are similarly coloured.
The caudal region is abruptly narrowed, and the notochord proceeds straight outward
even when fish is 8 mm. in length. The lower caudal rays are, however, cartila-
ginous as well as those above; all the others are membranous. The otocysts are
large and well developed. The head and abdomen, at this time, appear dispropor-
tionately large for a body so long and slender. By the development of the hypurals
the usual changes are brought about in the tail, and when the fish is 12 mm. long and
about 4°5 mm. broad (Pl. XVIII. fig. 8), the marginal fin is appreciably narrower, while
the interspinous elements appear along the edge of the trunk, and inferiorly the body
now slants from behind downward and forward, so as to embrace the gut. he ventral
fins are not yet visible. Five pigment-patches occur along the dorsal line as before,
besides some minute spots at the base of the tail. Inferiorly, on the right side, two
touches are present on the abdominal edge, and one at the curve of the rectum
superiorly ; three others lie in front of the caudal pigment-spots. On the left side
the abdominal patches are somewhat less distinct. A little black pigment also exists
on the tip of the jaw, at the ventral edge of its angle and on the prominent area below
the pectorals. The right eye is apparently a little in front of the left. The embryonic
tail remains with its superior rays, while the inferior rays (forming the main part of the
caudal fin) are well developed. Parasitic Caligi are frequently attached to the anterior
region.
When 14 mm. in length (Pl. XVIII fig. 9), the greatest breadth of the fish, including
fins, is about 7mm. The left eye at this time appears, in profile, above the head, and is
distinctly in advance of the right. The pigment-spots on the right and left sides are nearly
the same, though those on the right, perhaps, are more distinct; four patches occur
along the dorsal margin and three along the ventral margin of the body. The touches
on the abdomen are present, but somewhat altered by the growth of the tissues, and so
840 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
with those on the ventral margin as well as the head. Pigment-specks persist at the
base of the tail. The body is now proportionately broader.
In specimens 2 mm. or 3 mm. longer, similar features as regards pigment and other
points occur, but the left eye is mounting over the head, and the ventrals appear as
minute buds, while the marginal fins of the specimens are still infested by young Caligi.
These specimens were generally procured E. or S8.E. of the Island of May, in water
varying from 18 to 29 fathoms, the mid-water net being floated about 4 fathoms above
the bottom.
The earlier stages of this species have been observed by Mr J. 'T. CunnincHam,* who
secured the ripe adults in June by the trawl near Cumbrae in the Clyde. His oldest
larva, however, represents a considerably younger stage than our fig. 7, Pl. XVIIL., the
latter being about 8 mm. in length, whereas Mr Cunnincuaw’s earlier form (rather more
than two days old) measured 5°9 mm. Moreover, instead of three dark patches, there
are four on the tail. It is satisfactory to have a fairly complete series of this species,
which, on the eastern shores, is generally characteristic of deep water. Mr CunNINGHAM’s
ova hatched on the 6th day, but they were under abnormal circumstances as regards
temperature.
Pleuronectes platessa, L.—The ova of the plaice (which measure ‘065 to ‘069 in.,t or
1°65 to 1°77 mm.) were brought by Captain Burn, late of the 11th Hussars, on the 21st of
April, having been fertilised two days before. The zona radiata is minutely punctured,
and it is often peculiarly wrinkled. On the 28th the embryo is clearly outlined, and is
conspicuous by its bright canary-yellow spots (Pl. V. fig. 6). The spots do not extend
quite to the tip of the tail, but leave a considerable terminal portion bare. In one speci-
men a vesicle (kv), similar to Kuprrer’s, appeared in the mid-abdominal region, and was
thus considerably in front of the normal position. It possessed a distinct protoplasmic
covering. Moreover, a smaller vesicle appeared on the surface of the protoplasm of
the larger. The heart of the young plaice presents the same features as in other pelagic
forms, and begins to beat on the 6th day, and at 7.30 p.m. on the 28th April it pulsated
forty times per minute, Its long tubular region lies to the left side, goes forward and
forms a loop, turning backward just as in larval round fishes. The great breadth of the
marginal fin is noteworthy, and it is well seen in the egg. In several examples film-like
bands or ridges stretch across obliquely from the head of the embryo into the rest of
the blastodermie area. As the pigment develops in the eyes some are finely iridescent,
with a reddish-golden lustre, but ina day or two the silvery sheen surrounds the pupil.
The eggs are hatched in nine or ten days, and the larva is conspicuous amongst its
congeners, the flat-fishes, by its great size (Pl. XVI. figs. 5, 5a). This does not imply
that it is more readily observable, for the larvee are difficult to discern in the water.
When about a week old the canary-yellow colour seen so distinctly posteriorly is found
to be due to rounded corpuscles, which by transmitted light appear to be brownish,
and more or less opaque. The marginal fin of the larva is of great breadth, though in
* Op. cit., p. 101, pls. iii., iv., and v. + Mr Cunnineuam (op. cit.) gives 1°95 mm.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 841
ordinary views the body appears to be almost linear. A peculiar feature is the presence
of minute dark pigment-specks on the ventral lobe of the marginal fin, whereas into the
dorsal lobe (ef) only one or two of the yellowish corpuscles pass from the line of the
body. In this early stage the otoliths are remarkably small—much less, for instance,
than in the fluke of the same age. The larva swims actively at the surface of the
water, and is not easily noticed except by its large iridescent eyes, which now and
then exhibit a golden sheen. Like some other young forms already described, it floats
head downward in the water, besides frequently boring its snout into the sand at the
bottom of the vessel. When at rest it lies upon its side at the bottom, and if the
background be dark the yellowish pigment is conspicuous, especially in the caudal
region. A perceptible increase in length took place within a few days after emer-
gence. There is so little difficulty in hatching these ova, that this species could be
multiplied in any suitable locality which it did not already inhabit. Mr CunnincHam *
describes the yellowish spots as being in three rows on the lateral region of the embryonic
plaice.
In April large numbers of young pleuronectids at and near 12 mm. in length occur in
St Andrews Bay. The eyes in these are generally asymmetrical, though in the smallest
forms very slightly so. In the most advanced the left eye projects above the dorsal ridge,
but is mainly used for vision on its own side. The blackish pigment-corpuscles are chiefly
developed along the ventral margin of the body, though in some the sides posteriorly,
and the posterior half of the dorsal margin, have a few specks. The terminal region of
the notochord varies from a long dorsal filament to a mere trace beyond the hypural
elements in the older examples.
The foregoing may represent both the young of the plaice and the common flounder,
the earlier post-larval stages in spirit not yet having been clearly separated.
At the mouth of the Thames, young plaice 14 inch and upwards abound in the nets
of the shrimpers in October, and similar forms are met with at a later period at the
margin of the sandy beach at St Andrews. In June and July, at the latter place, the
smaller forms range from 24 to 3} inches, and these are probably the young of the
previous season. It is a noteworthy feature in connection with this and other species,
that the larger forms are characteristic of the deeper water, while the smaller, from 11
inches downward, abound in sandy bays (inshore water). The mature fishes (z.e., those
with the reproductive organs fully developed), as formerly shown, are thus mostly beyond
the three-mile limit.
Pleuronectes flesus, L.—No form is better adapted for studying the development of
pelagic Teleostean ova than this, though, as one of us has elsewhere pointed out,
specimens in confinement seldom deposit healthy ovat The comparatively rapid
development of the embryo (six to seven days) is further favourable for a connected
series of observations The lateness of the spawning period in 1886 was also fitted to
* Op. cit., p. 99.
+ Vide account of appearance of retained ova, Third Annual Report of Scottish Fishery Board, 1885, p. 62.
VOL. XXXV. PART III. (No. 19), 6P
842 PROFESSOR W. C. MSINTOSH AND MR E. E. PRINCE ON
bring out this feature, since the temperature was thus proportionally high. Moreover,
as indicated in the Report of the Royal Commission on Trawling just mentioned, with
reference to Hippoglossoides limandoides (Rough Dab) and other species, comparatively
small specimens of both sexes are capable of successful reproduction. Thus females not
more than 44 inches long, and males a little larger (74 inches), have been paired with
perfect success.
Ova fertilised at 4 p.m. on Ist April 1886, showed a wrinkled condition of the zona
radiata after extrusion, but soon became smooth in outline, and the germinal cap or
blastodise began to be formed. In some, however, no such protoplasmic cap appeared
for an hour or more. The two-celled stage was reached at 6 p.M., and the sixteen-celled
stage at 9.45 pM. The minute granules of the periblast were very evident in a profile
view. In these ova the micropyle was generally found near the disc. Next morning
(9 a.m. April 6) the blastoderm had made great progress, and the cells were nearly of
equal size. At 1 P.M. it had extended almost as far as the equator. At 9 P.M. a large
germinal cavity had appeared. On focussing down to the animal pole (the egg floating
with the dise downward in the usual manner), a peculiar group of cells was visible,
probably at the apex of the blastodermic cap, since the ordinary cells of the
germ lay above them. Moreover, the two ova specially under examination presented
certain (BRownraNn?) movements of the granules of the region, as if from decay,
yet such could not have been the case, as subsequent progress proved. On the
7th, at 9 a.m., the embryo appeared in the centre of the embryonic shield, as
a long curved cylinder with an expanded and thickened head. It is proportionally
longer than in round fishes, such as Gadus morrhua, G. exglefinus, and others. The
more distinct than in
cells of the blastoderm assume a honey-comb-like appearance
many Teleosteans. On the evening of the same day (the 7th) the optic vesicles are
well developed, and the tail shows a more evident enlargement in front of the tip
than in Gadus exglefinus. Kuprrer’s vesicle is present, while in many examples four
or five smaller vesicles exist on the ventral surface of the caudal enlargement. On
the 8th April, the vesicle referred to is larger, and situated just within the blunt knob
of the tail. It is a large clear bubble-like vesicle, bounded by slightly granular proto-
plasm (periblast) of variable thickness. The yellowish pigment, characteristic of this
species, now appears in the form of rounded corpuscles (Pl. XIX. fig. 5), which do not as
yet send out radial processes. Occasionally one or two clear vesicles occur under the head,
and they have the same appearance as Kuprrer’s structures. No other organs, except
muscle-plates and neurochord, are visible in the trunk. On issuing from the egg the
larvee (Pl. XIX. fig. 5) float on the surface if lively, but if feeble they rest on the
bottom in still water, 7.e., in the tanks, though it is probable that this latter phenomenon
does not occur in nature. They shoot with a wriggling motion along the surface, and
are recognised by the beautiful yellow grains of pigment; they appear, in fact, like minute
clubs of transparent tissue with chrome-yellow spots. One evident patch of colour
lies above the posterior end of the yolk, and another midway between that point and
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 843
the tip of the tail. The pigment is also scattered along the sides of the head somewhat
symmetrically, and produces a characteristic appearance.
The mandible, about the eleventh day, has the form of a remarkable process in front.
The larva differs from AGassiz’s figure of Pleuronectes americanus, and shows much more
pigment. The anus is open or nearly so. Instead of the hollow urinary vesicle behind
the rectum a merely granular band passes downward parallel to the anal tract.
After the yolk has been absorbed, the little flounder presents a somewhat deeper
aspect from increase of the marginal fin, as well as the more prominent pigment on it.
Eight touches of black pigment occur at the margin of the dorsal fin and four behind
the vent inferiorly. The large yellowish pigment-corpuscles (about eight in number) are
confined to the body, only a series of minute ones being distributed on the marginal fin, a
single speck generally existing in the centre of each blackish area. The latter are larger
ventrally than dorsally. The trunk and intestine are minutely flecked with black points.
The anterior region of the abdomen has a few yellowish specks. Ventrally about three
yellowish touches occur along the edge of the muscle-plates. The eyes are bluish silvery.
A dark mass of pigment lies internally at the pectorals, probably in connection with
the segmental ducts. The anus is at the margin of the fin. Corpuscles occur in the
heart. The mouth is widely open, and slight movements of the mandible take place.
As already mentioned, the ova of this species are very hardy, and the larve
after emergence will live for some days in a very small quantity of water, even if
unchanged.*
After the foregoing stages are passed, the little flounders are still pelagic, swimming
about with eyes on both sides of the head. Like other flat fishes, however, as they get
older they seek the lower parts of the water, though the eyes are still lateral and
symmetrical. They are obtained by aid of the mid-water net at various stages in April,
viz., some with the left eye still on its own side, though advanced a little and more
prominent ; others show the eye on the edge in front of the dorsal ; while in a third
series the left eye has gained the right side.
In April very transparent flounders, about 12 to 14 mm. in length, occur freely
in St Andrews Bay, and also in the sandy pools amongst the rocks. A few weeks
later (May 24) many occur at the mouth of the lade, which pours a fresh-water stream
into the harbour, and are caught while swimming at the surface in company with Mysvs
vulgaris, young eels, and sticklebacks. These specimens had the eye at the edge, just
as in the case of many caught in the sandy rock-pools. Moreover, each of the examples
referred to had a parasitic Anceus Hdwardi attached externally, generally near the
margin of the muscle-plates at the base of the dorsal fin. When the crustacean was
removed a deep pit in the tissues of the flounder showed the point of attachment.
Further the Anceus immediately sought a new place, and began to pierce a fresh portion
of the skin with its sharp spine-like gnathites, and tenaciously held to the fish. After
boring a little, a tongue-like process was thrust out, apparently for suction. The irrita-
* Vide remarks in Report of Roy. Commiss. on Trawling, 1885, p. 363.
844 PROFESSOR W. C. MINTOSH AND MR E. E. PRINCE ON
tion thus produced caused the flounder to dart about with great energy.* Young
flounders, colourless, and of glassy transparency, rapidly develop pigment in the laboratory.
The remarkable appearance of the tail (opisthure, RypEr), with its marginal fringe
of rays before any change takes place in the position of the eyes, recalls the condition of
the tail in such extinet forms as Kriver’s Graphiurus callopterus, in which, however,
the vertebral column is prolonged in a straight line, instead of being bent up, and the
ordinary caudal rays pass dorsally and ventrally from it. Kunrr’s form referred to, came
from the bituminous shale of Raibl in Kirmarthen.t
The young flounders proceed a considerable distance up the fresh-water stream at a
stage somewhat older than the foregoing.
If the forms observed in the muddy sand of the tidal pools, and also caught in the
mid-water net in the bay in April, are the young of the season, their growth is re-
markably rapid, even granting a much earlier period for spawning than has been observed
at St Andrews (April).
During April, May, and June, very small specimens of the flounder occur at St
Andrews in the shallow rock-pools, containing stunted Algze (Ceramiwm and other
forms), with a slight coating of grey mud. From their translucency the young fishes
are invisible, especially on the greyish silt, in which they are often partially immersed,
and, as ALex. AGassiz noticed, the two prominent eyes alone attract attention, while the
bodies of the fishes themselves cannot be seen. They are elongated and slender, about
12 mm. long and 5°5 mm. in total breadth at the widest part. At this stage the true
pleuronectid features have been assumed. They swim with the dorso-ventral line horizontal
(the right side uppermost), and dart about with rapidity, frequently in confinement leaping
over the margin of the vessel. They are fond of attaching themselves to the perpen-
dicular sides of a glass vessel, as if their left (white) side had a sucker, but the adhesion
is simply due to the muscular action of the whole surface. Both eyes are visible from
the right side, though the left eye is more or less lateral in position, or capable of looking
slightly downward. In company with them, plaice of the same length occur, being
distinguishable as broader and thinner fish, with the left eye not so far to the right,
and the ventrals as mere rudiments, while those of the flounder are well formed.
The flounder is apparently a considerably older fish, and its left side is quite white,
while in the plaice the pigments formerly mentioned occur. The coloration of the
flounder varies rapidly, and though, when first captured, their anatomy is readily ob-
served from their great translucency, yet, as indicated, a few days’ exposure to an in-
creased amount of light, from absence of shelter in the tanks of the laboratory, causes
such a development of pigment, that they are useless as transparent objects. The blackish
pigment-spots persisting after preservation, present a close approach to those in the young
plaice of the same size. Thus along the dorsal body-line five pigment-spots occur, and
four along the ventral line, almost the same number as in the former species. The general
* The food of these flounders consists of young Gammari and similar Crustaceans.
+ Sitzungsbr. der K, Akad. Wien. Naturwiss., Bd, 53 and 54, 1866, p. 155, Taf. i. fig. 1.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 845
surface of the body is, however, much more generally studded with pigment-patches and
cells, and the touches on the marginal fin are better developed. On the other hand,
except a few minute grains along the body-line, the whole left side in some is white.
The black pigment-spots in the American flounders, figured so deftly by ALEXANDER
Agassiz, show similar features, and the spots described are very generally distributed.
The difficulties in diagnosing from size alone, are well illustrated in this species.
Young forms, captured at different times, measured 9 mm. on the 15th April, 9 to 27 mm.
on the 26th April, 15 mm. on the 24th May, 8 to 30 mm. on the 8th June, 10 to 18 mm.
on the 18th June, 80 mm. on the 27th June, as well as 40 and 94 mm., while many
ranged on each side of three-quarters of an inch. In July from 22 to32mm. In August,
many captured in sand-pools near the estuary of the Eden were only 12 mm.
Rhombus maximus, Will.—The ripe ova of the turbot were procured from a female
of 12 lbs., on the 10th July, during the trawling expeditions of 1884.* They are very
small, only a little larger than those of the rockling, and the embryos, many of which
were hatched from pelagic ova of the same appearance, captured by the tow-net on the
spot, are likewise small. This seems to have been the first occasion on which ripe eggs
of this species had been procured in this country. No oil-globule is present.
A post-larval form procured in August in considerable numbers, both south-east of
the Isle of May and off the Isle of May rocks, is apparently the turbot. The youngest
example, the eyes of which are still symmetrical, measures about 6 mm., with a maximum
breadth of about 3 mm.t The larval tail projects backward and slightly upward,
and is still surrounded by the embryonic fin. It protrudes considerably beyond
the inferior fin-rays developed beneath it. The head of the fish is proportionally large, —
larger, as compared with the length of the fish, than in any other form examined. The
mouth is large. The dorsal line is nearly straight from above the otocysts to the base
of the tail, but the ventral line slopes rapidly downward from the tail to the anus, and
again rises with an anterior curve to the jaw. Thus the body has a triangular outline.
The dorsal and anal fins have rays, and are of moderate length. Papillee indicate the
rudiments of the ventral fins. Both surfaces of the body are minutely speckled with
black points, but the right is more uniformly marked in this way. The specks extend
to the marginal fins, but not over them.
The changes which follow—as seen in the next older forms—are the slight increase in
depth and roundness of the body posteriorly, the elongation of the rays of the marginal
fin, and the appearance of five or six touches, caused by aggregations of dots, in the
dorsal, the ventral still remaining speckled as before. The closely approximated ventral
fins have likewise minute black points, but the pectorals remain pale.{ The right eye
meanwhile is gradually passing upward, and the embryonic fin is rapidly disappearing.
* Vide Report, p. 363.
+ The spawning period of the turbot in the Bultic is given as May and June, but in the North Sea, July (Mosius
and HEINCKE).
+ A larval pelagic flounder of Mediterranean (Peloria riippelii, Cocco) has remarkably pedunculate pectorals, a
feature present in many young fishes (EMERY, Reale Accad. dei Lincet, Classe di scienze fisiche, math, &c., xiv., 1883).
846 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
The next phase consists in the strengthening of the abdominal wall ventrally, the
increase in the distribution of the pigment, the left side still remaining slightly speckled,
while the right is densely coloured; the more distinct grouping of the pigment in
“touches” in the fins both dorsally and ventrally, and in the progress of the right eye
towards the left. The marked notch behind the angle of the mandible, and the elevation
of the head behind the right eye, are also noteworthy features. When the right eye
mounts on the dorsum, the dorsal fin forms a high arch over it, and the body has con-
siderably increased in depth in comparison with its length. A specimen about 9 mm. in
total leneth has a depth of 6 mm. Besides the “ touches” of pigment on the fins, a
few minute blacks points are scattered over the left surface—the right being covered
with minute dots almost as densely as before.
A subsequent stage to the foregoing is shown in Pl. XIX. fig. 1, but no specimen in
our collection affords the intermediate or transition-features so as to ensure certainty by
continuity of stages. The occurrence of the pigment-touches in the dorsal and anal fins,
however, and their character, the general shape of the body, and the appearance of the
head, support the probability that they are stages of the same species. None show
traces of the spines, although the right eye has now reached the edge of the face. The
eyes appear to be larger. Though some examples are no longer, they are somewhat
better developed, a feature common in such fishes, certain individuals often reaching an
advanced stage more rapidly than others which are even larger. In such an example as
figured in Pl. XIX. fig. 1, which was 9°8 mm. in total length and 7 mm. in total
breadth, the tail measures 2°5 mm., so that the length from the snout to the base of the
tail is nearly equal to the total breadth. The right or ventral surface is pale, with the
exception of a few irregular black specks and streaks, while the dorsum is streaked across
with black pigment-bands, which have a remarkably regular arrangement, the touches in
both dorsal and ventral fins being joined by intermediate streaks, the head and abdomen
only showing scattered points. The under surface is quite pale, and thus contrasts with
the minutely speckled right surface of the specimen in the earlier stage. The dorsal
and anal fins have long rays toward their posterior border, and the body of the fish
acquires a somewhat quadrate form. The ventrals still show the pigment-streaks, and
thus are in uniformity with the anal in a lateral view. Moreover, a characteristic
larval cuticular spine appears at the posterior part of the head, above the opercular
margin, and somewhat in front of a vertical line running up from the pectoral, while
a smaller spine projects a short distance beneath. Both right and left spines are well
marked in another example a few mm. longer, and which shows a similar coloration.
They are probably protective spines, since they disappear as the fishes grow older. Their
appearance on both sides, after the right eye is at the edge, indicates the possibility that,
for some time, the fish may occasionally resume the vertical position in swimming.
Further, the presence of a young Caligus fixed to the right side supports this view. A
specimen, 20 mm. long, captured at the surface, shows the right eye just on the ridge,
with the dorsal fin close to its posterior border.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 847
When the turbot reaches a total length of 21 mm., and when the left side has assumed
the characteristic mottling of the adult, the spines above mentioned have disappeared
from both sides, and the right shows minute black pigment-specks. The right eye is
now on the left side, and the dorsal fin has advanced in front of it. The pectorals have
considerably diminished, but the ventrals retain their proportional size. Specimens
of these dimensions appear to be nearly a year old, and such are frequently found
swimming at the margin of the sea.
Our knowledge of the development of this species is meagre and very unsatisfactory.
Thus BucKLAND says that the turbot spawns in early summer, PARNELL states in spring,
and the young are seen in pools and on the surface in June and July. It is asserted in
Day’s recent work* that “the young turbot would appear to swim on its edge fora
longer period than the generality of our flat fishes;” and it is added that a specimen an
inch and a half in length (August) may be taken to be two months old. Day cites Mr
Duyn to the effect that they are hatched in June or July. “ For the first month they are
quite black, and swim on edge like a ‘John Doree.’ Then their skin commences to mottle
with white and brown, and their right eye begins to pass over to the left side of the
head. Next they become white underneath, and of a light leaden colour on the upper
surface, and during the period they remain of this shade on the back, which is until they
have passed two months of age, they swim on the surface of the sea.” Some of the
turbot of the east coast (Scotland) at any rate spawn in July. A female on the 10th of
that month, as already indicated, contained many ripe ova, which were of comparatively
small size and floated buoyantly in sea-water.t Unfortunately no male could be
procured on the occasion in question; but many ova of precisely the same size and
appearance were obtained on this ground in the tow-net and hatched, the larval
fishes resembling in all the usual points those of other Pleuronectidze. They are very
small larval fishes on emerging, and experience has shown that they could scarcely have
the size and appearance mentioned by Day in two months.
So far as present knowledge carries us, the young turbot of the season, hitherto
procured at St Andrews, measure about 11 mm.{ at the end of August. Others, again,
captured in the estuary of the Eden on the 25th July, had reached 23 mm.; and one,
from the surface, on the 20th August, 29 mm., some blackish pigment still remaining on
the right side. In April, again, specimens about 6 inches in length occasionally occur in
the salmon stake-nets. If these stages refer to a year’s growth, the latter would seem
to be slow, yet only very great irregularity in regard to the spawning period would
explain such differences.
Rhombus laevis (Brill).—No ripe brill has hitherto been seen at St Andrews, and none
occurred during the trawling expeditions in 1884, Rarrax LE considers that a pelagic ovum,
with a large oil-globule, which he procured in February and March in the Bay of Naples,
pertains to this species, and he is probably right. A similar ovum with a pale oil-globule
* British Fishes.
+ Report of H.M. Trawling Commissioners, 1884, p. 263. t Total length.
848 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
(which thus differs from that of the gurnard) has occurred in St Andrews Bay several
times in February and March. The oil-globule did not appear to be proportionally large,
and lay in the yolk under the lateral expansion of the embryo. The pigment in the
latter was well developed, and mainly yellowish, though black chromatophores were also
present; the eyes were silvery iridescent in the most advanced forms. From the
resemblance of the contained embryo to the plaice it was at the time supposed to be
that of the brill, and subsequent consideration of the remarks of other observers
have strengthened this view.
A specimen, apparently of the brill, though resembling the megrim, about 12 mm. in
length, with a breadth of about 6 mm., was procured on August 31, 1886, off the Isle of
May. The dorsal fin has about six dark bands at intervals, and the anal, which was
much injured, seems to have had similar touches. The right (ventral) surface, again,
instead of being white, is everywhere minutely dotted with black points. On comparing
with a turbot (Rhombus maximus) of the same size, the body is seen to be narrower, the
eyes larger, and the pectoral fins somewhat larger, while the comparative absence of
pigment from the dorsum, and its presence, as minute dots, on the ventral (right) side
are also diagnostic. In the former the head has less of the angular form of the turbot,
this difference being mainly caused by the roundness of the angle of the mandible, and
the smallness of the mouth. The specimen certainly resembles Arnoglossus; but the
last-named feature, the smallness of the mouth, is a point of dissimilarity.
The subsequent stages of the brill have not yet been fully investigated, and they are
not often met with in St Andrews Bay, not hitherto, indeed, till they reach 10 to 11
inches, when they are common in the local trawls in September.*
Solea vulgaris, Quensel.—On the Ist August 1884, a sole was captured 10 miles
from land (off St Abb’s Head), with ripe ova, which floated buoyantly.t No male was
obtained, so that the development could not be followed. Mr Cunnincuamy{ gives March,
April, and May as the spawning period of the sole, but he had overlooked this observa-
tion. Off the eastern shores of Scotland, therefore, the period extends from May to
August.
In the mid-water net on the 6th July a few eggs appeared for the first time along
with some of the gurnard, and they have since been more plentifully obtained by the
trawl-like tow-net on the bottom towards the middle or latter end of May. Like other
pelagic ova they are translucent, but they have the peculiarity of a more or less complete
ring of minute oil-globules in groups, of a yellowish-white colour from refraction of the
light, for when viewed by transmitted light they are faintly straw-coloured. When
floating, the ring of oil-globules is superior as in other instances, the dise being inferior.
Besides the ring mentioned, a few small groups occur here and there at other parts.
Under a lens the egg indeed appeared to be flecked with yellowish-white pigment. In
* Vide Trawling Report, pp. 358 and 361,
+ Report of the Trawling Commissioners, p. 363.
t Jour. Mar, Biol. Assoc., N.S. i. p. 18, where an excellent account, with figures, of the early stages is given.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 849
diameter the ovum measures ‘045 inch. The large oil-globules have a diameter of ‘0015
inch, while the smaller measure (0004 inch in diameter. The capsule, in a few slightly
undulated, is somewhat thick and tough, so that considerable force is necessary to rupture
it. The zona is very distinctly punctate, even more so than in that of the plaice
(Pl. I. fig. 20). In one example the surface of the zona was covered with flattened
papillz, giving it a scabrous aspect (Pl. X. fig. 7). In the early condition of the blasto-
derm the border of the yolk under it presented a few large vesicles (Pl. XXII. fig. 1),
which projected beyond the edge of the periblast, and at a later stage this vesicular
condition extended round the greater part of the yolk, except just at the tail of the
embryo. Moreover, pigment rapidly develops over the surface of the yolk as well as
on the head of the embryo, and it has a dull whitish or faintly yellowish hue, in marked
contrast to the yellow tint of the gurnard.
When the embryo is fairly formed (PI. II. fig. 11), the groups of oil-globules change
their position, most occurring along the ventral surface of the embryo, as in the egg of a
Solea (?) described by RAFFAELE (No. 125a, p. 42, Taf. 1, figs. 33 and 34).*
The oil-globules in this egg comport themselves differently from the single globule in
other eggs, e.g., of the gurnard. They do not move freely, so far as observed, at any
period of development, but retain their positions during the motions of the ovum. Their
relation to the periblast must therefore differ materially from that in the gurnard already
described. RAFFAELE considers they are in the cortical protoplasm, which divides the
vitellne segments, and move with the latter. They certainly advance with the rim,
but their subsequent arrangement under the developing embryo is a remarkable feature,
indicating, indeed, the probability that something like a streaming of the protoplasm of
the periblast takes place about the period of the closure of the blastopore, so as to carry
the globules under the developing embryo.
While in the living egg the foregoing is the condition so far as can be observed, it is
otherwise in the dead egg after the lapse of a day or two. In a dead egg at the morula-
stage, the oil-globules (now somewhat larger and of a dull yellowish colour) had grouped
themselves at the upper pole, the disc being at the lower. When the disc was placed
uppermost the oil-globules moved up to it at first apparently on the surface of the yolk,
but a more minute examination showed that they also moved through the yolk. It is
clear, therefore, that a change had occurred in the protoplasmic investment of the yolk so
as to release the oil-elobules, which to some extent had coalesced, and permit them to
pass through it.
The eggs develop with moderate rapidity, so that those with the rim about a third
over, and which presented segments in the periblast under the blastoderm (forming the
vesicular condition), hatched on the fourth day thereafter. The larval sole is a character-
istic form (Pl. XVII. fig. 13), the entire body, yolk-sac, and marginal fin being minutely
* Mr Cunnincuay, in his recent paper, describes the oil-globules as aggregated on each side of the embryo, though
there are a few groups at other parts of the surface of the yolk. He figures other stages than those given in this
paper, and shows the vesicular condition at a different period from that in our fig. 1, Pl. XXII.
VOL. XXXV. PART III. (NO. 19). 6 Q
850 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
speckled with opaque yellowish-white pigment. This pigment is arranged in interrupted
touches on the body and marginal fin (dorsal and ventral), behind the yolk-sac, so that
the pleuronectid character is early indicated. Moreover, the presence of pigment at
the extreme margin of the fin, both dorsally and ventrally, gives great apparent depth to
the body of the fish. The yolk-sac is comparatively large and globular, sustaining the
larval fish readily in the water, either as in ordinary cases (sac uppermost), or suspended
from it tail downward. Occasionally it remains in a vertical position with the head
downward. The large and rounded condition of the yolk-sac causes the active little fish
to roll over during progression, so that it often advances in a screw-like fashion. While
in lateral view the yolk-sac is somewhat ovoid, it is quite circular when seen either from
the front or the rear (Pl. XXIII. fig. 10). The same condition probably causes the larva
to make frequent gyrations. It would appear to be one of the most restless of the group,
seldom remaining quiescent under examination more than a few seconds. It is not quite
3 mm. in length. ‘The oil-globules form two main groups, one series running from the
heart obliquely backward to the region of the pectoral fin, the other at the posterior
part of the yolk, and extending ventrally along the posterior border (see fig. 13, Pl. XVII).
They slightly vary in different specimens. One or two isolated groups also occasionally
occur along the ventral border. All retain their periblastic position. No pigment other
than the superficial chromatophores exists in the eyes.
The vesicular condition of the yolk is not readily seen after hatching, though it can
be made out by manipulation of the light, or in favourable positions. The vesicles
appear to be flattened out at the margin of the yolk. In a specimen of the first day,
peculiar vesicles, having a faintly pinkish hue like those of the blastodise of the haddock,
were visible on looking down on the yolk-sac of the larval fish floating head down-
ward (Pl. XXIII. fig. 10). They were grouped in the neighbourhood of the posterior
oil-globules, and occurred nowhere else in the yolk. They differed in appearance
from the ordinary vesicles at the border of the yolk, and resembled peculiarly modified
protoplasm. Their globular condition was distinctly visible during the motions of the
larva, and they were situated in the transparent yolk within the oil-globules. One of the
vesicles presented a series of minute granules in its interior. They were observed subse-
quently in various specimens.
One example presented a vesicular process over the brain, so that it had a hooded
aspect, but this enlargement appeared to be abnormal.
On the second day the yolk has considerably diminished, and the posterior border
carries the groups of oil-globules forward with it, leaving a larger space between it and
the vent, while the pericardial chamber has become distinct in front. Minute pigment-
specks now appear in the eyes. The peripheral segments of the yolk are still indicated.
On the fourth day the yolk has still further shrunk. The cavity of the mouth is
formed, though no external aperture yet exists. The vent has not yet opened, indeed
the gut terminates a little within the margin of the fin. The clear vesicles observed in
the yolk of the former specimen were still visible, and one had a minute globule of oil in it.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 851
A feature of interest in several was the remarkable size of the optic lobes, which projected
dorsally so as to give the head a “ hooded ” aspect, as in the condition before mentioned.
The agility of the little larva is characteristic.
Three days later the activity of the larval fish had become even more marked, and it
seemed in a state of perpetual movement, the only interval being for a second or two
after a long course through the vessel. This almost ceaseless movement is probably
connected with respiration, the now widely open mouth being driven against the water
which thus rushes into it. The pectorals vibrate like those of Hippocampus (a re-
semblance the more appropriate from the dermal process on the vertex), and the tail
appears to move as rapidly. The larval soles chiefly kept the bottom of the vessel at
this stage, swimming obliquely with the head directed downward, as if boring into the
bottom or sides. Occasionally, however, a swift dart was made right across the vessel,
or a shorter one as if capturing prey. The mandible moves rapidly as in respiration.
The yolk has now diminished to a small mass anteriorly—with the groups of oil-globules
crowded together, while the posterior region of the abdomen is occupied by the viscera.
This forward progress of the yolk is interesting, for while different conditions occur in
different groups, one of the most common is the absorption of the anterior region,
and the consequent presence of the diminished yolk posteriorly. Another feature
of note is the occurrence of a prominent fold along the ventral margin of the abdomen.
The pigment seems in some to be more ochreous, and to have less of the dull yellowish-
white (like Tripoli powder) so characteristic of the early condition. Along the dorsal
margin of the muscle-plates are a series of pigment-patches, which appear to be more
numerous than in the example of the post-larval stage elsewhere described,* but variations
may occur in this respect.
As the larval sole gets a little older, for instance two days subsequent to. the preceding
stage, the pigment becomes more distinctly ochreous, and the yellow chromatophores
along the dorsal edge of the muscle-plates show signs of increase. Moreover, the pigment-
spot on the occiput so characteristic of the subsequent stage is outlined. Hight distinct
pigment-patches occur behind the former, one of the posterior (seventh from the occipital)
being larger and almost meeting that from the inferior edge. The character of the head
is as peculiar as in the previous stage, and the eyes are directed more or less forward
(forward and outward), so that the active little fish can readily see in front. The yolk
has now shrunk to a small mass under the liver—in front of the gall-bladder, and is not
easily distinguished. The change from the buff or stone-coloured, or even the dull
yellowish-white, of the early stage, to the ochreous tint of the present one is a feature of
interest. Moreover, one of the most marked changes is the disappearance of the yellowish-
white pigment from the edge of the marginal fin, so conspicuous in the early larva, and
which renders it so easily observed in a glass vessel. The speckled condition may be
associated with the more helpless stage, when, perhaps, it frequently rests on the
* Vide Ann. Nat. Hist., Dec. 1888, p. 469, and Seventh Annual Report, Fishery Board for Scotland, 1889, where a
coloured figure is given.
852 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
bottom, but this is conjectural. At any rate, the border of the marginal fin, at this
and the subsequent stage elsewhere figured, is so translucent as to be generally in-
visible, only the pigment-touches arising from the border of the muscle-plates being seen.
The other parts of the head and body, as well as the ventral surface of the abdomen, are
speckled with ochreous and black pigments. It would seem that the pale buff or yellowish-
white pigment of the early larva is transitory, for by and by the ochre-yellow, beginning
at first as very minute points over the head and body, gradually spreads and supersedes
the yellowish-white, which disappears. The differentiation between the two is clearly
seen at certain stages, the yellow being characteristic of the body, the pale buff or whitish
of the marginal fin. The pectorals have their fan-like distal regions directed forward, so
that the larva seems to row itself onward by their rapid motion. The basal parts of the
pectorals are also invaded by the yellowish pigment. The eyes are silvery with black
pupils, and a dark arch occurs superiorly. The great depth of the head and the prominent
ridge over the optic lobes are characteristic. Moreover, the skin-fold along the median-
line of the abdomen next day was marked by a central hiatus, so that it formed two
portions. Further, the anterior one in a day or two became broad and almost vesicular.
Zeugopterus punctatus.—A female example distended with ova was obtained in a pool
near the laboratory, on the 16th May. Most of the ova were unripe, but here and there a
translucent egg (Pl. I. fig. 6) occurred, especially anteriorly. They had a diameter of ‘042,
that of the conspicuous oil-globule being ‘008. Though, in all probability, not so large as
perfectly mature eggs discharged into the sea, the size is approximative. As might be
expected from the comparative scarcity of the adult off the eastern shores, the pelagic ova
are extremely rare in tow-nets ; indeed, so far as known, none have been met with.
A post-larval example, 9 mm. long., was captured by the mid-water net at 25 fathoms,
south-east of the Island of May, 30th August 1886, though unfortunately it was consider-
ably injured. It is easily distinguished from the turbot of the same size by the much
larger bright silvery eyes, and by the outline of the body. ‘The right eye is prominent
on the edge and its axis is directed laterally. The abdomen appeared to be prominent.
It is an older fish than the turbot of the same length.
The size and prominence of the eyes in the latter stage is noteworthy, for when the
fish reaches the length of 34 inches they are proportionally less, and moreover they are
deeply sunken.
Unknown Larval Pleuronectid ? (A).—When using the tow-net on July 9, 1884, ona
trawling expedition 47 miles east by south of the Island of May, and over very rich ground,
a larval fish about 3 mm. was obtained by one of us. At first sight (after preservation)
it resembled a heteropod, for a cylindrical process projected from the anterior end, and the
position of the yolk-sac and other features increased the likeness. The anterior process,
however, is a hernia cerebri, and it must be remembered that the optic lobes in the Pleuro-
nectids are prominent. ‘lhe mouth is indicated by a faint slit. The marginal fin is well
marked, extending from the front of the head to the tail, then forward to the anus. Here
it splits, a fold running along each side of the yolk-sac to the posterior part of the mandible.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 853
No form hitherto examined shows this double frill so well, a feature probably connected
with the peculiar condition of the ventral surface of the abdomen. In relation to the
latter, we have immediately below the small and vertically elongated pectorals a spherical
body, the liver, then a smaller mass (gut ?), and lastly the large ovoid swelling of the
yolk, which is closely applied to the gut above and to the rectum behind. The latter is
well marked, and appears to open by an anus at the tip.
Unfortunately the preservation of this specimen was defective and the sections unsatis-
factory, but one feature of note was observable, viz., the fact that the yolk contained a
large oil-globule surrounded by a belt of protoplasm in which were a series of small
oil-globules, which thus formed a ring round the larger central one. The lateral fold on
each side of the yolk showed epiblast outside a core of intruding mesoblast.
Certain features in this form approach those of the larval Arnoglossi, described by Dr
RAFFAELE (125a, pp. 49-55). Zeugopterus, Rhombus lavis, and probably other Pleuro-
nectids, however, also have an oil-globule in the egg.
Ovum of Pleuronectid (B)—with large perivitelline space.—This large ovum,
frequently met with in the trawling expeditions of 1884, and every year since,
is characterised by its large perivitelline space, in which the yolk with the early blastoderm
floats freely like a globule. At a later stage (PI. XIII. fig. 3) the yolk keeps the
upper arch of the egg with the embryo curved beneath. The zona radiata is com-
paratively thin, and it is sometimes difficult to obtain a clear view of the minute
punctures (Pl. X. fig. 8). It is, however, not devoid of toughness. The contained
embryo shows chrome-yellow and blackish chromatophores, the former extending nearly
to the tip of the notochord. The newly hatched larval fish has been figured and described
elsewhere,* so that it is only necessary to mention the later stages. The larval fish
during the absorption of the yolk often shows prominent processes projecting from the
surface of the yolk into the anterior space. When the yolk has been absorbed the fish
presents three distinct yellowish bars behind the vent (Pl. XVIII. fig. 2), another at the
latter (vent), and a line along the dorsum of the intestine, besides various touches of the
same on the head and elsewhere. Stellate black pigment-corpuscles occur along with the
yellow, and in the early condition are present over the yolk. ‘The eyes soon assume a
silvery aspect. The larval fish is active and comparatively large, resembling in certain
respects the plaice. It is probably a pleuronectid.
Mr Cunnineuam describes the same egg before hatching.t It is not uncommon both
in St Andrews Bay and in the open sea beyond.
Unknown Ovum (C).—Besides the foregoing, a small undetermined ovum occurred in
the mid-water net in April, and probably belongs to the same group (Pleuronectidz).
The contained embryo is comparatively large and fills up the capsule almost completely.
The larva issuing from this egg is represented in fig. 1, Pl. XVIII., the dull brownish-
yellow pigment being characteristic. Moreover, the mouth of the embryo is open at the
period of hatching—as in the plaice.
* Vide Seventh Annual Report, Fishery Board for Scotland, 1889. + Op. cit., p. 105, pl. vii. fig. 2.
854 PROFESSOR W. C. MINTOSH AND MR E. E. PRINCE ON
Clupea harengus, L., and remarks on Clupeoids.—The youngest stages (A) of the
herring were those hatched in the laboratory, 6th March 1885, and they measured 7 mm.*
They are distinguished by their elongation, by the situation of the anus, which lies behind
the commencement of the posterior sixth of the body, by the vesicular yolk, and by the
ovoid condition of the yolk-sac. The mouth is conspicuous in some, in others it is not
visible, therefore it is probable that there is diversity in regard to the degree of develop-
ment at the period of hatching, as indeed the variable length shows. The pectorals stand
at a slight angle to the body. The marginal fin is dilated in the caudal region. These
specimens seem to be larger than Dr Meyer's Baltic herring, which were only from 5:2
to 5°3 mm. in length, and the same length is given by Kuprrer.
Considerable progress had been made on the second day (stage B), for good examples
measure 8 mm., and the body is less filmy. The yolk-sac is elliptical rather than ovoid, with
the marginal fin carried forward on its surface posteriorly. A slight opacity occurs above
and below the tip of the notochord. An opaque internal process also appears some distance
in front of the anus. The mouth is a mere fissure, for the mandible is not much developed.
A faint black pigment-line runs along the ventral border from the yolk-sac to the anus.
The next stage (C) is represented by examples caught in the mid-water net at 4 fathoms
off the East Rocks, 29th March 1887. These Clupeoids are now about 10 mm. in length.
The general outline of the fish is still much elongated, the snout is blunt, the eyes
large and prominent, with a silvery lustre and a black arch of pigment superiorly. The
mandible projects considerably in front of the snout. The otocysts are so large and pro-
minent that the body appears to come off abruptly from the anterior region. The pectoral
fins are similar to those in the foregoing stage, but the marginal fin has disappeared from
the body, and a small elevation occurs on the dorsum (noticed even in examples two days
old), some distance in front of the anus. The caudal arises about midway between the
anus and the tip of the notochord (which is quite straight). Its outline is spathulate,
and there are many embryonic rays. The ventral pigment now forms a dotted line on
each side, between the pectoral region and the anus, and some specks also appear on the
ventral border of the notochordal region at the tip of the tail. The anus is at the com-
mencement of the posterior sixth of the body.
This form is evidently considerably older than the second, as the advances in the
head, the hyoidean, branchial, and mandibular regions show. The branchial arches project
freely ventrally. It is probable that it is at least a week or two older, a period which
would correspond with the deposition in March, and those captured appeared to be about
the same age, and were in great abundance amongst Sagittee, Medusze, Zoe, exuviee of
Balani and other forms. Mrysr observes that free herring at the age of a month are
17 to 18 mm. in length, so that the foregoing, according to this author, would be consider-
ably less than a month old. It has to be borne in mind, however, that there is great
variation in the growth of fishes.
* The form of these was much more elegant than the larval herring represented by Mr Cunnincuam, Trans. Roy.
Soc. Edin. vol. xxxiii. pl. i. fig. 3.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 85
Or
About a fortnight later, viz., on the 14th April, young Clupeoids (stage D) were
procured off the Pier Rocks by the mid-water net at 4 fathoms, along with a few young
sand-eels, which are distinguished in spirit by their greater opacity and the larger pigment-
spots forming an interrupted ventral line, as well as by the more or less median position
of the anus. They are now from 12 to 15 mm. in length, and show the interrupted line of
black pigment-spots from the pectorals to the middle of the body, after which the spots
are so closely approximated that they seem to form one line to the anus, which has a
speck or two externally on each side. These pigment-touches are all elongated antero-
posteriorly, those behind the middle being linear. A few specks also appear on the
ventral part of the caudal, next the notochord, and sometimes above the latter in those
most advanced. The somewhat thick notochord passes straight backward, and the
general outline remains spathulate. The embryonic fin-rays are still present, but the
ventral region of the tail shows considerable opacity from the development of the
hypural elements. A delicate narrow marginal fin is continued forward from the tail to
the vent, and from the front of the latter a thin border runs ventrally almost to the
pectoral region. Dorsally in the region of the process formerly noticed (7.e., above a
vertical line in front of the anus), a permanent dorsal fin is developing, its posterior
border being somewhat abruptly sloped, while its anterior runs into a thin marginal fin
which proceeds some distance forward. The base of this fin is opaque. The upper jaw
has increased in length, but the mandible is only slightly longer. The mouth forms a
large transverse slit. The brain and spinal cord are clearly seen anteriorly, and the
otocysts are still large. The branchiz communicate freely with the water.
At this stage the fishes are probably not less than a month old.
On the 28th April (two weeks subsequently) most have reached the length of 16 mm.
(stage E), and the depth of the body has notably increased. The dorsal fin is larger, and
so is the caudal, while the ventral opacity in the latter is also greater. The ventral and
caudal pigment is more distinct, and most specimens present a median streak of pigment
in front of the pectorals. The opercular fold is now growing over the branchiz, which
do not yet show papille. Viewed from above, the snout is broadly spathulate ; and the
alimentary canal is generally empty. Four days later all the structural features just
mentioned were better marked, and the notochord showed a tendency to bend upward
at the tip, but there was no increase in length.
A notable enlargement was observed on the 16th May (stage F), the length being
now 20 mm., and the depth in the median region of the body was much greater, the part
immediately behind the pectorals having, however, a less'depth than the succeeding, but
it was thicker transversely, so that there was less abruptness between the head and the
body. The pigment-touches along the ventral edge are much larger, still, however,
preserving their elongated shape and disposition—that is, arranged as an anterior series
of larger and a posterior of smaller specks terminating at the anus. The latter is
situated at this stage about the commencement of the posterior seventh of the body,
The snout retains its spathulate outline, the pectorals are large, and the dorsal shows
856 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
fin-rays ; the position of the latter fin, moreover, is unaltered. Behind the anus the fine
rays of the anal fin are visible for some distance. A marked thickening, forming a rounded
boss anteriorly, now exists under the tip of the notochord, which is slightly bent up.
True caudal rays occur from the latter thickened region to the tip of the notochord, the
embryonic fin completing the margin dorsally and in front ventrally. The direction of
the inner border of this hypural thickening is from above downward and forward, the
pigment marking it externally. The tail is thus being pushed upward. ‘This stage is
probably between two and three months old.
The next stage (G) at present available is illustrated by a specimen procured on
Ist July, and measuring 27-28 mm., or about 144; inch. This has now assumed most
of the characters of the adult. Thus the head has become more elongated and com-
pressed laterally, and the upward bend of the mandible is marked. The depth of
the body has much increased, so that the fish appears to be shorter, The dorsal fin
is shorter, and has an elaborate muscular ridge at its base. It stretches from a line
over the tips of the ventrals to the first third of the anal. No part of it extends
that is, it does not reach their anterior ends. A row of black
in front of the ventrals
pigment-spots runs on each side of the dorsum backward to the dorsal edge of the
caudal, The anal begins at the posterior fourth of the body, instead of the posterior
sixth or seventh, as in the earlier stages, and such is therefore a distinctive feature.
The pelvic fins arise from a point rather in front of the middle of the body, and thus
their position differs from that in the adult. The pectorals are still proportionally
large, with a fan-shaped basal region and expanded rays. The caudal is deeply
bilobed. When viewed from the dorsum the head smoothly glides into the body—from
the great increase in the thickness of the latter. The caudal is homocereal, the basal
(or hvpural) region having a double crescent, and the pigment has increased in this
and the neighbouring part of the base.
This form may fairly be considered as representing at this period the direct continua-
tion of the stages formerly mentioned, though perhaps it is an advanced one of the series.
The second series of the season commenced with two examples procured on the 30th
August. They nearly correspond with stage D of date 14th April.
On the 24th September, again, three stages occur, viz., those corresponding to stage
EK in spring; secondly, one, though only measuring 14 mm. in length, showing a further
stage of development than stage F of 16th May (and possibly a sprat), for the hypural
elements form a nearly straight vertical edge posteriorly, and the tip of the notochord
projects from the upper angle; and thirdly, one a millimetre or two shorter than stage
F, but somewhat more advanced than the previous (stage 2) in regard to depth of body,
firmness of muscle, size of dorsal fin, and especially in the condition of the caudal, which
has a straight vertical edge, with the permanent dorsal rays developing over the tip of
the notochord.
A considerable margin must thus be given in regard to the spawning period.
On the Ist of October, again, one corresponding nearly to stage 2 of 24th September
|
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 85
was procured, the posterior edge of the hypurals not being quite vertical; while the
upward bend of the notochord is in the form of a gentle slope.
Various stages were obtained on the 11th October in the same haul of the net, the
earliest being like those last mentioned (1st October). The most advanced (about 19 or
20 mm. in length) had well-marked dorsal and anal fins, vertical hypurals, and just a
trace of a notochordal spike at the dorsal edge, and therefore intermediate between F
and G (1st July).
These remarks would tend to indicate that, at least, two spawning periods, as already
known in regard to ova, occur in the neighbourhood.
Some whitebait procured in the Thames in June measured from 38 to 40 mm., and
presented most of the adult characters. These perhaps represent the young of a late
autumnal brood, though, judging from those procured in St Andrews Bay in July, a close
approach must be made by the winter broods, especially in the warmer southern waters.
Meyer’s statistics would further corroborate this view. Similar Clupeoids abound in St
Andrews Bay in March, and these may fairly be held to be the young of the previous
season, According to MEYEr’s statistics, such would be about 5 months old, but probably
they were from the ova of August, a period of seven months.
The gradual change in the position of the anus, by the elongation of the region
between it and the tail, is noteworthy, as also is the relative position of the fins in the
young and in the adult. The latter, which has been called the migration of the dorsal
forward, was pointed out clearly by SunpDEVALL and various subsequent writers, and
appears to be characteristic of the Clupeide. The recent remarks of F. RarFaELE
(No. 125a) on this subject are of much interest.
Clupea sprattus, L.—About the beginning of May numerous transparent ova having
a delicately reticulated yolk and somewhat thin zona radiata occurred in the bottom
trawl-hke tow-net. They appear to be the same as HENsEN first found in the Baltic, and
CUNNINGHAM obtained in the Firth of Forth west of Inchkeith, and which are described
and figured by him. HeEnsen truly indicates the pelagic egg of the sprat as having a thin
and transparent zona; while the larval form, he states, is distinguished from that of the
herring by a slight flexure of the intestine.* Many are not quite round, their long
diameter being ‘044 inch, and their short diameter ‘039. The reticulations of the yolk
(Pl. I. fig. 5) are very fine, and much less distinct than indicated by Mr Cunnincuam, the
margins of the sphere in an ordinary view presenting a confused series of lines. These
eggs occur in very considerable numbers, and are evidently those of an abundant species.
They are easily recognised from ova which resemble them in size by their translucency
and the colourless embryo. They develop very quickly, and the larva soon escapes as a
translucent form about 3°6 mm. in length, and, as Mr CunNINGHAM says, is at first devoid
of pigment. It is a characteristic Clupeoid (Pl. II. fig. 13), with the anus situated
posteriorly. The yolk has the same kind of reticulation as described above, and it is
comparatively large. Well-marked sense-organs are present on the sides, the last pair
* Funfter Bericht der Komission x. wiss. u. d. deutschen Meere, 1887, p. 40.
VOL, XXXV. PART IIL. (NO. 19), 6R
858 PROFESSOR W. C. MSINTOSH AND MR E. E. PRINCE ON
(opposite the anus) being larger than the others. Five pairs occur behind the yolk-sac,
while a sixth exists in front of its posterior border. These organs are not opposite each
other, but the left is a little in advance of the right. The marginal fin is not deep, and
extends a short distance on the yolk. Very fine cells are visible on its surface.
The young fishes are somewhat delicate in confinement, the oldest example reared
in the laboratory being represented in Plate II. fig. 18a—about nine or ten days after
hatching. The yolk-sac has now shrunk considerably, and the snout projects forward as
a blunt process. The surface of the yolk-sac anteriorly in one example is minutely
papillose, but this is probably an abnormality. The pectoral fin is well developed, and
the eye is slightly silvery. The mere change of these young fishes from a deeper to a
shallower vessel sutices to cause distress, with speedy opacity and death.
Ammodytes tobianus, L.—Young sand-eels were found during the Trawling Expedi-
tions in great numbers about the middle of April,* and they are similarly met with
annually in St Andrews Bay, generally at a depth of 4 fathoms.
The youngest form associated with the sand-eel was procured in the mid-water net on
the 29th March, and measured 6 or 7 mm. in length. The body is slender and elongated,
while the head is large and bluntly rounded in front. The mandible projects considerably
beyond the premaxillary region when the mouth is widely open. The pigment of the
eyes (in spirit) is black, and scarcely a trace of the silvery sheen is noticeable. The eyes
closely abut on the front margin of the snout. The notochord passes straight backward
in the centre of the tail, which has only the fine and symmetrically arranged embryonic
fin-rays. The delicate marginal fin had been injured, and only a remnant existed in front
dorsally. The pectorals are largely developed. The anus opens about the end of the
middle third of the body. Black pigment-specks are distributed along the ventral
surface, viz., a single line from the pectorals a short distance backward, then a double
line (on each side of the gut) to the anus. Behind the latter a very closely dotted line
extends to the base of the tail.
A large number of larval forms similar to the foregoing, though somewhat longer
(9 to 11 mm.), abounded in St Andrews Bay about the beginning of April, but their
identity is at present uncertain.
What appears to be the next older stage (between 8 and 9 mm.) was captured on the
14th April. The marginal fin (which occurs all round) shows no differentiation, but the
increase of the hypural elements and the true fin-rays inferiorly cause a slight upward
bend of the tip of the notochord. A single dotted line of pigment passes from the
pectorals to the tip of the tail, and a series of large pigment-corpuscles exists on each side
of the alimentary canal in the middle third. The eyes now show a slightly silvery sheen,
The mandible is still prominent. Cartilaginous rays occur in those parts of the dorsal and
anal fins behind the vent. The pectorals are very large, much larger proportionally
* Moprus and Herncoxe give the spawning season of A. lanceolatus, according to BLocu, in May, and mention that
Mato found a female with enlarged ova in June. A. tobianus, again, is said to spawn in summer (7.¢., from May to
August).
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 859
than in the adult, the basal region being massive and muscular, while the distal forms
a broad fan-shaped fin still having embryonic rays. It would appear that the relative
sizes of the basal and the distal regions of this fin vary according to the different stages
of the young fishes, the basal being especially large in the early larval condition, and
gradually diminishing as the older stages are reached. These form most efticient organs
during the purely pelagic life of such fishes. The branchial arches show small rounded
papillae (representing the branchial lamella). The otocysts are large and prominent.
This form seems to vary considerably in length in the subsequent stages, thus, e.g.,
on the 28th April, some, though further advanced in general structure, were shorter than
in the earlier condition. The snout shows less of the previous disproportion—the pre-
maxillary region having grown outward so as to project almost as much as the mandible.
The tail forms a symmetrical fan-shaped organ, the base presenting a straight vertical
line (hypural), while the upper edge is pointed, from the tip of the notochord. The
marginal fin is prominent from the vent inferiorly, and somewhat in front of this dorsally,
rising a little in each case in the middle, and diminishing toward the tail, which it
joins. Permanent rays occur in both, the anterior and posterior ends, however, being
devoid of them. The black pigment forms in front of the anus two lateral rows of large
spots, and a median more continuous series as far as the anus; while behind the latter a
row of smaller specks exists on each side of the median line. Just in front of the
pectorals a black pigment-bar occurs on each side.
At 12 mm. in length (also in April) the body has considerably increased in depth,
while the tail-fin is now more elongated, and presents a median notch. The fin-rays in the
dorsal extend distinctly forward to a line running upward from the anus, and less clearly
for some distance in front of this. In the anal fin the rays reach the anus. These fins
are at this stage distinctly separated from the caudal, and the base of the latter has a
double crescent at the edge of the hypurals. The oblique bars of pigment in front of the
pectorals, and the black pigment-spots along the ventral line are well marked, especially
in front of the anus. The anal has now a double row of minute black pigment-specks
at its base, a feature apparently coincident with the development of the rays. The
mandible slightly projects beyond the premaxille. On 28th April they ranged from
9 to 14 mm. in length. Like other food-fishes, this species is subject to the attacks of
parasitic young Caligz.
The next stage in the collection was procured in the mid-water net on the 5th May
1887, at the depth of 4 fathoms on 6 fathom ground, and they reached from 17 to 18
mm. in length, though some were less. The shape and arrangement of the pigment-spots
generally agree with those mentioned in the last stage. The tail still shows two hypural
crescents—with a dotted line of pigment running from the dorsal to the ventral edge.
The rays of the dorsal fin, though short, can be traced forward to a poimt midway
between the anus and the pectorals. The eyes are still proportionally large, and the
mandible projects in front of the premaxille. The branchiz have simple papille, with
at most traces of crenations at the sides, and the gill-rakers are developing. The same
860 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
stage was found on the 11th October 1886, so that either the spawning period is pro-
longed, or two spawning periods occur.
On the 7th May 1884, a form still further advanced was caught in the tow-net in
Aberdeen Bay, its total length being 27 mm. This would therefore correspond in some
respects with the progressive growth of the foregoing, though the irregularity in this
respect of marine as of fresh-water forms renders great caution necessary. The dorsal fin
has now nearly reached a vertical line from the tip of the pectorals, but not quite, and it
shows short fin-rays anteriorly. From the vent backward both dorsal and ventral fins
have long rays—much longer than in the previous stage. The hypural crescents are
crossed by the caudal fin-rays. The snout has grown still further in front of the eyes,
and the head more closely resembles that in the adult. The branchial processes now
present well-marked papille, and the gill-rakers are longer than in the previous stage.
The former come off nearly at right angles, but the rakers slant differently. ; inch long, the spaces being formed in very dense
and thick tissue. The walls of the auricle in Anarrhichas, as in Clupea, Gobius, and
others when + inch long, consist of a thin muscular layer lined by endothelium. In the
most advanced stage of the wolf-fish (20th June) the two valves at the base of the bulbus
are well defined. The reticulations of the conical ventricle are much finer and more num-
erous, and the fibres more distinct. With the exception of the central chamber, which
occupies about a fourth of the thickness towards the base, the whole organ is reticulated in
this manner, and the blood passes into the reticulations. So accurately do the auriculo-
ventricular valves close that in the preparation a thick column of blood projects into the
auricle, the mass being covered by a tense membranous layer, apparently valvular.
The heart in the young salmon, at thirteen and forty-five days respectively, presents
corresponding features to that of the wolf-fish, though the nuclei in the muscle-cells are
much more distinct both in the early and later stages.
When fully developed the circulation in the larval wolf-fish presents, in regard to the
vertical or what may be called the vertebral branches of the aorta, a similar arrangement to
that in the salmon, which has about 26 or 27 of them. These somewhat differ in the latter
fish in the several parts of the body. Thus the anterior branches (Pl. XXVIII. fig. 2, a)
course straight up from the aorta to the middle of the trunk, then give off the oblique
twigs (b) which proceed downward and backward so as to form the oblique lines so notice-
able in the living fish. They alternate with venous trunks (¢ and d) having the same
direction. These arterial twigs admit only a single line of corpuscles, which proceed with
great rapidity, and join the respective veins (c), and then by the larger trunk (d) debouch
into the cardinal. Beyond the oblique arterial branches just noted the vessels course
upward and slightly backward to the border of the muscle-plates, and give off various twigs
before terminating in the venous radicles. Posteriorly the oblique branches appear to
884 PROFESSOR W. ©. M‘INTOSH AND MR E. E, PRINCE ON
be less complex, and finally they form simple twigs towards the termination of the
chorda. The arterial branches along the sides of the body appear (in optical section) to
be more deeply situated than the veins.
At this time no blood-vessel extends beyond the line of the muscle-plates—including
those of the tail; indeed, it is not till the third day that three or four loops of capillaries
(Pl. XXVIII. fig. 8, aa) pass from the distal ends of the vertical vessels in the region of
the adipose fin. They increase in number about the tenth day, yet at this period none
occur in any other fin, except the tail. This is a noteworthy feature, though it is in
consonance with what ALEx. AGassiz has generally observed, viz., that the posterior
dorsal is the first to be differentiated. *
In the wolf-fish the anterior region of the intestine (Pl. XXVL. fig. 2) is supplied by a
large artery (mesenteric) d, which leaves the aorta on the right side, proceeds towards the
intestine, and bifurcates after a short course. The superior branch runs along the posterior
third of the upper part of the gut to inosculate with the main artery from the posterior end,
as formerly mentioned. ‘The other trunk passes to the lower side of the gut, and gives
twigs anteriorly as previously seen, and these terminate in veins passing upward to the
intestinal (portal) vein. A hepatic branch is also sent to the liver. Another branch (the
subclavian) is given off by the aorta in front to each pectoral. In the salmon, again, besides
this branch, the aorta sends twigs to the right and left sides of the yolk-sac. These, how-
ever, were not noticed in Anarrhichas, though they may have been present. When about
a week old, moreover, minute branches occurred in the salmon in the space between the
yolk-sac and the ventral fin. Some of these seem to come from the arterial twigs of the
sac, others from the oblique twigs on the side of the body. In the newest and most
minute capillaries in the developing fish (salmon) the blood-discs pass edgewise, and at
intervals, the rest being simply a flow of pale fluid: nothing else at least could be observed.
Caudal Circulation.—The circulation in the tail of Anarrhichas, at the stage shown
in Pl. XXVIL. fig. 2, may very well be contrasted as regards the arrangement of the
vessels with that in the salmon two or three days old (Pl. XXVIII. fig. 1), though it
has to be borne in mind that the presence of the fairly formed cartilaginous hypural
elements in Anarrhichas has an influence on the relations of the parts. The aorta (ao) in
the wolf-fish leaves the notochord just at its dorsal bend, a twig passing up, over the
chorda, a little beyond the point of departure. The course of the vessel is backward and
downward between the upper and lower hypurals. The next branch is a slender twig
(cad) which passes, with a nearly equal interval on each side at its origin, almost to the
tip of the notochord, where a few coils occur. It then enters the venous system. It is,
probably, the representative of the small artery which, about a fortnight before, went
upwards along the notochord and returned by a similar vein, as in the salmon.
At the posterior termination of the hypural fissure the artery splits
proceeding dorsally and another ventrally—the two lying nearly in a continuous line.
a branch
From these a series of more or less parallel loops pass outward and obliquely downward
* Proc. Amer. Acad. Arts and Sci., vols. xiii. and xvii.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES, 885
in a fan-like manner into the caudal expansion, the whole having a somewhat semi-
circular outline, since the dorsal and ventral branches are less prominent than the
median. A considerable margin of the tail is devoid of vessels. A downward loop is
usually formed by the vessels just described, which enter the vein, and various inoscu-
lations also occur terminally. The terminal, dorsal, and ventral series present
slight irregularities, the dorsal loops especially being broader and less definite. The
venous twigs from the arteries just alluded to pass forward in a similar direction to the
two large venous trunks running along the posterior border of the hypurals. In regard
to the axis of the body, these veins, as well as arteries, lie at an angle of about 45°,
the ventral edge, moreover, having twigs which curve even further forward. By the
union of the foregoing venous ramifications, the great caudal is formed. It lies beneath
the aorta, and follows the same curved course as the artery.
The circulation in the tail of the wolf-fish exhibits, at this advanced stage, a com-
plexity similar to that in the salmon two or three days old, and the contrast between
their rate of development is thus very great (conf. Pl. XX. fig. 1, wolf-fish newly
hatched, with Pl. XXVIII. fig. 1, salmon newly hatched). It is unlikely that the
development of the former in the egg is much more rapid than that of the latter, yet
the wolf-fish on being hatched presents only a few loops of vessels below the straight
notochord, while the salmon has attained a complexity of organisation in regard to the
vessels and the curvature of the notochord only reached by the former two months later.
Moreover, the nearly horizontal direction of the median vascular loops in the salmon is in
contrast to the obliquely downward direction of those in the wolf-fish. It must, however,
be remembered that the influence of altered circumstances (e.g., those in the Laboratory)
upon the eggs of Anarrhichas is unknown: yet other eggs with thick capsules do not
seem very readily affected by such external conditions.
The size of the arterial trunks in the tail of the salmon seems to be smaller in com-
parison with the veins than in the wolf-fish, and, moreover, the former has a large venous
sac (comparable to the caudal heart of the eel) at the upward bend of the notochord,
forming a large ovoid dilatation sloped upward and backward, and with a siphonal bend
dorsally, and a slight contraction ventrally (P]. XXVIII. fig. 1, evs). No pulsation is ever
present in it, except the impetus from the pulsations of the arteries and from the action of
the auricle. Stasis very readily affects this sac. In the somewhat older larva as much
blood passes by the vessels beneath as through the sac in these circumstances. The sac seems
to diminish rapidly, for it is indistinct on the thirteenth day, though the increased amount
of pigment renders accurate observation difficult. When about a week old, a secondary
enlargement in the form of a rounded sac sometimes occurs just behind the former.
In the more advanced condition, as at the end of March, the vessels in the tail of Anar-
rhichas (Pl. XXII. fig. 2) have become much more elongated, and more definitely arranged.
Further, instead of the obliquely downward direction of the main vessels, the whole form
a fan-shaped arrangement, the median being horizontal, as in the salmon on the first day.
The two main branches which respectively leave the aorta and join the caudal vein
886 PROFESSOR W. C. MINTOSH AND MR E. E. PRINCE ON
have now assumed a neatly vertical position, instead of being directed from above down-
ward and forward. This position is due to the changes in the upward bend of the
notochord, and the relations of the hypural elements. The regularity of the vascular loops
towards the tip of the tail is noteworthy, each correspondiag with a prominent cutaneous
frill or process of the marginal (caudal) fin.
Pigment.—On emerging from the egg, about the beginning of February, the larval
Anarrhichas shows finely stellate black pigment on the head and other parts, especially
along the dorsal region of the pronephros and alimentary canal, and behind the pectoral
fins (Pl. XXI. fig. 1); a considerable number also occur on the adjoining region of the
yolk-sac. It so rapidly increases that a conspicuous blackish band soon stretches from
the pectoral fins to the anus. The pigment just described as passing along the dorsal
line of the alimentary canal is found in section to be deeply seated, and to be scattered
near the commencement of the segmental duct—on each side of the aorta and below the
notochord. The pigment dips between the involutions of the duct anteriorly, and after-
wards forms a lining to the roof of the perivisceral cavity, splitting in the centre to
enfold the segmental ducts. It continues all the way back to the urinary vesicle,
diminishing much posteriorly, then dips in between the vesicle and the rectum and
ceases. In the case of those embryos long retained in the egg, the pigment is abundant.
The general hue of the fish is a translucent straw-colour, with the exception of the
blackish pigment just referred to. As the latter increases it is found that dorsally, in
lateral view, it becomes aggregated largely in two lines above the level of the notochord,
and gradually reaches the base of the tail. Much of this pigment is doubtless deep seated,
that is, is developed in the membranes of the brain and spinal cord.
In the beginning of April the blackish dorsal and ventral bands on the side become con-
spicuous. Each commences behind the pectoral fin, and envelops the lateral region of the
body almost to the lower border of the liver, where it is defined by a straight lie which
commences somewhat above the notochord in front, and dips slightly in its course until
it reaches the anus. It covers the entire alimentary tract, and posteriorly shows
numerous dorsal digitations. The head is now so closely covered by the stellate pigment-
spots that it assumes a dull slate-colour, and the same hue characterises the anterior
region of the body. A double line of pigment runs internally (1) along the tips of the
neural spines, processes interdigitating with them, and continuing very distinctly almost
to the end of the notochord; (2) the other passes from a point a little behind the head on
the surface of the muscle-masses, to cease a little before the other band just described.
This outer pigment-layer is within the bases of the spines (interspinous bones). Towards
the end of the month a still further increase takes place in the pigment between the snout
and the base of the tail, and it extends latterly to the ventral marginal fin. The densest
region is at the dorsal margin of the abdomen on each side, and stretching from the
pectorals to the anus. The fish laterally shows a silvery lustre (from the peritoneum),
with black touches, which form an obliquely striped arrangement (Pl. XXVII. fig. 1).
Toward the upper region of the abdomen the colour progressively increases, so that about
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 887
the 1st of May the upper arch of the cranial cavity, and a considerable portion of the sides
superiorly, are covered with continuous pigment. It extends along the spinal cord—en-
veloping two-thirds of its surface dorsally—while the lower aspect is free from it. The
abdominal cavity has a continuous coating on its silvery peritoneal surface, and the same
occurs, as previously noted, round the segmental organs. A dense layer of pigment also
lies beneath the skin, over the muscles, and posteriorly the upper arch splits to send off a
layer to the tip of the interspinous bones. The latter layer ceases a little above the bases
of the V-shaped fin-rays. There is considerable variation in the pigment, some specimens
towards the end of June, with the yolk-mass completely absorbed, presenting in trans-
verse section, besides the continuous layers, large isolated pigment-masses here and there,
breaking the continuity of the layer, both in the subcutaneous and peri-nervous regions.
The silvery sheen extends a short distance over the yolk-sac. The dorsum of the
head is deeply pigmented, while the sides are less so. A little below, the lobes of the
brain are outlined by their blackish pigment. About the middle of May, the con-
dition of the young fish is shown in the figure before mentioned (Pl. XXVIL. fig. 1). The
pigment on the dorsum and sides is dull blackish or a uniform dull grey, with black specks.
The abdomen is silvery and iridescent, as well as dotted with black pigment-corpuscles. The
pectorals have a little pigment at their bases, and the same is present along the bases of
both dorsal and ventral marginal fins, the former being definitely banded. The tail is still
translucent. The iris is iridescent silvery, with black pigment—chiefly visible superiorly.
When about five inches in length, the dorsal fin has about a dozen black spots at inter-
vals, the anterior being nearer the free edge than the posterior. The sides are also marked
by a somewhat reticulated arrangement of spots which, in a few instances, coalesce to form
bars. The lateral dark patches proceed from those in the dorsal fin, and meet when about
a third of the body is traversed, and then they form a single or double band to the ventral
border, which is devoid of them. The increase in the pigment, e.g., at six inches, demon-
strates how, from the former arrangement, the bold stripes on the sides and dorsal fin of
the adult are formed. The hue of the latter must render it very much in harmony with
its surroundings on rough hard ground amidst stones and zoophytes.
In the young salmon we find many points of contrast at this stage. The pigment
on the head is much developed on extrusion from the egg. A few black pigment-
corpuscles occur beneath the cranial tract and along the spinal cord, but they are
isolated, and often in the abdominal roof only a single one occurs in a transverse section
of the fish. In this region, also, a line of pigment passes dorsally on each side of the
median (embryonic) fin. A few, again, occur at the base of the ventral median fin. Both
cease before reaching the tail. The young salmon at this period is of a translucent pale
yellowish hue, with a tinge of pink, while a considerable number of pigment-corpuscles
are present on the head, and a chain of them along the neurochord. The large oil-
globule is of a dark orange-colour. The pigment very soon becomes denser at the upper
part of the yolk-sac, as well as over the body of the fish. The indications of the “ parr-
marks” occur at the third week. A little later (fourth or fifth week) the pigment
888 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
is much increased, especially at first over the opercular region, and other parts of the head.
The “ parr-marks ” on the sides are eleven in number, though, from the close proximity
of several, they do not appear to be sonumerous. They are not symmetrical on the sides,
the fourth being double on the left side, whereas it is the third that is so on the right in
the specimen examined. Along the dorsum the pigment is arranged in a double chain,
while the head shows an hour-glass pattern. The black spot on the operculum is well
marked. The tail laterally and posteriorly exhibits a brownish-pink hue from the presence
of the reddish pigment-corpuscles. These latter are likewise distributed on the general
surface of the body and on the dorsal fin.
About a fortnight later the entire body is covered with pigment-corpuscles, which are
larger and more closely aggregated at the “ parr-marks.” Minute glistening granular
bodies also occur in various parts of the integument. The dorsum anteriorly has a con-
siderable member of pinkish-red corpuscles, giving it a reddish tint to the naked eye.
Small corpuscles of the same hue occur in the “fatty” fin, in which the vessels ramify
very plainly.
Along the dorsum (behind the pectorals) are seven pigment-masses. The first, imme-
diately behind the pectorals, is large and distinct. The second, also distinct, is situated
at the anterior part of the dorsal fin, covering a space in front and a portion on each
side of the fin. The third has similar relations to the posterior part of the fin, besides
proceeding some distance behind it. An elongated and less defined mass follows, in front
of the “ fatty ” fin, and connected with a smaller patch at the anterior border of the fin,
which proceeds a short distance on either side. Eight fairly definite lateral bars are
present on the left side, with a less evident ninth bar at the tail. On the right, likewise
are nine, the sixth being placed a little behind the (posterior) margin of the dorsal fin, and
so elongated and large as to appear double or compound. The ventral surface is silvery
white, and the general colour of the back greenish. Scales are now present on the
dorsum, and mucus scraped from the surface is found to contain many flat nucleated cells
(epithelium) of a delicate transparent character, with a large granular nucleus, and one or
more nucleoli.
The young salmon, about a month older, shows a little variation in the “ parr-marks.”
Thus, in some eleven occur on the left, while nine are present on the right side. The
dorsal pigment remains much the same as above described. A reddish tint is still observ-
able at the margin of the fins. The young fishes, however, differ somewhat in size and
colour, some being quite light, others very dark under the same conditions. In many
examples a large yellowish patch occurs in the posterior part of the cranial region, while
in front is a greenish-yellow area. The usual changes in tint, however, are observed on
removal from a darker to a lighter situation, except in sickly or apparently dying fishes.
The round glistening bodies composed of transparent granules are still abundant.
The pigment of the two species mainly considered in the preceding pages offers a few
interesting features to which brief reference must now be made,
The young wolf-fish is uniformly tinted, or at least exhibits no bars, in the stages up to
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES, 889
the length of 1} inch ; whereas the adult wolf-fish is boldly barred with dark pigment.
On the other hand, the young of the salmon, as well as of allied species, are just as
prominently barred in their larval state, as they are uniformly tinted in their adult con-
dition. We have seen that the young cod is at first boldly speckled, and later is definitely
tesselated, whereas in its adult state the tints are more or less uniformly arranged.
The ling (Molva vulgaris), again, after the ochre-yellow colour of the early embryo—a
colour which extends along the enormous pelvic fins of the subsequent stage—becomes, in
a more advanced condition, beautifully striped, and still later is barred in a most striking
manner, while the adult form is almost as uniformly tinted as the cod. The young green
cod (Gadus virens) is, however, uniformly tinted both in its young and adult condition,
the larval stage not yet having been described; and, as far as is known, the haddock and
whiting (Pl. XVII. fig. 12), after the absorption of the yolk, do not exhibit any divergent
feature in regard to colour. On the other hand, the young gurnard (7. gurnardus) shows
little that is noteworthy in the pigment of the early stages, but when ? inch in length it
is characterised by the remarkable crescentic disposition of the pigment on the pectoral
fins. The dragonet (Callionymus) is less beautifully tinted in the young stages than in
the adult, but it is noteworthy that the ventral surface of the abdomen is blackish in the
post-larval stage—white in the adult.
The rocklings (Motella) are distinguished by their remarkably long ventral fins, the
base being white and the tips black. In the Plewronectide there is a tendency to
transverse rows of blackish spots, as in the turbot (Rhombus maximus), or in an earlier
stage to dots along the bases of the marginal fins, both dorsal and ventral.
The Integument.—Few features of interest are found in the integument of other post-
larval forms, as the scales appear to be late in developing, and the various dermal and
epidermal strata are not readily distinguished. In some forms, as in Callionymus, } inch
long, and Cyclopterus, large cellular spaces occur from the snout to the tail—developed
probably in the Malpighian stratum of the integument, and by their increase in size they
are pushed towards the surface. Their contents are usually clear in stained sections ; but
in Cyclopterus they are coloured very deeply by Beale’s carmine, and in all cases are
probably glandular. In Cottus, 3 inch, also very large spherical cells of a similar character
appear ; and in the post-larval Labrus, 3%; inch in length, they are most numerous over
the frontal and epiotic regions.
Serous Spaces.—In the early larval condition of certain forms considerable serous
spaces occur in the dorsal regions of the head and trunk, but they gradually diminish,
and lymphatic fluid appears to collect in chambers, often of large capacity, which occur as
in the post-larval gurnard when 4%, inch in length, between the roof of the mouth and the
cranial floor. A blade-like plate of hyaline tissue is developed in the membrane arching
over the two supra-oral cavities. Each plate is placed at an angle, and abuts on the
posterior median process of the rostrum. Again, in the cod, $4 inch in length, a large
lymphatic chamber occurs behind the urinary bladder, and a network of connective
tissue occupies the contained space. Around the fore-part of the membranous cranium
VOL. XXXV. PART III. (NO. 19). Gax
890 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
in Pleuronectes flesus, ;°; inch in length, a space occurs—evidently filled by gelatinous or
lymphatic matter with widely separated nuclei.
Pectoral Fins.—In the larvee of the wolf-fish hatched at the time the eggs were obtained
(viz., January) the movements of the pectoral fins (Pl. XX. fig. 5) were as active as those
in the salmon on its escape from the ovum. Their motion within the egg, however, was
not noticed at this period. As the season advanced these organs showed more vigorous
motions, and were kept in rapid vibration when swimming. On the Ist of April they pre-
sented a crenate margin, and before the end of that month attained great development as
large fan-shaped expansions, but during the stages under observation their axes remained
more or less vertical, as indeed they are in the adult. A comparison with the salmon is
interesting, since, in the wolf-fish, the pectorals remain very large throughout life, whereas
in the adult salmon they are of moderate dimensions. Viewed laterally in the newly-hatched
salmon (Pl. XXII. fig. 4) they are very prominent, rising above the line of the dorsum and
its median marginal fin. In vertical transverse section their tips far exceed the dorsum,
and thus they present a great contrast to those of the wolf-fish, which do not at this stage
reach so high. Their plane is nearly parallel with that of the body, and they are more or
less rounded in form, On the fifteenth day they show embryonic fin-rays, and distinetly
droop to the sides, and do not extend so much above the dorsum (Pl. XXII. fig. 8).
As development proceeds, they gradually increase in size, and by the rotation of their
axes they, in the fourth or fifth week, assume a horizontal position (Pl. XXII. fig. 10).
They form, indeed, two shark-like organs which, when the fishes are resting on the stones
at the bottom, are often moved in a reptant fashion, after the manner of Chelonian fore-
feet. Moreover, the fin of the parr, at a somewhat later stage, becomes less rounded
(more lanceolate) than in the earlier form. In horizontal sections of post-larval Gadoids,
+4 inch long, the free fin-plate of cartilage is separated by an interval from a proximal
(coraco-scapular) plate, internal to which is the hyaline clavicular rod. The interval
referred to is filled up by deeply stained cellular tissue which forms a thick protruding
band.
Ventral Fins.—A similar change takes place in the shape of the ventral fins in the
salmon, from the rounded form of the seventh day salmon (P1. XXVIIL. fig. 2) to the lan-
ceolate outline of the adult. These organs (ventral fins) are sometimes used for support
when resting on the bottom. In the early larva only the embryonic fin-rays are present, but
at the end of the third or fourth week there is externally a pale margin, with few cells, which
increase from without inward until a mass of cells—traversed by the fin-rays—appears.
The ventral fins in marine fishes develop late in larval life, one of the most rudi-
mentary stages occurring in a post-larval Ammodytes (?), + inch in length. On the
flattened ventral surface two angular knobs appear laterally below the posterior hepatic
region. In transverse section the epidermic evagination exhibits an inner columnar layer,
with a dense central core, limited internally by the thin peritoneum. A similar appearance
is presented by the ventral fin-buds in Gastrosteus spinachia at a late larval stage. In
Pleuronectes flesus, .°; inch in length, the buds are more advanced and have the form of
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 891
ventrally directed flaps on each side of the diminishing median embryonic fin-membrane.
In the central core above referred to, a simple bar of cartilage passes downward from a
point immediately below the peritoneum, at the anterior border of the liver, and ends,
near the tapering margin of the fin-bud, in a dense aggregation of small cells deeply
stained in the preparation. In a Gadoid, 3? inch in length, similar cartilaginous plates
appear, not, however, in bold projecting flaps of the integument, but in flattened hori-
zontal ridges; this difference in position being due, no doubt, to the flatter and more
obtuse character of the ventral surface in the post-larval Gadoid. Posterior to the paired
cartilaginous plates, which have an upper and a lower muscular mass, an expansion of
the integument forms a membranous fin supported by four or more hyaline rays. The
fin-rays at this time consist of paired hyaline rods, semilunar in transverse section, each
pair enclosing a strand of dermal tissue. A still later stage is seen in the post-larval
goby, 3% inch long, in which the two basal skeletal rods of the developing ventral fins
approximate, and are united posteriorly, forming an angle, with the apex directed back-
ward. Thus early is the union of the ventral fins effected which results in the disk-like
structure characteristic of the adult. The liver lies immediately over the developing
ventral fins, which are slightly anterior to the position they subsequently occupy.
Median Unpaired Fins.—In the larval wolf-fish the marginal fin-membrane
commences behind the head in a position similar to that in the salmon, and extends
all round to the anus, and again forward in front of it to the yolk-sac. Proportionally
it is much less developed than in the salmon, and while the changes in its outline in the
latter are complex, those in the wolf-fish are less so. Moreover, whereas the marginal
portion of the tail of the salmon does not increase much at the period of absorption of
the embryonic fin, the contrary is the case in the wolf-fish, whose caudal expansion
attains large dimensions as the fin of the body diminishes. Whether this is altogether
due to the increase of the marginal web of the tail, or absorption in the other parts, is
doubtful. Probably both causes are concerned. The embryonic fin-rays appear first in
the caudal region, and afterwards in the anterior region. As the larval fish increases in
size, the marginal fin remains stationary, its further apparent diminution being due
merely to the general increase in the bulk of the body. It, however, increases in
thickness, and spinous rays are developed during the second month. On completing the
larval phase, z.e., on the absorption of the yolk in the beginning of June, the number of
dorsal spines is seventy-one; the first pair are separate, and the second diverge at the
tip, while the last is single and small. The ventral spines are forty-four in number, and
the last likewise is single and small.
In the salmon the marginal fin (Pl. XXIL fig. 4) shows, on emergence, considerable
differentiation. Thus the first dorsal is well marked, though it has only the granular
structure characteristic of the rest of the fin. The adipose fin is indicated by the eminence
situated between the former and the caudal, which is somewhat lobate, and generally
shows a slight notch above the tip of the notochord, marking, apparently, the homologue
of the embryonic tail-fin. The anal is distinguished by an elevation posterior to the anus,
892 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
and a similar prominence (pre-anal) corresponding to no structure in the adult fish, and
not comparable to the first anal of the Gadide, occurs between the ventral and the anus.*
When a week old, these portions, which correspond to the regions of the permanent fins,
are denser, the other parts being very thin, and apparently undergoing absorption.
The embryonic rays are now distinct. Meanwhile the blood-vessels begin to ramify
in the “fatty” fin (Pl. XXVIII. fig. 3), and the capillaries in front and behind the
primary series are on the ninth day increased; they soon, indeed, extend throughout the
entire length of the fin. Several indications of true fin-rays occur in the first dorsal, and
at the end of a fortnight the embryonic marginal fin has, to the naked eye, nearly
disappeared, so that the permanent fins are more boldly marked. Pigment appears in
both dorsal fins at the same period; while pale capillaries ramify in the anal fin, and
stretch nearly to the tip. They probably also develop in the dorsal and ventral; but
they were not seen. The marginal (embryonic) fin is now almost absorbed, except in
the interval between the ventral fin and the anus.
Between the fourth and fifth weeks, the dorsal and anal fins show the cartilaginous
rays, while the membranous parts between them are widened and coloured by numerous
yellow and brownish pigment-corpuscles. Thirteen rays occur in the dorsal, and the
same number in the anal fin, and the interspinous elements produce wavy marks beyond
the muscle-plates. Both fins have crenate borders, as in the tail at this period; while
the adipose fin presents a fibrillated aspect, and has a network of fine blood-vessels. All
the fins are proportionally larger than in the adult, as observed in the outline of an
average specimen (Pl. XXII. figs. 10 and 11). In minute structure the dorsal and other
fins already present most of the characters of the adult. Thus, at the anterior part of
the dorsal, are two narrower and shorter rays, the first a simple spike, the second con-
sisting of two which form a loop. At the base of the larger rays is a projecting median
point, and the terminal process is long, and almost unciform. The pigment is chiefly
placed on the cartilaginous rays.
In considering the condition of the median fin-rays of these young fishes, it will be
observed that on the thirteenth or fourteenth day the dorsal of the soft-rayed salmon
corresponds nearly with the condition in the adult, but in the anal fin the number of rays on
the tenth or the twelfth day, viz., thirteen, is in excess of the number in the adult. In this
respect, however, it is doubtful how far authors in numbering the rays have anatomically
examined the parts, or how much they have depended on external appearances. On the
other hand, the osseous rays in the dorsal of the young wolf-fish seem, if Day be right,
to be fewer than in the adult, viz., 71 as compared with 72 or 74 (Day), while the rays
in the anal present a similar condition, viz., 44 in the young as against 45 to 46 in the
adult. An examination, however, of the skeleton of a fine adult in the University
Museum here shows that the number of the dorsal fin-rays exactly corresponds with that
of the young forms just mentioned, and so with the ventral. There may be variation ;
* The outlines of the fins of the young salmon seem to differ considerably from those of the larval Lochleven
trout, as shown by Mr J. T. Cunninawanm, Trans. Roy. Soc. Ldin., vol. xxxiii. pl. i. fig. 4.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 893
but it is remarkable that so little exists. Mr Day ™* had, therefore, certain grounds for
stating that fin-rays do not materially increase with age.
The condition of the growing rays and of the interspinous elements in certain other
post-larval Teleosteans is interesting. Thus, in a section of the caudal trunk of a
gurnard, 3%; inch long, four series of interspinous cartilages are developed in the
connective-tissue strand which extends upwards from the neural arch. The neural spine
is the proximal element, and has the form of a rounded nodule clothed on each side by a
plate of hard hyaline tissue. The third nodule in the series is large and irregular, and
like the second presents a cartilaginous structure only ; but the highest nodule, lying at
the base of the 2nd dorsal fin, exhibits on each side a horizontal hyaline plate passing
outwards parallel to the plane of the flattened dorsum. ‘The fin-rays are paired rods of
hyaline tissue, and at this time each rod is separated from its fellow by intervening
tissue. Hach of the cartilaginous elements just described has its special muscular strand
on each side, and it is possible that they may at a later stage unite to form one javelin-
like neural spine. Further forward, indeed, the neural spine does develop as a single rod
of cartilage surmounted by a nodule of the same tissue which is trifid superiorly. In
Cottus quadricornis the neural spine in the mid-trunk region is cartilaginous, with one
superior (interspinous) element; but the neural arch itself is formed by two dense
hyaline arms which grow out from the perichordal ring of the same tissue. In the post-
larval goby (Gobius ruthensparri) the interspinous element appears before any neural
arch or spine is developed, and it has the form of a rounded nodule at the summit of the
connective-tissue continuous with the perichordal sheath. In the young wrasse, j4; inch
in length, no supra-neural cartilage appears at all in the region of the dorsal fins. The
fin-rays are, as usual, formed by the union of paired hyaline rods, having a semilunar
form in transverse section—the concave surfaces being opposed, and the neural spine, as
will be described later, is formed of hyaline matter.
On escaping from the egg the tail of Anarrhichas is more or less lobulated, though
in many it is lanceolate. A distinct constriction (Pl. XX. fig. 1) occurs in front of the
organ, which then gradually widens out—the dilatation being more marked inferiorly
than superiorly. The notochord goes straight backward from the nuchal curve to the
commencement of the caudal region proper, and then tapers to the termination, the axis
of this part being in the same line as that in front, viz., horizontal. In many views,
in newly hatched forms (January), a slight fold appears at the margin of the caudal fin,
in a line continuous with the notochord ; but whether this is a definite structure or not
is uncertain. All that can be said is that the appearances indicated in the figure
(Pl. XX. fig. 1) were frequent, and recalled the notch above the tip of the notochord so
familiar in the larval salmon. Structurally the tail, at this stage, presents a minutely
cellulo-granular appearance (due to the cutaneous elements), most marked in the thicker
central region, and becoming translucent towards the margin. The embryonic fin-rays,
* [It is with deep regret that the authors have just received intimation of the death of this experienced and meri-
torious worker in the field of Ichthyology—both British and foreign. ]
894 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
like fine fibres, radiate over the whole area of the organ. The notochord transfixes the
tail considerably above the median line, leaving a much larger proportion of the lobe
beneath than above, and into this the blood-vessels pass. A little posterior to the
marked caudal diminution of the notochord the neurochord abruptly narrows, and a
delicate continuation (Pl. XX. figs. 1 and 3) proceeds to the tip of the former.
In the course of the succeeding month (February) the dorsal bend of the noto-
chord commences, so that on the 17th a considerable change in outline has occurred.
The upper border, especially along the posterior line, becomes prominent, while the
inferior is less so, and the hind edge assumes a broad blunt outline (PI. XX. fig. 3).
It is evident that the inferior lobe of the tail in the early stage (Pl. XX. fig. 1) now
becomes more or less the posterior, a change, perhaps, partly due to the terminal and
upward curve of the notochord. The latter at this stage is much less marked than in the
salmon of the first day. ‘The appearance of the hypural elements (Pl. XXVII. fig. 2), as
already indicated, probably aids in the transformation. The notochord is still less curved
than in the salmon of the first day, and the posterior hypural margin slopes downward
and forward. The hypural (cartilaginous) element most anterior (uc) is quadrate, and
devoid of the notch seen by Professor Huxuey in that of Gastrosteus.* Its longest side
is directed inferiorly and posteriorly. The posterior or superior hypural cartilage is
triangular in outline, its longest side being applied to the under surface of the ascending
notochord, which projects about half the length of this side beyond it. The bases of five
or six caudal rays rest on the larger hypural, and a somewhat smaller number on the
upper. They may be estimated at twelve in the earlier stage (March). In the following
month (April) the further curvature of the notochord upward is accompanied by a
tilting of the posterior edges of the hypurals into a nearly vertical position, and the
greatly elongated vessels now run straight outwards along the rays. The posterior
margin of the caudal fin has also become conspicuously crenate, and at this stage (PI.
XXII. fig. 2) the inferior margin is more rounded than the superior, which ends after
a straight course somewhat abruptly in a crenation. In front of the tail, ventrally, a
slight inflection of the marginal fin occurs. The notochordal sheath now shows serial
constrictions indicating the separation of the centra.
In the next stage (Pl. XXVII. fig. 3) the tail is considerably elongated, and its
vertical diameter is diminished. The notochord is less in proportion to the other parts,
while the anterior, or inferior, hypural has increased in length, and shows a distinct
upward curvature at the base.
There are upwards of twenty caudal rays, 7.c., about twenty-four, a larger number than
is present in the adult. Day records the number in the adult at fifteen to eighteen,
while in the St Andrews University Museum three specimens each possess twenty-one.
The fin-rays show three vertical rows of articulations, and they spread out distally,
and terminate in fine fibres, like those of the embryonic fin. The marginal crenations,
posteriorly, are now so disposed that they correspond with the expanded ends just
* Quart. Jour. Micr. Soc., 1859, p. 40, pl. ili. fig. 1.
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 895
mentioned. », 4th day (optic vesicles),
Fig. 4. A om - », 4th day (nuchal region), F :
Fig. 5a. ; os 59 » 4th day (posterior region of the trunk),
Fig. 5b. % : op », . 4th day (posterior region of the trunk),
Fig. 5c. % 29 ; » 4th day (posterior region of the trunk),
Fig. 5d. § 5 = » 4th day (posterior region of the trunk),
Fig. -5e. 5 e ; » 4th day (close to margin of rim),
Fig. 5f. . = § », 4th day (close to margin of rim),
Fig. 6. x % x) » immediately posterior to fig. 5),
Fig. 7. ) bn i ,, the two layers of fig. 5e, :
Fig. 8. 5 a mh », the two layers of the blastodermic (extra-
embryonic) area,
Fig, 9. G. eglefinus, 5th day, hind end of embryo,
Fig. 10. 0 5th day, otocystic region,
Fig. 11. 7. gurnardus, 4th day, longitudinal section,
Fig. 12. 3 4th day, slightly oblique longitudinal eniieal Sects Gantenal sagen
Fig. 13. a oblique section through fore-brain and eye, . , -
Fig. 14. P. flesus, oblique longitudinal horizontal section of anterior end of embryo,
Fig. 15. G. eglefinus, oblique longitudinal horizontal section of anterior end of embryo (rim at the
Fig. 15a. y
Fig. 16. - 4th day, oblique longitudinal horizontal section, further advanced than
fig. 15,
Fig. 17. P. flesus, transverse section at a later stage than fg 4,
Fig. 18. Molva vulgaris, horizontal section through the choroid fissure, ,
Fig. 19. S horizontal section through the choroid fissure at a lower plkine sham fig. 18,
Fig. 20. * transverse section through fore-brain,
Pirate V.
Fig. 1. Molva vulgaris, front view of head, 6th day, x
Fig. 2. 7. gurnardus, pigment-spots on the trunk, 4th day, June 1886,
Fig. 2a. a yolk-sac, Ist day out, ; é
Fig. 20. 3 pigment-spot on yolk-sac (three tags in progress of cor Pte)
Fig. 3. P. limanda, ovum with abnormal embryo, May 8, 1885,
Fig. 3a. os ovum with abnormal embryo, 3 days later,
Fig. 4. Undermined ovum (r) with oil-globule (-034 inch in diam.),
Fig. 5. 7. gurnardus, cyclopean embryo in ovo,
Fig. 6. P. platessa, ovum with embryo well-developed, Resi 20, 188 6,
VOL. XXXV. PART III. (NO. 19). 7D
equator of the eg),
oblique longitudinal horizontal section on a inner land than fig. 15,
about 55
x 250
x 400
x 400
Enlarged
Enlarged
x 40
Enlarged
x 40
938 PROFESSOR W. C. M‘INTOSH AND MR E. E. PRINCE ON
Fig. 7. Molva vulgaris, aboral end of notochord, 10th day, : A ‘ : : x 200
Migs 38.) 5; 5, Showing early pigment, 7th day, May 4, 1886, ; ; ‘ , x 55
Tite BBE oy » embryo still further advanced, 8th day, May 5, 1886, ; j é x 70
itty »» ventral aspect of embryo, . rs ; ‘ x about 30
Fig. 11. Pleuronectes imanda, ovum showing protoplasmic eee ¢ - , x about 40
Prats VI.
Fig. 1. G. morrhua, surface view of ear, May 10, 1886, . - ; c : ‘ x 210
Fig. 2. 7. gurnardus, surface view of ear, 7th day, June 22, 1886, : ; : : x 205
The anterior edge is on the right, and the dorsal is superior.
Fig. 3. * longitudinal vertical section of the otocystic region; 3 days old, June 1, 1886, x 230
Fig. 4. s transverse section of the same region; 3 days old, June 1, 1886, . 3 x 230
Fig. 5. G. cglefinus, anterior end of larva, : : : . 6 : x 150
Fig. 6. Larva of 7’. gurnardus, from the dorsum, June 15, 1886, . : : : x 156
Fig. 7. Pleuronectes platessa, head of larva 2 days old, May 1886, . : ; ; Highly magnified
Fig. 8. T. gurnardus, sensory organ in integument behind the cephalic region, May 12, 1886, ‘ x 156
Fig. 8a. H sensory organ in integument behind the cephalic region, June 24, 1886, —. x 415
Fig. 9. Transverse section through the otocystic region of larva of G. aglefinus, 19th day after
hatching, : : : : : : : : : x about 300
Fig. 10. Section of the same region, 5 ‘ x 230
Fig. 11. Otolith of Cottus scorpius, sl; in. long (° 188 men): eee Beonely Grane core sont un-
stained concentric stratum, c ; i é 4 5 : é x 750
Prats VIL.
Fig. 1. G. eglefinus, transverse section, 13th day (7 hours before hatching), April 14, 1886, : x 200
Fig. 2 + transverse section, 14th day after fertilisation (just emerged), ; : x 150
Fig. 3 5 transverse section, 3rd day after hatching, April 24, 1886, . ; 3 x 175
Fig. 4. p transverse section, posterior to fig. 3, 5 : 3 x 175
Fig. 5 3 transverse section through mid-gut and diverticulum (ewiste ladder), : x 450
Fig. 6 transverse section, 2nd day out, April 24, 1886, 4 4 : : x 200
Fig. 6a. x transverse section (section succeeding fig. 6), : : x 200
Fig. 7. t longitudinal horizontal section, 3rd day out, March 23, 1886, : ; x 135
Fig. 8. Molva vulgaris, 6 days old, ventral aspect of the alimentary canal, 5 x 250
Fig. 9. T. gurnardus, longitudinal vertical section of the alimentary canal, 17th day, July 8, 1885, x 175
Fig. 10. + dorsal view of pectoral fin of embryo before hatching, May 27, 1886, : x 210
Fig. 11. G. morrhua, section of the anal portion of the gut, 6th day out, May 4, 1886, 5 x 175
Fig. 12. Molva vulgaris, longitudinal horizontal section through the hind-gut, 2 se old, May 7, Ife
1886, ‘ : : : x 175
Bigs: 75, 3 longitudinal horizontal Anta at a lower pene : ; ; x 175
Fig. 14. ,, i longitudinal horizontal section half-way down marginal fin, 2 x 600
Hig 1b: , 2 longitudinal horizontal section of the anal opening, on a lower plane fhan
fig, 14, : : : : c : : 5 x 600
Puate VIII.
Fig. 1. Undetermined larva (p) with oil-globule (see p. 861), . : c - : x 25
Fig, 2. G. eglefinus, 8th day after fertilisation, view of the heart, 8.50 p.m., March 30, 1886, : x 210
Fig. 3. 7. ger nardus, from right side, focussed deeply: pew, anterior seni) wall, July 18,
1886, : : : : : : : ‘ x 156
Fig. 4. 35 ear, eye, and other organs, . ; x 156
Fig. 5. oF Ist day, slightly oblique view of the eandioe 3 region froth Below June , 1886, x 156
Fig. 6. Head and anterior region of 7. gurnardus, newly hatched, : ; : a SOD
Fig. 7. Head of G. wglefinus, 7th day, April 30,1886, . 5 ; , : ; x 65
Fig. 8. Branchial region of 7. gurnardus, newly-hatched, ; ; : : : x 790
—
DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES. 939
Fig. 9. Heart and other organs of 7. gurnardus, just hatched, seen from above, June 2, 1886, ° . x 90
Fig. 10. Young pleuronectid (unknown sp.), April 7, 1887, front face view, ; . x 50
Fig. 11. 7. gurnardus, 4th day, transverse section divongh the heart, with mesoblast ies) : x 600
Puate IX.
Fig. 1. Anterior end of T. gurnardus, 3rd day, June 19,1886, F j j : x 100
Fig. 2. Molva vulgaris, 4 days old, May 12, 1886, : : : , : : x 25
JO SE © op ; 5 days old, May 13, 1886, : x 25
Fig. 4. Head and anterior region of P. platessa, 8 mm. in length, and 4 ae old, eal 22, 1886, . x 40
Fig. 5. Anterior end of 7. gurnardus, 8th day, June 24, 1886, . é : : , x 55
Fig. 6. G. eglefinus, branchial and mandibular cartilages, April 20, 1886, ; : : x 200
Fig. 7. Mandible of G. eglefinus, 10 days old, 5 x 140
Fig. 8. Blastoderm of 7. gurnardus at the stage of About sixty Pinson: um inte. Blaatomanie
spaces apparently filled with fluid, ; ‘ : : : 4 x 40
Fig. 9. Molva vulgaris, margin of dise and nuclei of neniinse : x 450
Fig. 10. Gadus eglefinus, 24th hour; the figure shows some marginal cells of the blastoderany anak a
portion of the nucleated Fehibinet : ° ‘ : : ‘ ° x 415
PiatE X.
Fig. 1. Slightly oblique view of the head of an advanced larva (15th day) of Trigla gurnardus, . x 40
Fig. 2. Trigla gurnardus, showing pigment in pectoral fin and visceral anatomy, 16th day, . Magnified
High 2050s, os ventral view of same, 16th day, ‘ : , : . Magnified
1 BL op A advanced embryo, 17th or 18th day, : 5 - Magnified
Fig. 4. Blastodise of Trigla gurnardus at the 6th hour, viewed from above ; third furrow nearly
completed. Oil-globule (0g) seen below, é . : : F x 80
Fig. 5. Larva of Gadus morrhua, ventral view of head, May 11, 1886, : . . Magnified
Kiss da. 5; 5 = dorsal view of head, May 11, 1886; the heart is adrewtad by te
dotted lines, ‘ c ; : . Magnified
Fig. 6. Opercular aperture of Molva vulgaris, May 10, 1886, 5 ; x 205
Fig. 7. Zona radiata of an abnormal egg of Solea vulgaris, showing flat aan on “the surhioes : x 50
Fig. 8. Zona radiata of the pelagic egg with large perivitelline space with distinct punctures, : x 480
Fig. 9. Ovum of Gadus morrhua in the morula stage ; blastomeres boldly spherical, 4 : x 50
Fig. 10. Ovum of Plewronectes flesus, lateral view of the multicelled condition of the disc, . : x 35
Puate XI.
Fig. 1. @. eglefinus, transverse section through the fore-brain, 17th day, . ; : ¢ x 200
Fig. 2. 3 transverse section through the fore part of heart, ; ; : : x 200
Fig. 3. transverse section posterior to fig. 2, . ; ; : x 200
Fig. 4. e transverse section through the fore part of the safvarilan?. : : : x 200
Fig. 5. 3 transverse section, lateral portion of section fig. 2, . : : : x 435
Fig. 6. Molva vulgaris, transverse section, branchial region and heart, 11th day, . : : x 135
Tie, Uo 5 transverse section, branchial region and heart, 14th day, . ; : x 135:
IMs, hp P transverse section posterior to fig. 7, : x 135
Fig. 9. Gastrosteus spinachia, longitudinal vertical section through the ianetials region aout tp
time of hatching, : : x 135
Fig. 10. 5 Fi longitudinal vertical section Agus the prenehit region and oper-
culum, slightly more advanced than fig. 9, : : 5 x 135
Fig. 11. G. eglefinus, 2 days old, oblique horizontal section of the branchial region, ¢ é x 175
Fig. 12. 7. gurnardus, section of a portion of the protoplasmic investment of the oil-globule, : x 450
Fig. 13. Molva vulgaris, section through the oil-globule, showing pigment in the protoplasm, 0 x 150
Fig. 14. G. eglefinus, 17 days old, transverse section through the hind-gut, : : : x 230
Fig. 15. 3 transverse section through the base of the tail, é : 5 : x 230
PROFESSOR W. C. M‘INTOSH AND MR-E. E. PRINCE ON
. 16. G. eglefinus, transverse section showing a tract, probably sensory, in the lateral region of
the tail, . 3 : 5 c é x 230
eli. “ transverse section near the Ge of the Sanalal Punk. ; ; x 230
. 18. TL. gurnardus, 22 days old, bony elements in the roof of the mouth, riubebly palatine . x 120
. 19. Clavicle of undetermined pleuronectid larva (possibly plaice), : - x 70
, 20. LT. gurnardus, 22 days old, premaxillary (?) elements: a, anterior eee b, ene é x 120
Puate XII.
1. 7. gurnardus, 1st day out, June 2, 1886, . ; : : : : x about 32
2. G. morrhua, advanced larva, May 2, 1855, : ; : : : : x 45
3. Early larva of Motella mustela, May 8, 1886, : 5 ; : : : x 60
4, Molva vulgaris, just hatched, 4.30 p.m., May 5, 1886, . ; : d : x 40
5. Cyclopterus lumpus, newly-hatched, May 27, 1886, . : ‘ 7 . Magnified
6. Larva of Pleuronectes flesus, 13 days old, April 26, 1886, . : : ; : x 50
6a. 5, 18 days old, dorsal view.
ie Tateral view of the larva of P. platessa, May 7, 1886, : x 40
8. G. eglefinus, 6 days old, longitudinal vertical section through ponent aioe sinus
venosus, and branchial arches, : : : ; : : ; x 150
Prate XIII.
1. Larva of Liparis montagui, March 19, 1886, ‘ 3 5 : x 24
2. Termination of the tail in the larva of Cottus scorpius, Apne 8, 1886, . : - x 40
3. Ovum of undetermined pleuronectid (?), with large perivitelline space.
4. Molva vulgaris, 1st day out, May 6, 1886, : : ‘ : : x 40
5. Centronotus gunnellus, head and anterior region, March 18, 1886, . « : ; . x about 90
6. : * early larva, March 14, 1886, : : : 2 . Magnified
6a.Caudal region of larval gunnel, . : ; ; : : . x about 24
7. Centronotus gunnellus, advanced larva, May 1, 1886, : : - ‘ . x about 24
Puate XIV.
1. Embryo of G. eglefinus, removed from capsule, April 1, 1886, viewed somewhat obliquely, x 55
2. Head of larva of 7. gurnardus, 3rd day, . A ; . : x 55
3. Abnormal tail of larva of 7. gurnardus, 1st day, June ff 1886, . : 5 : x 210
4, Anterior end of larva of Cottus scorpius (?), April 8, 1886, : 5 : : x 24
5. P. platessa, anal region, . 4 : ‘ : x 55
6. Cardiac region of larva from ovum mn ihe SeeeR hry space, . x 40
7. T. gurnardus, hind end of embryo and edge of blastopore, showing the ajoining een of
the periblast, . : 5 x 210
8. 33 blastoderm shortly after the Gth hous the 4th iui in progress, . : x 80
Prats XV.
1. Molva vulgaris, subnotochordal trunks and blood-elements b/c, May 8, 1886, 5 : x 220
2. Larva of Liparis montagui (2), showing vitelline circulation, April 12, 1886, C : x 40
3. Aboral end of the notochord and tail of post-larval P. jlesus, : ‘ 3 : x 55
4, Tip of the tail in the larval Motella mustela, . x 220
5. Marginal fin and part of alimentary canal in the larva of Camrose ees July 1,
1885 [the caudal fin in this figure has been marked ef instead of cf], . é ; x 200
6. Cyclopterus lumpus, lateral view, 26 days old, June 17, 1885, : x 30
7. Longitudinal section through the caudal portion of the notochord of G. rae 13th ee x 200
8. P. jlesus, head of young specimen, May 18, 1886, : : . Magnified
9. Cyclopterus lumpus, same age as in fig. 6, ventral view showing eins erm fins, . x 25
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DEVELOPMENT AND LIFE-HISTORIES OF TELEOSTEAN FISHES.
Pratt XVI.
941
1. Pleuronectes flesus, larva 13 days old, April 26, 1886, (reduced) x 40
2. Gadus merlangus, early larva, April 24, 1885, 4 x 40
3. Pleuronectes limanda, 11 days old, May 22, 1886, . x 56
4. Dorsal view of the same, x 50
5. Slightly oblique view of an aavanced larva ‘ot Pleabaonectes alae May 1, 1886, : x 15
5a. Slightly oblique view of an advanced larva of _,, 3 May 7, 1886, dorsal
aspect, . ‘ : : . Magnified
6. Anterior end of the larva of Ie Thani, Sth day tice emerging, May 19, 1886, . Magnified
7. Advanced larva of Liparis montagui, April 13, 1886, ‘ , x 18
8. Larva of Trigla gurnardus, 3rd day out, May 31, 1886, x 50
9. Advanced larva of Cottus scorpius, April 13, 1886, x 18
10. Abnormal ovum of Trigla gurnardus, July 8, 1885, x 40
Prats XVII.
1. Gadus eglefinus, larva, 7 days old, with circulation active, April 19, 1886, . x 40
2. Motella mustela, advanced larva, May 11, 1886, x 90
3. Cyclopterus lumpus, artificially extruded om the egg-capsule, Enlarged
4, Undetermined larva, with oil-globule, newly emerged from the ovum fared on Plate V. fig. 4, x 40
5. Trigla gurnardus, post-larval stage, August 23, 1886, x 20
6. 33 % post-larval stage, older stage, dorsal view, Aehac 16, 1886, Enlarged
he Fe 55 post-larval stage, older stage, side view, August 16, 1886, Enlarged
8. Young Gadus morrhua, June 11, 1886, . : . About natural size
9. Larva of Molva vulgaris on the 2nd day, May 8, 1886, x 50
10; Marva ‘of ~,, » 13 days old, May 13, 1886, x 80
11. Post-larval Cottus quadricornis, 5 x 8
12. Advanced larval stage of Gadus merlangus, x 50
13. Newly-hatched larva of Solea vulgaris, x 52
Puate XVIII.
1. Undetermined Pleuronectid, 24th hour after hatching, April 7, 1887, x about 75
2. Another undetermined Pleuronectid, 2nd day out (for ovum, vide Plate XIII. fig. 3), 6 x 40
3. Post-larval ling (Molva vulgaris), showing long ventral fins, ; 8 ili)
4, Post-larval ling ,, 5 showing long ventral fins (later stage), : : x 5
5. Post-larval rockling (Motella), showing long ventral fins (later stage). The dorsal fin is
entered in the text as df, ; F : xe 6
6. Post-larval rockling (Motella), younger stage than fig. 5, ian
7. Post-larval “witch” (Pleuronectes cynoglossus), : 5 aide
8. Post-larval “ witch” =! 35 older stage, x5
9. Advanced post-larval stage ,, oS
10. Advanced post-larval stage of armed ballesd (ge gonus Lasagne Pepa yal 28, 1887, .xabout 9
11. Late larval stage of the same, April 4, 1887, 5 ; : ‘ . x about 20
Pratt XIX.
1, Young turbot (Rhombus maximus), August 23, 1886, . x about 10
2. Post-larval stage of Gadus morrhua, in spirit, May 1887,
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