"TIE CIRCITCATION O F BLOOD IN OPIIIOCEPRALUS PUNaTATUS BLOCR
49
The circulation of Mood in the air-breathing chambers of Ophiocephnlus pumtatus Rloch. By S . H. LELE, The Royal Institute of Science, Bombay.
(Communicitted by Or. S. L. HORA,F.L.S.)
(With 4 Toxt-figuree)
[Read 22 Oct,obor 19311
THEsnake-headed fishes of the genus O p h k p h u l u s have attr,wted the attention
of naturalists and zoologists for a very long time on account of their habit of
temporarily leaving their aqueous homes and of going on excursions over
surrounding marshy lands. This unusual behaviour is rendered possible by
the possession of special air-breathing organs in addition to the gills. Max
Rauthcr in ' Die Akzessorischen Atmungsorgane der Kriochenfische' (Ergebnisxe
11. Fortsohritte d. Zool. vol. ii, 1910) has described in detail the air-breathing
organs of 0.striatus, and 13. K. Das in ' The Bionomics of certain Air-breathing
Fishes of India, together with an Account of the Development of their Airbrrathing Organs ' (Phil. Trans. Roy. SOC. Lond B, vol. ccxvi, 1928) has dealt
with the structurc and development of air-breathing organs in ' Snake-headed '
Fishes. In both these papers the network of capillary blood-vessels in the walls
of the air-chambers has been described and illustrated. As, however, the
conditions observed in Ophiocephalus pumtutus differ in certain salient features
from those described by thew authors, it has bcen thought advisable to give
a description of the circulation of blood in its air-chambers.
STRUCTURE
OF AIR-CHAMBER
There arc two air-chambers, onc on cach sidc of the auditory region of the
skull. When the lower jaw, with part of the gills, is removcd, each of them
is seen as a deep pit in thc roof of thr mouth, lying between thc first gill-arch
and the hyomandibultir (text-fig. 1, A . C . ) . It is a spacious cavity, extending
posteriorly to the last pharyngeal cleft and communicating freely with the
mouth-cavity on the one side and the gill-chamber on the other side. When
exposed from the side (text-fig. 2), it has an oval outline and is seen to lie between
the roof of the pharynx and the thin rocfing bones of the skull. As the cavities
have cnlarged, the auditory region of the skull appears to have been compressed
between them.
In order to increase the respiratory area two processes frcjm the surrounding
bones project into the air-chanil)er. The hyomandihular process (text-fig. 1, H . P . )
is in the form of a thick, short, vertical plate. passing obliquely inwards and
LISS. JOURS.-ZOOLOGY,
VOL. X X X V l l I
4
50
MR. 8. R. LELE ON THE CIRQULATION OF BLOOD IN THE
backwards. The uecond process arises from the cpibranchial of the first gillarch (text-fig, I , L.P.),and has the form of a thin broad plate lying between the
hyomandibular procew and the outer wall of the air-chamber. This epibranchial plate is homologous with thc lahyrinthine organ of Ambas, and may
be termed the labyrinthine plate. The cpibr.znchia1 of the second gill-arch
also has a shelf-like projection in front, Similnrly, thero is a lateral flap
TEXT-FIO.
1.
---A.O
A.C.
HJ?
LP
---A.C.
RR
---p.T.
---0e.
Ventral viow of tho air-chambers of 0. punctalru, as soon on removal of the lower llalf
of the h o d with the vontral halves of tho branchial archon on the right sido and with
the surrowiding parts on the left nido 80 BB to expono the whole of tho loft air-chomhr
(diagrammatic).
A.G., air-chamber ; D.R., branchial arches : H . P . , hyomandibulor proccrss ; L.P., labyrinthine plato of the firnt opibranchial ; Oe., oesophaguH ; P.T.,pharyngeal tooth ;
K O . , roof of the oral cavity.
from the narrow base of the bruin-case. These two latter processes join
to form the floor of the air-chamber and conceal most of its posterior part
in a ventral view.
Tho air-chamber is lined by a. thin, richly v&qcular epithelium, which is
continuous with the mucous membrane of the mouth-cavity and with the inner
ATR-BREATHING CHAMBERS OF OPHIOCEPHALUS PUNCTATUS BLOCH
61
lining of the gill-chamber. Its superficial layer is smooth, except a t the pasterior end of the chamber. Rctween the epithelial membrane and the surrounding bony capsule there is a thick layer of loose connective tissue which
contains the largc and small blood-vcsscls with thcir innumerable finer branches.
The subjacent connectivo tissue is so loose that the epithelial wall v c ~ yeasily
comes iiway from thc surrounding bones and the muscles which lie around its
posterior parts.
CAPILLARIES
The epithelial membrane is relatively thick and composed of many layers of
cclls towards thc inner side and posterior end of the air-chamber, and also
whcrc it covers the epibranchial and hyomandibular processes. It contains
TEXT-FIQ.
2.
0 e.
A.C.
M.C.
S.E.
Lntcrnl view of the air-chamber of 0 punrlatzr.9 exposed by complctely removing
lateral parts of the body (dingrammatic).
A C., nir-chainhr : M . C . mouth-caklty ; Oe., oosophaps ;
S h'., socket of tho PYP.
numerous mucous glands, and is richly supplied with blood-capillaries. The
brtinchcs of the subjacent blood-capillaries reach the surface in the form of
loops and tufts passing through the layer of epithelial cclls, as described
and illustrated by Rauthcr in 0. stridus and by Das in 0. punctatus. The
dorsal and outcr sides of the air-chamber have a relatively thin membrane,
which has been said to
' practically non-vwcular ', but sections trcated with
Mallory's connective tissue stain show it to be highly vascularized. Here the
epithelium is reduced to a single layer of squarnous cells (text-fig.3, S.E.), and
is stretched by the protruding blood-capillaries. The capillaries (B.C.) are
large, and appear a t first sight to be only resting on the surfacc of the lining
of the air-chamber ; they are so numerous. and their network so close-meshed,
4*
52
MR. 8. H. LELE ON THE CIRCULATION OF BLOOD IN THE
that in section a continuous series of these transvervcIy cut capillaries iy usunlly
seen. Their connections with tho underlying vessels are often indicated by
Mood-corpuscles situatccl obliquely in the thin intervening tissue. This litycr
of conncctive tissue is fibrous and is underlaid by a very loose connective
t,iswe with large intcrcellular spaces. The large blood-vesseln come to the
siirfacc of the lattcr tiwiie :tnd form a noticeablc layer of large and small Iloodvcssels immediately below thc thin fibrous layer. Thc blood-vessels are lined
with niimcrous pigment-cells and can be easily seen. The single layer of flitttencd cpithcliid cells, with the undorlying capillary network, is anitlogous
to the respiratory wall of thct alveoli or air-sacs in thc l ~ ~ofi land
g ~ vertcbrutcs.
TEXT-FIO.
3.
B .v
Soction of tho siiprrficial respiratory ltrycr of tho wall of the air-chambor
of 0.punchfun (diagrammatic).
N.C., blood-capillary; R. V . , blood-vossol ; b’.C., filJrous conncctive tissue ; L.C.,loose
roniirctivo tissuo ; R.B., red bh~ntl-cnrpiisalos; S’.E,, sqiianioiis opithelium.
&OOD
CIRCULATION
The capillitric~sof t.he air-chambcr wc iiltimately conncctcd with the 1st
and 2nd afferent branchial artcries on the one sidc and with the anterior jugiiliir
vein on the ot,hcr. The 1st afferent branchial artery (tcxt-fig. 4, A . T ) ,hesides
giving b~i~1~clit:s
to its gill-filaments, is continued as hrge labyrinthine artery
( L A.), passing t.o the anterior end of the air-chitmber across the 1al)yrinthinft
platc of t h 1st tqibranchial. This artery, af.kr emerging from the gill, givw
off a Iargc brcmch, and lwth it and this branch give off smallcr branches. Tho
2nd itffcrent itrttbry is similarly continued lxyond thc gill ( A. A .). It divides
into two, each of which branches out on the surface of the posterior part of thc:
wall of thc tLir-(:llii1llhr. The efferent arterics of the 1st i ~ n d2 n d gills brcak
up into numerous small branches in the wall of the rLir-chamlwr.
Thc capillurics of thc! itir-c:hamlw drain into the tributaries of the anterior
jtigiilitr vein (text-fig. 4, A . J . ) . The latter thus returns to the hearb the deoxy-
AIR-BREATHING CHAMBERS OF OPHIOCEPIIALUS PUNCTATUS BLOCH
63
genated blood from the anterior part of the bcdy, and also the Oxygenated
Mocd from the first two gills and the air-chamber. Thus it is seen that thc
first two gills of each side do not directly supply oxygenated blood to the rest
of the body through the dorsal aorta, as is usually the case in fishes.
On the 3rd and 4th effcrent branchial arteries (text-fig. 4, E . III, E . IV)
join the supra-branchial artery (S.B.)of their side. Further these efferent
branchial arteries are found to be in direct communication with the afferent
branehials of these two gills. After giving branches to the gill-filaments,
TEXT-IUQ.
4.
Blood-vesscls of the air-chamber and branchial arterial system
of 0. punctulua (diagrammatic).
A . I, first afferent branchial artory ; A . A . , air-chambor artery arising from tho second
afferent artery ; A . J . , antorior jugular vein ; C . M . , coeliaco-mcsentoric artery ;
D . A . , dorsal aorta ; E . III &. IV, third and fourth offerent branchial arteries ; G., gills ;
Ht., heart, ; L.A., labyrintllino artery ; O N . ,orbito-narral artery ; P.C., postorior
carotid artery ; S.B., supra-branchial artory ; S.C., subclavian artery.
they continuo as large vessels to join the supra-hranchial of their side. Thus
the 3rd and 4th branchial arteries now form two arterial arches, and take most
of the blood passing through them directly to tho central arterial system without
oxygenation in the branchial filaments of these two gills, which are relatively
very small. The blood which flows to them from the two arches appears to
be distributed, after oxygenation, to the neighbouring parts.
54
THE CIRCULATION OF BLOOD IN OPEIOCEPEALUS PUNC'f'ATUS BLOCB
The 3rd efferent branchial joins the supra-branchial of its side in front
of the transverse commissural vessel joining thc two supra-branchiah. The
supra-branchial of the left side, after giving off the left subclavian artery (S.C.)
und being joined by the 4th efferent branchial (h'.IV), is continued posteriorly
as thc dorsal w r t a ( D . A . ) . Similurly, after giving off the right snbclilviiln
artery and after being joincd by the 4th arterial arch, the right supra-branchial
is continued as the coeliaco-mcsenteric artery which soon divides into two
large vessels. Anteriorly both the supra-branchials receive the orhito-nasal
(O.N.)and posterior carotid arteries (P.C.)of their sides.
REMARKS
Kauther has observed in 0. etriatus that the first two uffcrcnt branchial
arteries exhaust themselves in giving off branches to the filaments of t.hc first
two gills, und that the arteries of the air-chamber are branches from the efTt:rc:nt
branchial arteries of these two gills. Uas has shown that tho air-chambers
of the Ophiocephalid fishes develop iLs pockets of' the pharynx. Putting
these two facts together, it appears that in 0. stri(itus, although the pharyngeal
tyithclium has increuscd and bulged out, and has tuken on the respiratory
function, its vascularizntion is not greatly modified, sinoc IL supply from tlic
effcrcnt branchiuls might be expected in an organ in this position. In 0.punctalus, howcver, the arterics of the air-chamber start directly from tho afferent
branchial arteries, and thus it appears that the vasculurization of its chambers
is more efficient and more advanced than in 0.stridus so fur as aerial respiration
is concerned. This is so bccause the blood-stream does not puss through the
capillaries of the gills before going to the air-chamber. The britnches of the
cfferent branchials of the first two gills thidt supply blood to the air-chambers
in 0. puunctatus may be regarded mainly as nutrient arteries of the walls of
the air-chambers.
From the modifications of the branchial iLrterics noted above and from the
fbct that the fish dies when deprived of uccess to utmospheric oxygen (Uas,
op. cit. p. 205, Experiment e ) , it is evident that its air-chambers play an important part in the respiration of the fish. It ifi also clcur that the blood oxygenated
in thc air-chambers is mixed with the venous blood from thc rest of the body,
the resulting mixture being then supplied to the body as arterial or oxygcmtcd
blood.
This investigation was carried out p r t l y a t the Royd hstit.utc of Scicnecb,
Homb;Ly, ttnd partly in the Department of Occttnography, University of Liverpool. My best thanks are due to Prof. 1'. K.Awati, Bombay, and Prof. J. Johnstone, Liverpool.