Download Further Notes on the Structure of the Bony Fishes

377
FURTHER NOTES OX THE STRUCTURE OF THE LYOMEKC
Further Notes on the Structure of the Bony Fishes of the Order Lyomeri (Eury(From the Department of Zoology, British
pharynx). By V. V. TCHERNAVIN.
Museum, Natural History.)
(PLATE
8 and 8 Text-figures.)
(Read 8 May 1947.)
CONTENTS.
Page
1 . Introduction (scope of the study ; material and method ; acknowledgments)
2. Sature of the extra (sixth) visceral cleft in Eurypharynx (the course of the
facial, glosso-pharyngeal, and the vagus nerves, conclusion). . . . . . . . . . . . . .
3. Gills . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4. Vascular system (afferent arteries ; thyroid gland ; efferent arteries ; lateral
dorsal aorta ; medial, unpaired dorsal aorta ; veins of the head) ........
5. Relation of pectoral fins to the pericardinm ......
...................
6 . Summary and conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
..........................................
7. Key to the figures . . .
X. References ............................
....
377
359
3X 1
384
389
390
392
393
1. INTRODUCTION.
My previous work on Lyomeri (Tchernavin, 1947) was handicapped by the
scarcity of material, and so several obscure points in the structure of these extraordinary fishes could not be studied.
Through the kindness of Dr. b. V. Tbning of the Marine Biological Laboratory
in Charlottenlund Slot, I received several specimens of Euypharynx, qnd Dr. T h i n g
gave me his kind permission to dissect some of them. An account of the results
obtained from the dissection of the branchial region of E u y p h a y n x is given here.
This present investigation deals mainly with the nature of the extra visceral
cleft of Eurypharynx ; the relations of the facial nerve and the nerves of the vagus
group to the visceral clefts ; and the vascular system of the branchial apparatus.
I had in hand for this study specimens of the genus Euypharynx only, and used
mainly the specimens which were damaged during their capture or which had
already been dissected by my predecessor in the study of the ' Dana ' collection
of Lyomeri. I dissected the specimens under a binocular microscope, but did not
prepare sections, and I could not inject the blood vessels owing to the smallness
of these vessels and the unsuitable condition of the material.
It is probable that using such a primitive method, I have missed some of the
features of these fishes, or made some errors. I hope, however, that my description
and figures of the structures concerned, of the course of the cephalic nerves, and of
the main blood vessels are correct on the whole.
The work was done in post-war conditions, and with post-war equipment, of
which the less said the better.
The figures are drawn by the writer. The photographs were taken by the
officialphotographers of the British Museum (Natural History).
Acknmledgmnts.-I thank most warmly Dr. A.V. T h i n g for h i kind permission
to use for this investigation the material of Eurypharynx collected by the ' Dana '
Expedition, and Prof. L. Bertin for sending me this material from Paris. I am much
indebted t o Dr. E. Trewavas for her kind interest in my work, help and advice.
..
n
THE STRUCTURE OF THE LYOMERI
379
2. NATURE
OF THE EXTRA (SIXTH)VISCERAL
CLEFTIN Euypharynx.
First of all i t must be stressed here that all the numerous specimens of Eurypharynx
of different sues, collected in W e r e n t regions, invariably have six branchial clefts
andjive holobranchs (Pl. 8, figs. A, B). All the six clefts and all the five holobranchs
are functional, and none of them can be described aa vestigial ; this is also confirmed
by study of the branchial arteries.*
Two M e r e n t ways of interpreting the extra cleft of Eurypharynx seemed to me
possible (Tchernavin, 1947 p. 312).
(1) All six clefts of Eurypharynx are branchial clefts. If so, the ventral hyoid
elements are completely missing, the foremost branchid c l e . is situated between the
mandible and the first branchial arch, and an extra, sixth, branchial cleft, and an extra
posterior hemibranch, homologous to those found in some Selachians, are found
in Eurypharynx, though never in all known recent and fossil Osteichthyes.
(2) The cartilages supporting the septum behind the foremost cleft are the ventral
elements of the hyoid arch, and this cleft corresponds to the ventral part of the
prehyoid cleft. If so, the five posterior clefts of Eurypharynx correspond to the
usual branchial clefts of Osteichthyes ; and Euryphaynx, having the ventral part of
the prehyoid cleft open, recalls to some extent the Acanthodians as described by
Watson (1937)7.
Having no specimens for dissedtion during my previous study, I left this question
,open.
Relations of the facial nerve and of the nerves of the vagus group to the branchial
arches.-The truncw hyomandibularis vii (hmf.) emerges through the jugular foramen
(text-fig. 2, fj) ventrally to the head vein. After a short run it turns slightly
outwards, soon dividing into two branches. One branch (ramus mandibularis, mf.),
runs outwards close t o the hind edge of the hyomandibular, enters from the inner
side into this bone and passes out from the outer side of it, running towards its
distal end. It gives off a branch which runs first further in the same direction along
the suspensorium, and after passing the hyomandibulo-quadrate articulation, turns
caudad along the inner side of the thin wall of the oral cavity. It gives branches
to the series of the lateral line organs disposed between the suspensorium and the
first branchial arch. The nerve runs dorsally to the foremost branchial cleft and
passes beyond this cleft. It is probably the ramus opercularis superfacialis vii. The
ramua mandibularis facicclis runs further towards the distal end of the suspensorium
and divides into two branches, which are probably the rr. mandibularis internm and
externus. Apparently only one of them ( r . mandibularis internus) reaches the lower
jaw. A t the distal end of the quadrate, this nerve runs along the posterior edge
Of this bone, then passes to its inner side, medially to the mandibulo-quadrate
articulation and to the ligament attaching the palatine to the inner surface of the
quadrate ; further the nerve runs along the inner side of the mandible.
The hyoid branch of the facial nerve (r. hyoideus, hf.) separates from the truncus
hyomandibularis before the manidular nerve enters the hyomandibular bone, and runs
eaudad behind the hyomandibular. The hyoid nerve soon divides into two uneven
branches. Both turn sharply dorsad and pass between the strong ligaments of the
m. adductor hyomandibularis (ma.). Then they turn medially, towards the lateral
,dorsal aorta, and come close t o it in the region of the first vertebra. They run
further towards the tail dorsally to this artery. The smaller branch gives off a small
twig (not seen on text-fig. 2) before reaching the m. adductor hyomandibularis, this
twig subdivides and enters this muscle.
* Nussbaum-Hilarowicz (1923, p. 64, pl. ix, fig. 13) describes five branchial clefts in
Eurypharynx, but on the figure, representing the 8ame specimen, shows six branchial clefts.
Rauther (1937, footnote on p. 243) doubts whether it is true that Euryphurynx has five holobranch ; Regan (1912, pp. 347-49) and Berg (1940, p. 439) do not mention the sixth cleft of
Euryphaqnx in their descriptions of this group.
t The presence of a complete prehyoid cleft in Acanthodians is most emphatically denied
%yProf. N. Holmgren (1942, pp. 144, 146).
380
V. V. TCHERNAVIY : FURTHER NOTES ON
The main trunk of the hyoid nerve runs further backwards, but already in the
region of the ninth vertebra it becomes of smaller volume ; running further caudad
it gives off a large branch which runs obliquely ventrad and caudad ; still further
caudad, i t divides into two branches which take a course in the same direction as
the first branch. Thus, the hyoid nerve divides into branches running between
the oblique transverse muscles of the wall of the gut, infront of the foremost visceral
cleft, and does not pass beyond this cleft. This indicates that the oblique muscles,
in front of the foremost visceral cleft, correspond to the hyoid muscles, that the
ventral elements of the hyoid arch are missing, and that the foremost visceral cleft
of Ezirypharynz is the first branchial cleft.
TEST-FIG.
?.-Diagram
showing the position of the hyomandibular trunk ( I’II), the gloswopharyngeal and vagus nerves and the head vein of the left side on the ventral surface of
the cranium of Euryphuryns. x 10. fj.,foramen jugularis (in the prootic) ; fo., foramen for
the IX and X nerves (in the lateral occipital) ; hf ., hyoid nerve ( V I I ); mf., mandibular
nerve ( T’II) ; hmf., hyomnndibnlar trunk (T’II) ; hv.,head vein ; I , ligaments of the lateral
muscle of the body ; ?nu.,?)A. adductor hyo?iaandibularis ; ng., glossopharyngeal nerve ;
ngl., branch of the glossopharyngeal nerve ; nv., branchial trunk of the vapus nerve;
nvl., lateral trunk of the vagns nerve ; vf.. v. fusciulis ouzxillaris.
The glossopharyngeal nerve (text-figs. 2 , 3, ng.) leaves the skull through the same
foramen (fo.)in the lateral occipital as the vagus nerve (Tchernavin, 1947, p. 315).
It emerges anteriorly to the ganglion of the latter nerve, then turns ventrad between
the two hgaments (l.), of the dorso-lateral muscle of the body, close to the place
where these hgaments are attached to the cranium. It turns then sharply caudad,
passing ventrally .to the head vein but dorsally to the lateral aorta, and lying between
THE STRUCTURE O F THE LYOMERI
38 1
these two vessels. It soon gives off a branch (ng,.)which runs outwards. The main
trunk of the nerve has a ganglion-like swelling and runs further straight caudad,
ventrally to the head vein and dorsally to the lateral aorta, in close vicinity to these
vessels.
Reaching the junction of the lateral dorsal aorta with the fi&t epibranchial
artery, the ninth nerve turns ventrad following closely the course of the artery,
gives off a pre-trematic branch which runs towards the anterior end of the foremost
branchial cleft, while the post-trematic nerve passes into the gill septum between
the fist and second branchial clefts. The nerve passes mesially to the efferent
dorsal loop d, but laterally to the main efferent branchial artery. After passing
through the branchial septum it turns a t about a right angle forwards, and runs
towards the head close to the ventral branch of the first branchial efferent artery (ha.).
The uagw nerve (text-figs. 2,3, nu., nvl.)passes out through a foramen (fo.)on the
lateral occipital (the foramen is common with the ninth nerve). A large ganglion
is found just outside this foramen. It is apparently a n expansion of the ramus
lateralis vagi (nvl.). The main lateral branch of vagus (nvl.) runs straight caudad
medially and dorsally to the cardinal vein along the vertebral column. It gives
off a t regular intervals branches running obliquely backwards and dorsad straight
to the lateral line organs. The foremost pair of these nerves arises opposite the first
vertebra. The branchial trunk of the vagus (nu.), after leaving the cranium, turns
round to the ventral side of the ganglion and passes straight caudad, dorsally to the
ninth nerve.
Before reaching the region of the branchial clefts a nerve (nu,., truncus branchialis
primus) separates from the dorsal side of the main trunk of the nerve, passes downwards laterally to this nerve, to the cardinal vein, and to the lateral aorta, and
follows very closely the first epibranchial artery. It divides then into three branches,
the anterior (pre-trematic) reaches the first branchial arch ; the post-trematic branch
runs into the septum between the second and the third branchial clefts, passes
through the septum and turns towards the cranium, its course resembling closely
that of the post-trematic branch of the glossopharyngeal nerve. A third branch
of the truncus branchialis primus separates from it and runs backwards into the
third branchial arch. The truncus branchialis secundus (nu2.) separates from the
dorsal side of the trunk of the vagus nerve somewhat further caudad and runs into
the third branchial septum. The branchial trunk of the vagm nerve continues its
course towards the tail ; reaching the level of the sixth branchial cleft i t gives off
a bunch of four nerves which run ventrad. The anterior of these nerves (nu3.)passes
into the fourth branchial arch and gives off a twig, which runs into the septum
between the fifth and sixth branchial clefts. The next nerve (nul.) passes into the
fifth branchial arch. The two posterior nerves (nu5. and nu,.) pass behind the sixth
cleft. The main trunk of the vagus much diminished in volume follows its caudad
course close to the coeliaco-mesenteric artery (cma.).
Thus, the course of the facial, glossopharyngeal and vagus nerves show that the
foremost branchial cleft of Eurypharynx corresponds to the first branchial cleft,
and that the sixth cleft is an additional branchial cleft which is never found in
Osteichthyes.
3. GILLS.
I described in a n earlier paper (Tchernavin, 1947, p. 302) the position and the
general structure of the branchial chambers in Lyomeri. From better material
in hand I add here a brief description of the gills of Eurypharynx.
Euryphaynx has five well-developed holobranchs situated behind the five anterior
branchial clefts ; there is no gill behind the sixth cleft. All five holobranchs have
the same structure.
The branchial arches are much reduced in Eurypharynx and not ossified. They
are represented by separate cartilaginous rods extending along the branchial septa,
close to the inner surface of the latter. The mucous membrane covering the inner
TEXT-FIG.
3.-Vaacular
system and the nerves of the branchial region of Euryplwrynx ;
right side ; seen from within ; diagrammatic, simplified ; (afferent and efferent vessels
of the gill filaments, and the arteries issuing from the unpaired dorsal aorta to the segments
of the body not shown). About x 6.
Afferent vessels dotted dark, efferent dotted lighter, veins striated, glossopharyngeal nerve
black, vagus nerve white. Branchial clefts black.
a1-u6, afferent branchial arteries ; at., artery of the thyroid gland ; o., commissural vessel uniting
the lateral dorsal aorta with the unpaired dorsal aorta ; c d 1 4 , . lateral commissural vessels
(dorsal series) of the efferent arteries ; ctna., coeliaco-mesenteric artery ; cwl+xr, lateral
commissural vessels (ventral series) of the efferent arteries; dl-d,, dorsal arches of t h e
efferent arteries ; el-e6, eqibranchial arteries ; eal-ea,, efferent branchial arteries ; ha.,ventral
branch of the fist branchial artery ; he., dorsal branch of the first branchial artery ; hv., head
vein (jugular, cardinal) ; ijw., inferior jugular vein ; Zal-Za8,parts of the lateral (paired)
dorsal aorta ; na., branch of the 5th epibranchial artery (nutritive artery of the heart ?) ;
t q . , glossopharyngeal nerve ; nv., branchial trunk of the vagus nerve ; nv,-nv,, branches of
the vagus nerve ; p., base of the pectoral fin ; pa., posterior ventral artery passing below the
sixth gill cleft ; pc., pericardium ;r., rays of the pectoral fin ; 8V., sinus venosus; v1-v5, ventral
arches of the efferent arteries : va.,ventral aorta : ttda.. anterior part of the unpaired dorsal
aorta ; udp., posterior part of the unpaired dorsal aorta.
FURTHER NOTES ON THE STRUCTURE OW THE LYOMERI
383
surface of the septa is thick and much folded, while the cartilages forming the arches
are soft and transparent, more slender than a branchial artery. When the cartilage
is isolated from the surrounding tissues, it twists and bends. It is thus rather
m c u l t to trace the branchial skeleton without preparing sections. As far as can
be seen from a dissection, the branchial skeleton of an arch consists on each side
of a single cartilage, which is about aa long as the septum ; i t is of irregular thickness,
and two narrow isthmuses can be distinguished, subdividing the cartilage into three
parts. It may be, however, that these subdivisions are due t o the shrinking of the
soft cartilage in spirit.
The cartilages of the branchial arches are quite separate from each other, from
the cranium and from the vertebral column. There are no ventral branchial elements,
and the right and left semi-arches are thus also quite separate. I found such
cartilaginous rods behind the first, second, third, fourth, and fifth branchial clefts ;
I have not found any cartilages behind the sixth cleft. But it is not impossible
that I could have missed them.
Nussbaum-Hilarowicz (1923, p. 66) describes four branchial arches in Eurypharynx;
Bertin (1936, p. 23) writes that Eurypharynx has five branchial arches.
The gills of Eurypharynx are not attached to the skeleton of the branchial arches,
and the gill-rays supporting the gill filaments are broadly separated from the cartilage
of the branchial arch (Nussbaum-Hilarowicz, 1923, p. 66). The gill is not confined
to the septum between two clefts but extends along the wall of the gut dorsally and
ventrally beyond the septum. I counted the gill-filaments in the posterior hemibranch of the third cleft ; seven filaments are attached to the wall of the gut above
the septum, ten are attached to the septum itself, and nine to the wall of thegut
below the septum. Thus, the additional parts of the gill below and above the septum
play as important a r81e in the breathing process as the part of the gill on the septum
itself.
The gills of Eurypharynx consist of filaments which have substantially the same
structure as in other Osteichthyes ; it seems that there is no need to use a special
nomenclature for their description (comp. Nussbaum-Hilarowicz, 1923, pp. 6 4 4 6 ;
Bertin, 1934, p. 23). The filaments are long and the gill rays supporting these
filaments are soft. Thus the filaments are not rigid and not projecting into the
branchial cavity at a right angle t o the branchial arch ; they bend freely and hang
downwards forming a kind of neatly arranged, wavy branch or tuft. The filaments
of the additional parts of the gill are attached t o the wall of the gut in a different way
from those attached t o the septum itself; but the alternate arrangement of the filaments
of the two hemibranchs of one gill is very distinct throughout the gill, so that i t is
quite clear t o which holobranch each single filament belongs (compare Bertin, 1934,
p. 34). The basal parts of the filaments of the two hemibranchs in the part of the
gill attached t o the septum, overlap each other in the usual teleostean way, for the
afferent and the efferent arteries pass along the middle of the branchial septum
(text-fig. 4), and the afferent and efferent vessels of the filaments issue from this
midline. The gill-filaments of the additional parts of the gill have a different disposition. Their afferent arteries run along the midline of the gill (between the two
hemibranchs,) but their efferent vessels originate from an arch-like efferent vessel
(text-fig. 4, d 2 . ,wz.). Therefore the bases of the filaments of the two hemibranchs
are arranged in such a way that their afferent ends are disposed along the midline
of the gill, but their efferent ends are set apart along the arches of the efferent artery-.
The branchial lamellae are well developed, but appear thicker than usual in
Osteichthyes (this is also found in some other deep sea fishes). Kussbaum-Hilarowicz
(1923, p. 67) described their minute structure.
I did not study the muscular system of Eurypharynx, and mention here only
some of the uncommon features of their branchial muscles which I saw when I
examined the branchial arteries. The branchial muscles are not attached t o the
skeleton of the arches. Each hranchial cleft is surrounded by two muscles overlapping each other in a way similar to the mm. sphincter branchia.lis anterior and
384
V. V. TCHERNAVIN
:
FURTHER NOTES ON
profundus of Petromyzon. A large muscle extends (dorso-ventrally) along the
branchial septum, recalling by its position the m. constrictor interbranchkdis of
Petrmymn. Two longitudinal muscles run above and below the branchial clefts.
All these muscles are controlled by the IXth and Xth nerves. There is a series
of transverse muscular fibrils in the wall of the pharynx in front of the foremost
branchial cleft ; they are innervated by a branch of the VIIth nerve.
The muscle arising from the hind edge of the sixth branchial cleft is described
with the heart.
4. VASCULAR
SYSTEM
* (text-figs. 3, 4, 5, 6 ) .
Afferent arteries.-The ventral aorta (va.) after leaving the heart almost at once
divides dorso-ventrally into three trunks.
(a) The most ventral one is of small diameter ; it issues from the left side of the
ventral surface of the ventral aorta. After a short run downwards and forwards as
a single vessel, i t divides into two arteries. The left vessel enters the left longitudinal
ventral muscle of the body in front of the heart, the right (at.) passes along the right
side of the thyroid gland (t.) and divides completely into small branches entering
into the gland. This vessel has no further extension.
The origin of the common trunk of these vessels varies in specimens ; in one
specimen it issues from the ventral side of the left first afferent artery, in another
specimen from the common root of the four posterior afferent arteries (2nd-5th
branchial arteries). However, i t originates always from the ventral side and very
close t o the heart, its further course is always the most ventral one, and its branches
have always the same relation to the ventral muscles and the thyroid.
(b) The pair of vessels carrying the blood to the foremost holobranchs issue
from a short common trunk. After a long run forwards under the branchial region,
these vessels turn upwards a t almost a right angle, towards the foremost gills,
forming the first pair of afferent arteries (a,.).
(c) The most dorsal division of the ventral aorta is also very short, and subdivides into a pair of large vessels. At their origin these vessels are twisted in such
a way that the one originating from the left side passes t o the right half of the
branchial apparatus, and that originating from the right side to the left half. The
further course of these vessels can be seen on text-figs. 3, 5 B . Each vessel subdivides into two smaller vessels ; the anterior one gives off the second and the third
afferent branchial arteries and the posterior one the fourth and the fifth afferent
branchial arteries.
The afferent arteries themselves have some peculiarities which must be described
(text-fig. 4). They have all five the same structure. The artery passes mesially
t o the ventral arch (v.) of the afferent artery, then i t enters the gill septum and runs
upwards laterally to the efferent artery ; it extends upwards beyond the septum
between the limbs of the dorsal arch ( d ) of the efferent artery. Before entering
into the gill septum, the afferent artery gives a short branch (av.) which turns sharply
downwards, and runs parallel to $he afferent artery, but in an opposit'e direction,
inside the ventral efferent arch (d.). This branch cannot be seen in text-fig. 3 (inside
view of the branchials), being hidden behind the main trunk of the artery, but it is
shown in text-figs. 4 and 6 .
The thyroid gland in Eurypharynx ( t . ) is apparently supplied with blood directly
by a n afferent artery and thus can be described here. The gland is situated just
in front of the heart on the ventral side of the body, close t o the left side of the
inferior jugular vein (ijv.) and dorsally t o it. The gland together with the adjoining
vessels, is enveloped in a rather loose sheath of connective tissue. To the naked
eye the gland appears as a compact organ, light orange in colour. It is longer than
broad, its length exceeds the greatest length of a branchial cleft. Under a microscope it can be seen that the gland consists of rounded follicles axranged in three
ut A brief account of the vascular system of
Eurypharynx was published in ' Nature'
(Tchemavh, 1946).
385
THE STRUCTURE O F THE LYOMERI
irregular longitudinal rows. The follicles are loosely connected with each other.
The right afferent artery of the most ventral arterial trunk (at.)passes close along
the side of the gland and divides into small twigs which sub-divide again, entering
into the gland. The artery has no further extension.
Nussbaum-Hilarowicz (1923, p. 68, pl. ix, fig. 12) studied the morphology and the
minute structure of this gland in Euryphaynx. He found that the thyroid is situated
in “ un Bpaississement sp6cial du tissue conjunctif de la paroi d’un divertiaulum
pharyngein ” and that the gland is connected anatomically with the respiratory
organs.
3
TEXT-FIG.
4.-Arteries of the second brnnchial arch of Eurypharynr. Inside view ;right side.
Diagrammatic. x 15. Lettering as in text-figure 3 and in key, p. 392.
The fact that the thyroid retains its connection with the gut, suggests a primitive
state of this gland in Eurypharynx. Nussbaum saw large blood vessels connected
with the gland, but does not mention what these vessels are ; as already mentioned,
they are branches of an afferent artery (at.).
Efferent arteries.-The main vessels of the five efferent arteries run in the septa
behind the lst-5th branchial clefts mesially to the afferent arteries. I could not
make certain whether these vessels are single or consist of two vessels united together.
Dorsally the efferent arteries are continuous with the epibranchial arteries, but give
off each a pair (right and left) of lateral commissural vessels, running above the
branchial clefts. Ventrally each efferent artery divides into two lateral commissural
vessels running below the branchial clefts. Thus the efferent arteries of each cleft
unite above and below the branchial clefts, forming a series of vascular loops round
the 2nd-5th branchial clefts. These loops are very similar to those found in
Selachians. The foremost efferent artery sends two vessels towards the head, one
27
JOIiRN. LINN. S0C.-ZOOLOGY,
VOL. XLI.
386
V. V. TOHERNAVIN : FURTHER NOTES ON
(he.) passing above and the other (ha.)
below the foremost cleft. The fifth afferent
artery sends two vessels running towards the tail, above (crna.) and below (pa.)the
6th branchial cleft.
Beside the five vascular loops round the branchial clefts, two series of five dorsal,
and of fiveventral smaller loops are found above (d.)and below (w.) the branchial septa.
These loops are formed by arch-like vessels uniting the lateral commimral branches
of the efferent arteries. They are connected with the additional parts of the gills
situated above and below the gill-septa.
h
A
9 9
B
h
P ?
ea,
Ia,
0
c
TEXT-RO.5 (A, B).-Diagram of the efferent (A) and the afferent (B) arterial systems of
E q p h r y n x , simplified, not to scale; A, dorsal view; B, ventral view. For lettering
see texb-figure 3, or the key to the figures on p. 392.
The dorsal branch of the first efferent artery (he.) passes above the 1st branchial
cleft and runs along the wall of the oral cavity towards the cranium. After pasing
about twice the distance between this cleft and the cranium it gives off a small
branch running upwards, and close to it a second markedly larger one. The first
branch soon divides in the wall of the oral cavity into smaller vessels;&he second
branch runs firat ventrad a t almost a right angle to the main vessel, then turns
caudad and divides into small twigs in the pharyngeal wall not quite reaching the
THE STRUCTURE OF THE LYOMERI
387
branchial apparatus. The main vessel of the artery follows its a h o s t straight
course forwards, gives 'off another small branch running dorsally, and reaches the
suspensorium mandibulae as a very small vessel. I could not follow its further
course.
The ventral branch of the fist efferent rqrtery (ha.)pctsses below the foremost
branchial cleft and runs in the pharyngeal wall obliquely forwards and downwards
towards the lower jaw. At the end of its long course, close t o the mandibulo-quadrate
articulation, i t divides into small branches in the ventral wall of the oral cavity
close to the inferior jugular vein.
I could find nothing suggesting that these arteries or their branches supply with
blood any remnants of a gill.
The dorsal posterior branch of the fifth branchial artey ( c m ) passea above the
sixth branchial cleft and then runs obliquely upwards and backwards. It is soon
joined by a branch of the vagus nerve which runs close to it. The artery turns then
caudad. It corresponds probably t o the coeliaco-mesenteric artery. I did not
follow its further course.
The ventral posterior branch of the Jifth branchial a&y (pa.)has a short run. It
passes below the sixth branchial cleft and then turns sharply upwards behind the
sixth branchial cleft, where it divides into two small branches.
Epibranchial arteries.-The f i s t epibranchial artery (e, ) reaches the lateral aorta
independently from other epibranchial arteries. The second and the third epibranchial arteries meet together in a short common trunk which is soon joined by
the fourth and fifth arteries. This trunk runs upwards and backwards, unites with
the rather thin middle part of the lateral dorsal aorta (la,) and follows its course
as the hind part of the lateral aorta towards the midline of the back where i t reaches
the unpaired dasal aorta, and closes the circulus cephalicus posteriorly.
Lateral dorsal aortae.-Three distinct parts can be distinguished in the main
trunk of the lateral (paired) dorsal aorta ; a large vessel (la,) which extends from
the dorsal end of the first epibranchial aorta to the base of the cranium ; a narrower
vessel (Za,) which extends between the dorsal end of the first epibranchial artery
to the common trunk of the four posterior arteries ; and a large vessel (la,) which
is continuous with the latter trunk and runs dorsad to the median, unpaired dorsal
aorta. Reaching the base of the cranium, the lateral aorta gives off a vessel (ec.),
the orbital artery (external carotid), which runs forwards under the cranium and
enters the orbit. The lateral aorta turns mesially, gives off another branch and enters
the cranium where it probably meets its fellow from the other side, closing the
circulus cephalicus anteriorly. I had no opportunity of seeing the actual union
of the lateral aortae in the cranium and did not follow their further course inside the
cranium.
The median (subvertebral, or unpaired) dorsal aorta has two parts (text-figs. 3,
5 A, 6). The anterior part (uda.)
extends from the cranial base backwards between
the limbs of the lateral aorta to the posterior end of the circu1u.s cephalicus. The
posterior part of the unpaired aorta (udp.) extends from the posterior end of the
circulus wphalicus t o the end of the tail. The unpaired dorsal aorta divides anteriorly
into two branches, and gives off a pair of lateral branches to each metamere.
Nineteen or twenty pairs of such vessels are found in its anterior part (uda.)running
between the lateral dorsal aortae.
The median dorsal aorta has no direct communication with the f i s t epibranchial
artery, and is mainly supplied with blood from the four posterior branchial arteries
The median dorsal aorta has from its right side a thin commiwural vessel (c.)
which unites it with the narrow portion of the lateral dorsal aorta.
I n a carefully dissected specimen it can be seen that this vessel (text-fig. 3, c.) unites
with the median dorsal aorta between the dorsal ends of the two lateral dorsal aortae.
(In this specimen the mouth of the right lateral dorsal aorta lies slightly in front of'
the left one ; text-fig. 3.)
67 *
'
la
at
-
TEXT-no.6.-Diagram of the arterial system of the branchial region of Eiiryphamynx simplified, not to scale, no division of the ventral aorta
and no unions of the epibranchial arteries before they reach the lateral aorta are shown. Left side slightly from above. For lettering
see text-figure 3 or the key to the figiims on p. 392.
ec. external carotid!
ec
c
‘i!
0
c
THE STRUCTURE O F THE LYOMERI
389
A vessel (text-fig. 3, na.), the homology of which is not clear t o me, and which
I could not follow along its whole course, originates from the fifth epibranchial
artery and runs backwards and downwards towards the heart. It soon divides
into two branches which run nearly parallel to each other. They both oome close
to the dorsal side of the pericardium, but I could not see their further course. It
seems possible that they are the nutrient arteries of the heart.
The veins of the head.-The head vein (anterior cardinal or the superior jugular)
leaves the cranium through the jugular foramen, mesially to the articulation of the
hyomandibular with the cranium, and at about the vertical level of the articulating
groove for the condyle of the hyomandibular. This groove is unusually deep,
its roof lies dorsally to the jugular foramen, while its ventral edges lie ventrally
to this foramen. I n this respect the position of the jugular foramen in relation t o
the horizontal level of the articulating groove of the hyomandibular differs from that
typically found in Osteichthyes (comp. de Beer, 1937, pp. 410, 411). However,
this unusual relation may be due to the great flatness of the cranium of Eurypharynx,
while the condyle of the hyomandibular is very large and the groove receiving it
very deep. The facial nerve passes through the jugular foramen ventrally to the
head vein.
The inferior jugular vein is single posteriorly in the region of the branchial apparatus
and of the heart, but paired anteriorly.
showing the relation of the pectoral fins to the pericardium of
Euryphurynx. x 3.3. 7, ventral view ; 8, lateral view (right side).
Zv., ligaments of the ventral muscle of the body ; p . , base of the pectoral fin ;
pc., pericardiurn ; sw.,sinus venosus ; wa, ventral aorta.
TEXT-FIGS.
7, 8.-Diagrams
5 . RELATION
OF THE PECTORAL
FINSTO THE PERICARDIUM.
The heart in Euypharynx lies far away from the cranium on the vertical of about
the 18th vertebra, very close to the ventral surface of the body. The pericardium
is clearly visible through the thin transparent ventral wall of the body. The main
protection of the heart from the outside is the very thick wall of the pericardium.
The close relation of the pericardium to the pectoral fins is unusual. The
pectoral fins are small, and their basal parts are lobate. The fin rays are simple
and not segmented. Though small, the fins are functional and each ray has its
muscles well developed (apparently, two attractors, and a dilatator). The b a d
lobe of the f
h extends obliquely inwards, passes through the peritoneal septum
and inserts into the ventral wall of the pericardium close to its posterior end.
The elastic fibrillae of the pericardial wall extend right into the basal parts of the
fins, and unite i t firmly with the pericardium. The connection of the basal lobe of
the pectoral fin with the pericardium is very firm ; some of the elastic fibrillae of the
pericardial wall pass along the sides of the lobe, some crosR the lobe.
390
V. V. TCHERNAVIN
:
FURTHER NOTES OX
The pair of ventral muscles passing along the midline of the ventral side of the
body are long and narrow. These muscles are firmly attached t o the ventral side
of the pericardium (each muscle by two ligaments, text-figs. 7,8, Zv). The contraction
of these muscles would affect the heart by pressing on i t ventrally and lifting i t upwards. Another narrow long muscle issues from the ventral edge of the sixth gill
cleft, passes close but laterally to the posterior wall of the pericardium and to the
base of the pectoral fin, then turns round the ventral side of the pericardium, where
it spreads out fan-like and is inserted into the ventral longitudinal muscle of the body.
By the contraction of this muscle the posterior part of the heart and the pectoral
fins would be pulled upwards into the branchial chamber. As far as I am aware,
in this relation of the pectoral fins and of the ventral muscles of the body to the
pericardium, Eurypharynx is unique among fishes.
6. SUMMARY
AND CONCLUSIONS.
As I mentioned in my earlier paper (Tchernavin, 1947), the Lyomeri disagree with
many characteristics of the class Osteichthyes, to which they can be referred as having
true bones with cells, the head vein passing out of the cranium medially t o the articulation of the hyomandibular with the otic region of the cranium, and having the
nostrils on the dorsal side of the head.
I n Lyomeri the mandibular arch has no direct contact with the cranium. The
dorsal end of the quadrate unites intimately and directly with the ventral end of
the hyomandibular (no symplectic) ; the dorsal ends of the palatine bones (apparently
fused with the suborbitals) meet each other under the cranium and are attached
by a ligament to the ventral side of the cranium. There is no secondary upper jaw
(premaxillary and maxillary). The infraorbital lateral line runs along the front
part of the upper jaw. The bones of the lower jaw have no connection with the
lateral line system. The hyoid arch consists of one element only-the hyomandibular. It is situated well in front of and far above the branchial cavity, and has
no contact with the: latter. There is no hyoid operculum (no operculum, sub- or
interoperculum, no branchiostegals) ; the preoperculum is also missing. The
branchial apparatus of Lyomeri differs most substantially from that of Osteichthj-es.
The branchial clefts are situated far behind the cranium and close to the ventral
midline of the body, the branchial arches having no contact with the cranium
nor with the vertebrae. As the ventral hyoid elements are missing, and the hyomandibular is situated well above the level of the branchial arches, the foremost
branchial cleft lies between the mandible and the first branchial arch. Eurypharynx
has six functional branchial clefts and jive holobranchs. The hyoid branch of the
facial nerve does not extend behind the foremost visceral cleft. The glossopharyngeal
nerve runs into the septum dividing this cleft from the second one ; branches of the
vagus nerve run behind the third, fourth, Hth, and sixth clefts. Thus, this foremost
cleft is a branchial cleft, homologous to the first branchial cleft of other fishes, and
the sixth branchial cleft of Eurypharynx is homologous to the sixth branchial cleft
of some Selachians ; no such cleft is found in Osteichthyes.
The branchial arches are not ossified; they have no elements uniting them
ventrally, and the right and left parts of the arches are completely separated from
each other. Each such semiarch consists of a single thin rod extending along the
branchial septum (Eurypharynx). There is apparently no arch behind the sixth
branchial cleft. The branchial arches are not <-shaped. The septa between the
branchial clefts are broad and fleshy. The branchial muscles are not attached to
the branchial arches ; they surround the branchial clefts, forming a kind of sphincter
round each cleft. Two longer muscular bands paas above and below the clefts.
The gills extend dorsally and ventrally beyond the branchial septa on the wall
of the gut. There is a special arrangement of the afferent and efferent vessels for
supplying these additional parts of the gills.
The vascular system is unusual. The single ventral aorta is very short, and
almost at once after leaving the heart divides vertically into three short afferent
THE STRUCTURE OB THE LYOMEBI
#
391
trunks. The shortest of the ventral aortae rec& that of Dipnoi. The most ventral
afferent artery supplies the thyroid gland with blood. There are five pairs of afferent
branchial arteries, the foremost of which rune behind the first branchial cleft. Such
an arrangement is never found in Osteichthyes. The afferent branchial arteries
extend dorsally beyond the branchial septum and supply with blood the dorsal
additional parts of the gills. Each afferent artery before entering the gill septum
gives off a branch running in the opposite direction (ventrad) and supplying with
blood the ventral additional part of the gill.
The efferent system presents a singular combination of features which, individually,
are characteristic of Selachians, Osteichthyes and Cyclostomata, and of features
which are unique among fish-like animals.
The efferent branchial arteries, five in number, are united by longitudinal commissural vessels above and below the gill-clefts, forming loops round the clefts,
recalling those of Elasmobranchs. Above and below the branchial septa, arch-like
vessels unite the commissural efferent vessels, forming thus a dorsal and ventral
series 05 five additional loops, which collect the blood from the additional dorsal
and ventral parts of the gills. As far as I know, no such additional series of loops
are found in other fishes.
As in other Osteichthyes there is a paired lateral dorsal aorta, which forms the
circulus cephalicw, emitting no lateral vessels to the muscular segments; i t is
supplied with blood mainly from the first epibranchial artery. Beside the paired
lateral aorta, an unpaired dorsal aorta extends from the posterior end of the circulw
cephalicus t o the base of the cranium, between the limbs of the lateral dorsal aorta.
This anterior part of the unpaired dorsal aorta gives off nineteen or twenty pairs
of intersegmental arteries to the metameres of the body. Posteriorly the dorsal
aorta extends as in other fishes. The unpaired dorsal aorta is supplied with blood,
mainly from the common trunk of the four posterior epibranchial arteries. No such
arrangement is found in Osteichthyes. But a similar structure is found in Myxine,
and rudiments of the anterior part of the unpaired dorsal aorta are found in some
Selachians, and Selachian embryos (Dorn, 1885, fig. 3 ; Ayres, 1879, pp. 197, 220;
Hoimgren, 1946, pp. 65-67). Among Osteichthyes only a minute rudiment, possibly
of this vessel, is found in the common eel (Anguilla) (Ridewood, 1899, p. 949, pl. lxiv,
fig. 16).
It seems worth mentioning that the epibranchial vessels of Eurypharynx present
an almost mirror image of the trunks of the afferent arteries. The first branchial
afferent and efferent arteries are separated from the four others. The four posterior
afferent arteries have a common trunk, which subdivides into two twigs, from which
the second and the third, and the fourth and the fifth arteries issue. The efferent
arteries of the second and third arches unite into a common vessel, which then receives
the fourth and the fifth efferent arteries, forming a common trunk for these four
vessels.
The jugular vein passes out of the cranium through the jugular foramen with
the hyomandibular nerve medially to the articulation of the hyomandibular with
the cranium (as in other Osteichthyes). The inferior jugular (cardinal) vein is unpaired posteriorly (in the region of the branchial apparatus) but paired in front.
The lobate basal parts of the pectoral fins unite with the outer side of the pericardial wall in Eurypharynx. In Sampharynx (Tchernavin, 1947) the basal parts
of the pectorals articulate laterally (not mesially) with a reduced piece of the pectoral
girdle, which apparently corresponds to the scapula. I found no secondary shoulder
girdle in Lyomeri.
In my earlier paper I have shown also that in Lyomeri the bones of the cranium
articulate movably with each other, so that the cranium can markedly change its
shape ; Lyomeri have no supraoccipital, no ossified lateral ethmoids, and the parasphenoid is very small with no lateral processes (Eurypahrynx), or absent ( S a m pharynx) ; finally, the cover bones on the dorsal side of the cranium are unusual
and their homologies are not clear. One has to remember also that the fin rays of
392
V. V. WHERNAVIN : FURTHER NOTES ON
Lyomeri are ossified but not segmented and not branched, in disagreement with
one of the main charateristics of Osteichthyes.
Where can the Lyomeri be placed in the system of Fishes ? It seems that there
is no ground for relating the Lyomeri to any of the known orders of Osteichthyes,
and that the Lyomeri can be readily opposed to all known Bony Fishes. If the
Lyomeri are included in the group Osteichthyes on the ground of their ossified
skeletons (which is not a sufficient character), and owing to the mesial position of
the head vein in relation t o the hyomandibular (which is a n important feature),
the main characteristics of the class Osteichthyes must be revised.
Such fundamental characters of Osteichthyes rn the presence of a hgomandibular
operculum, symplecticum, parasphenoid, secondary upper jaw, secondary shoulder
girdle, lepidotrichian type of fin rays, no more than five branchial clefts and no more
than four and a half gills, reduced and <-shaped branchial septa, efferent arteries
separated from one another, and the absence of the median anterior unpaired aorta,
can no longer be used as features characterizing the Osteichthyes, if the Lgomeri
are included in this class.
One can see also that by the Lyomeri having several Selachian characteristics,
the differences between the Osteichthyes and Selachians are less definite.
A study of the development of Lyomeri would be of great help for a judgment
on their relationship with other fishes. But all that is known about the development
of Lyomeri is that their larva is " Leptocephalus "-like.
7. KEYTO
first-fifth nfferent branchial nrteries.
anus.
UlL.
ut.
artery of the thyroid gland.
nu l-uTs
ventral branch of the nfferent
artery.
commissural Gessel uniting the
C.
lateral dorsal aorta with the
unpaired dorsal aorta.
lateral commissural dorsal vessels
cdl-cd,.
of the efferent arteries.
CIllU.
coeliaco-mesenteric artery.
cv,-cv,
lateral commissural ventral vessels
of the efferent arteries.
dorsal arches of the efferent
d1dS.
arteries.
el-es.
epibranchial arteries.
eul-eas.
efferent branchial arteries.
ec.
orbital artery (external carotid).
folds in the wall of the oral cavity.
f.
foramen jugularis (in the prootic).
fj.
foramen for the IX and X nerves
fo.
(in the lateral occipital).
gills.
g
ha.
ventral branch of the first branchial efferent artery.
he.
dorsal branch of the first branchial
artery.
hyoid nerve ( V I I ) .
hf.
ILV.
head vein (jugular, cardinal).
hnif.
hyomandibular trunk of the facial
nerve.
ijv.
inferior jugular (cardinal) vein.
1.
ligaments of the lateral muscle
of the body.
la,, la, ,Za3.parts of the lateral (paired) dorsal
aorta.
a1-a5
THE
FIGURES.
11.
lv.
ma.
tllj.
n.
)La.
11g.
W l .
UL'.
I1U1-lLV5.
IEUl.
0.
1' '
pa.
PC.
Pf.
r.
S.
SO.
RU.
suj.
t.
U1-U5.
oa.
?f.
iidu.
udp.
uj.
laternl line.
ligaments of the 1-entral muscle
of the body.
t i t . udd iictor hyomu rid ib ii1tiri.s.
mandibular nerve ( V I I . )
nost.ri1.
branch of the 5th epilmmchial
artery.
glossopharyngeal nerve.
branch of the glossopliaryngeal
nerve.
branchial trunk of the vagus
nerve.
branches of the vagus nerve.
lateral vagus nerve.
eye.
base of the pectoral fin.
posterior ventral art.ery passing
round the sixth brancliial cleft.
pericardium.
pectoral fin.
rays of the pectoral fin.
suspensorium mandibulae.
infraorbital branch of the lateral
line.
sinus venosus.
symphysis of the upper jaw.
thyroid gland.
ventral arches of the efferent
arteries.
ventral aorta.
facial vein (?).
anterior part of the unpaired
dorsal aorta.
posterior part of the unpa.ired
dorsal aorta.
upper jaw.
J O U R N . L I N N . SOC. LOND. Z O O L . VOL. 41. PL. 8.
TCHERNAVIN.
A. THE GILLS OF
EURYPHARYNX.
B. THE GILL CLEFTS OF
EURYPHARYNX.
THE STRUCTURE OF THE LYOMERI
393
8. REFERENCES.
AYERS,H. 1889. The morphology of the carotids, based on a study of the blood-vessels of
Chlaiiiidoselachus anguineus Garman. Bull. Mus. Comp. 2001.17, pp. 191-223, pl.
DE BEER,G. R. 1937. The development of the Vertebrate skull. Oxford, 552 pp., 143 pls.
BERG,L. K. 1940. Classification of fishes, both recent and fossil. Travaux Inst. Zool. Acad.
Sci. U.S.S.R. 5, 2, pp. 1-517, 188 figs. (Russian and English text.)
BERTIN,L. 1934. Les poissons Apodes appartenant a u sous-ordre des Lyombres. Carlsbeg
Foundation’s Oceanogr. Exped. 1928-30, and previous ‘ Dana ’ Exped. ‘ D a m ’ Report,
no. 3, pp. 1-56, 47 figs. 2 pls.
DORN,A. 1885. Studium zur Urgeschichte des Wirbe1thierkorpers.-VIII. Die Thyroidea bei
Petromyzon, Amphioxns und die Tunicaten. Mitt. 2001.Stat. Neapel, 6, pp. 49-92.
8 plates with 29 figs.
HOLJIGREN,
N. 1942. Studies on the head of fishes, 3, The phylogeny of Elasmobranch fishes.
Acta Zoologica, Stockholm, 23, pp. 129-251, 54 figs.
HOLYGREN,
N. 1946. On two embryos of Myzine glutinosa. A c h Zoologica, Stockholm. 27,
pp. 1-90, 56 figs.
NESSBAGJI-HILAROWICZ,
J. 1923. Etudes d ’ h a t o m i e compart5e sur les poissons provenant des
compagnes scientifiques de S.A.S. le Prince de Monaco, 65, 100 pp., 12 pls.
RAUTHER,
M. 1937. Kiemen der Anamnier, in Bolk’s Handbuch der vergleichenden Anatomie
d . Wirbeltiere, 3, pp. 211-278, 93 text-figs.
C. T. 1912. The anatomy and classification of the teleostean fishes of the order Lyomeri.
REGAX,
Ann. Mag. Nut. Hist. ser. 8, 10, pp. 347-349, 1 fig.
RIDEWOOD,
W. G. 1899. On the relation of the efferent branchial blood-vessels to the ‘ circulus
cephulicus ’ in Teleostean Fishes. Proc. Zool. SOC.London, pp. 939-956, 3 pls.
TCHERNAVIN,
V. 1946. A living Bony Fish which differs substantially from all living and fossil
Osteichthyes. Nature, 158, no. 4019, p. 667.
TCHERNAVIN,
V. 1947. Six specimens of Lyomeri in the British Museum (with notes on the
skeleton of Lyomeri). Journ. Linn. SOC.Lond., Zool. 46, pp. 287-350, 15 text-figs. 2 pls.
WATSON,D. M. S. 1937. The Acanthodian fishes. Phil. Trans. Roy. SOC.London, no. 549,
228, pp. 49-146, 25 text-figs, 14 pls.
EXPLAKAITION OF T H E PLATE.
PLATE
8.
A. The gills of Euryphnrynx ; i n situ ; left side. The fold covering the gills removed. x 8 .
In front of the first holobranch the foremost branchial cleft can be seen ; behind the fifth
holobranch the sixth cleft is seen. The lower (ventral) part of the fifth holobranch is partly
covered by the gill filaments of the fourth holobranch.
B. The gill clefts of Euryphnrynx, right side. ?, 8. The gut is dissected and the inner apertures
of the six hranchial rlcfts are seen from the inside of the gut. Gill filaments are seen through
the clefts.