Histochemistry and the structure of the skin of a murrel, Channa striata

(Bloch, 1797) (Channiformes, Channidae). I. Epidermis

Department ofzoology, Banaras Hindu University, Varanasi221005, India

Received October 25,1974

MITTAL,A. K., and T. K. BANERJEE.1975. Histochemistry and the structure of the skin of a
murrel, Channa striata (Bloch, 1797) (Channiformes, Channidae). I. Epidermis. Can. J.
Zool.53: 833-843.
Can. J. Zool. Downloaded from www.nrcresearchpress.com by UNIVERSITY OF MICHIGAN on 11/11/14

The functional organization and cytochemistry of the epidermis of an air-breathing fish,

Channa striata, is described. In the basal cells a dense population of mitochondria, strong
alkaline phosphatase, and succinic dehydrogenase activity indicates high metabolic activity. In
the outermost layer, polygonal cells showed strong succinic dehydrogenase activity and elabo-
rated sulfated acid mucopolysaccharides and lipids. Mucous cells were also numerous. A new
term, 'sacciform granulated cells,' is proposed for the 'sacciform cells' or 'granular cells.' The
contents of these cells are basic proteins. A thick coat of slime containing mucopolysaccharides,
lipids, and basic proteins is probably important in keeping the skin moist for cutaneous respira-
tion, retarding the rate of water loss by evaporation, facilitating burrowing in the mud and
swimming movement in water, and protecting the skin from bacterial and fungal attacks. A
relatively thin epidermis (32 pm on the general surface, 18 pm at the posterior free margins, and 6
pm below the scales) in conjunction with vascularization of the stratum laxurn probably assists
cutaneous respiration.

MITTAL,A. K . , et T. K. BANERIEE.1975. Histochemistry and the structure ofthe skinof amurrel,

Channa striata (Bloch, 1797) (Channiformes, Channidae). I. Epidermis. Can. J. Zool. 53:
833-843.
On dicril lbrganisation fonrtionnelle et la cytochimie de I'epiderme chez un poisson i
For personal use only.

respiralion airienne, Cllanna srriafa. Dans les cellules de base. la population de mitochondries
est dense, I'activiti de Fa phosphatase alcaline et de la dishydrogiinase succinique sont 6Ievies.
ce qui indique une activie rniraboliqve importanre. Dans la couche la plus exteme, les ceIlules
polygonales sont te sikge d'une grande activitE de la dkshydrogknase succinique et efaborent des
rnucopolysaccharides acides sulfatks e l des Iipides. Les cellules rnuqueuses sont aussl pksentes
en grand nornbre. On propoge le teme de "cellrtl~ssaccifonnes gwnulkes" en rernplacement des
anciens rermes "cellules saccifonnes" eu "cellules gmnulaires." Le contenu des ces cellules est
constitui. de protiines de base. On observe une epaisse couche visqueuse contenant des
rnucopolysaccharides, des lipides et des protkines de base; cette couche est probablement
importante pour garder la peau hurnide, permettant une bonne respimtion cutanie, pour retarder
la perk d'cau par 6vapomtion et pour faciliter I'enfouissement dans la h u e et les mouvements
natatoires dans I'eau et, enfin, pour protkger la peau contre les infestations par les bactkries et les
champignons. La respiration cutanee est probablement favorisee de plus par un tpiderme
relativernent mince (32 pm en genkral, 18 pm aux bordures posterieures libres et 6 pm sous les
tcailles) associe B la vascularisation du stratum laxurn. [Traduit par le journal]

Introduction The present investigation examines the func-

Channa striata is an air-breathing freshwater
fish belonging to the family Channidae, order
Channiformes (Greenwood et al. 1966). It can
survive for months without water when buried
in moist soil (Hora and Pillay 1962). According
to Giinther (1880), the members of the family
Channidae are able to survive droughts, living
in a semifluid mud, or lying torpid below the
hard-baked crusts in the bottom of a tank from
which all trace of water has disappeared.
'This investigation was supported by Research Grant
No. 38(131)/72 GAU-I1 from the Council of Scientific
and Industrial Research, Government of India.
tional organization of the epidermis of Channa
striata in relation to its peculiar mode of life by
examining the cytochemistry of the various epi-
dermal components.
Materials and Methods
Fish of about 11 cm in length were collected from local
ponds and rivers at Varanasi, Uttar Pradesh. Skin frag-
ments of about 8 x 5 mm were cut from the back be-
tween the dorsal fin and the lateral line and fixed in
Bouin's fluid, Helly's fluid, Regaud's fluid, and 10%
neutral formalin. Ethyl alcohol was used as a dehydrating
agent. Paraffin sections were cut at 5 pm. For lipid
histochemistry, tissues were fixed in 10% neutral formalin
and form01 calcium; for enzyme studies tissues fixed in
fresh, cold 1 0 z neutral formalin or cold absolute acetone
 834 CAN. J. ZOOL. VOL. 53, 1975

were used, and frozen sections were cut at 15 to 30 pm
using an American Optical cryostat.
Sections were stained with Mallory's triple stain
(Jones 1950), Verhoff's elastin stain (Lillie 1954), and
Ehrlich's haematoxylin counter-stained with eosin (H/E).
Periodic acid - Schiff's .(PAS) technique (McManus
1946) with or without prior treatment with saliva/malt
diastase for I h at 37°C (Lillie and Greco 1947) was used
to demonstrate mucosubstances. The acidic and sulfated
nature of the mucopolysaccharides was determined by
metachromatic reactions with thionin (Pearse 1968),
toluidine blue buffered at pH 2-5 (Tock and Pearse
1965), and alcian blue solutions at pH 0.5-1.0 (Lev and
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thick layer covering the outer surface of the
distal part of the underlying scale.
The epidermis may be divided into three
layers: the stratum germinativum (basal layer),
the middle layer, and the outermost layer
(Table 1; Fig. 1).
Stratum Germinativum
This was mainly composed of a single layer
of basal cells (Table 1; Figs. 1, 2, and 3) on a
thin basement membrane which was diastase

Spicer 1964). Acidic and basic proteins were differen-
tiated by the acid solochrome cyanin method (Pearse
1968). Calcium was demonstrated by the alizarin red
S method (Lillie 1954). Heidenhain's iron haematoxylin
(Claydon 1955) and Regaud's iron haematoxylin (Lillie
1954) were used to stain mitochondria, and nuclear
deoxyribonucleic acid (DNA) was shown by the Feulgen
reaction (Pearse 1968). The dihydroxy-dinaphthyl-
disulfide (DDD) technique (Barrnett and Seligman 1952),
for the demonstration of bound sulfhydryl groups of
cysteine, and Papanicolaou's stain (Gurr 1958) for
keratin were also used. Alkaline phosphatase and suc-
cinic dehydrogenase activity were demonstrated using the
calcium cobalt method (Gomori 1952) and nitro-blue-
tetrazolium (nitro-BT) method (Pearse 1972), respectively.
Sudan black B and Oil red 0 techniques for lipids
(Casselman 1959). and the Acid haernatin method (Baker
1946) for the localization of phospholipids were also
applied.
For personal use only.
resistant; gave weak positive color reactions for
sulfated acid mucopolysaccharides, phospholi-
pids, and calcium; and showed moderate
alkaline phosphatase activity (Table 2). Re-
gaud's iron haematoxylin and Heidenhain's iron
haematoxylin preparations for mitochondria re-
vealed the presence of darkly stained fine mito-
chondrial granules in the perinuclear cytoplasm
concentrated mainly at the apical ends of the
basal cells (Fig. 2). These areas of the cells
showed moderate succinic dehydrogenase acti-
vity and gave strong reactions for alkaline
phosphatase (Fig. 7). The cell membranes were
smooth without any differentiation of inter-
cellular cytoplasmic bridges.
Between these cells were found small irregular

Observations lymphatic spaces which were very often inter-

The average thickness of the epidermis
covering the outer surface of scale is about 32
pm. It is thinner (ca. 18 pm) near the posterior
free margins of the scale and very thin (ca. 6
pm) on the underside of the scale, where it runs
for a short distance and then continues as a
- -
connected with each other, establishing a well-
defined lymphatic plexus. One or two small
lymphocytes (Tables 1 and 2) were invariably
found inside these spaces (Figs. 1 and 3).
Middle Layer
This was mainly composed of unicellular

ABBREVIATIONS: BC, basal d l ; DL, basal layer; BM, basement membrane; LS, lymphatic space; MC,
mucous cell; ML. middle layer; OL, outer Iayer; PC, pigment cell: PEC. Polygonal epidermal cell: SGC,
saccirorm granulated cell.
FIG. I . Cross section showing the general organization of the epidermis of Channa striata. Note the
presence of n saccifom granulated cell (arrow) the contents of which appear homogeneous in nature.
[Ehrlich's haematoxylin/eosin. Rouin's fluid fixed tissue.) x 2280. FIG.2. Part of the epidermis showing a
den% population or mitochondria at the apical and perinuclear areas (arrows) of the basal cells. (Regaud's
iron haematoxylin.) x 3420. FIG.3. Epidermis showing mucous cells containing flat basal nuclei. and
opening Lo the surraw by small pores. Nore thc presence of lymphatic spaces (arrows) containing lympho-
cytes between the basal cells. (Ehrlich's haematoxylin/eosin.) x 2280. FIG.4. Epidermis showing saccirom
granular cells (arrows) having granular contents and openina to the surface. (Ehrlich's hacmatoxylin/eosin,
Helly's fluid fixed tissue,) x 2960. FIG.5 . Epidermis showing the presencc of lipids (sta~nedblack) in the
cells of the outermost layer. The peripheral areas OF the glands (arrows) also gave weak positive reactions.
(Sudan black. 2 0 - ~ mfrozen sect ion.) x 1825. FIG.6. Epidermis showing phospholipids at rhc free margins of
the polygonal cells of the outermost layer (arrows) and at the peripheral cytoplasm of mucous cells and
sacciform granulated cells. (Acid haemat in test, 2 h r n frozen section.) x 2780. Frc. 7. Epidermis showing high
alkaline phosphatase activity in the basal ceIls(arrows). Note weak reaction at the peripheral areas of poly-
gonal cells. (Calcium cobalt method for alkalinc phosphatase, 30-pm frozen section.) x 3420. FIG. 8.
Epidermis show~ngmucous celts (~tainedgreenish bIue with a purplish tinge in original) secreting muco-
polysaccharides forming a thick coat on the sudace. (Periodic acid - Schiff's/alcian blue.) x 3420.
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MITTAL AND BANERJEE: SKIN OF CHANNA STRIATA. I. EPIDERMIS

835
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TABLE 1
A summary of the cell types and their cytology within different layers of the epidermis of Channa striata

Average dimensions. Dm
- - -

Epidermal layers Cell types Shape Height Width Cytoplasm Nucleus

Basal layer Basal cells Columnar. 7.0 5.0 Homogeneous, slightly Centrally placed, prominent.
(stratum cuboidal o r eosinophilic dilated, oval or spheriml
germinativurn) almost f l a ~ , with welldifferentiated
low cuboidal, chromatin material and
where ~ h c deepIy stained nucleolus
epidermis i s
very thin
Lymphocytes Irregular, 2.9 2.9 Very littlc in amount, Eccentrally placed, round, o
>
roi~ndo r oval homogeneous. slightly deep1y stained nucIeus ?
basophilic and is thrown without much differentiation ?
into pseudopodia-like o f chromatin material and N
processes nuclcolus 0
Middle layer Polygonal Polygonal
P
10.0 3.5 Homogeneous, slightly Centrally placed prominent. r
cells eosinophilic round or ova[ with wcll-
differentiafed chromatin
6?
material and deeply W
VI

stained nucleolus
Mucous cells Elongated flask- 30.0 8.5 Homogeneous, Darkly stained, basal, flat VI
5
shaped or sac- slightly or crescentic, without much
like basophilic differentiation of chromatin
material
Sacciform 25.0 13.0 Homogeneous, Basal. round or oval with
granulated slightly well-differentiated chromatin
cells basophilic material and nucleolus
Outermost Polygonal Polygonal or 6.0 5.0 Homogeneous, Centrally placed. round or
layer cells roughly slightly oval having well-differentiated
triangular basophilic chromatin material and a
deeply stained nucleolus
Chloride 6.0 2.5 Granular, Basal, spherical or oval,
cells eosinophilic without much differentiation
of chromatin material
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TABLE 2
A summary of the cytochemistry of the various components of the epidermis of Channa striatu

Polygonal cells
Sacciform
Serial Cytochemical Basement Basal Middle Outermost Mucous granuIated
No. technique Fixative Section Reference membrane Lymphocytes cells layer layer cells cells
Schiff's Bouin's fluid, Paraffin Pearse 1968 - - - - -
without IOZ neutral
oxidation formal i n
Periodic acid - Bouin's Ruid, Paraffin McManus 1946 +M - +M +M -
Schjif (PAS) I neutral
rormal in
Biastaso/PAS Bouin's fluid, Paraffin Lillie and +M - +M +M -
10% neutral Greco I947
fomalin
SaIiva/PAS Bouin's fluid. Paraffin Pearse 1964 +M - +M +M -
1% neutral
formalin
Alcian blue, Bouin's Ruid, Paraffin Lev and +GB - +GB +++GB -
pH 0.5-1.0 10% neutral Spicer 1964
formalin
PASlAB Bouin's fluid, Paraffin Pearsc 1968 +Pur - +Pur + + +GBP -
10x neutral
formalin
AE/PAS Bouin's fluid, Parafin Peam 1968 +PUT - +Pur + + +GBP -
10% neutral
Formalin
Th ion ine Bouin's fluid. Paraffin Parse 1968 +meta + + ortho + + +meta f + +meta + +ortho
10% neutral
formatin
abtuidine Bouin's h i d , Paraffin Tock and
Rlue 10% neutral Pearse 1965
formalin
pH 2 - +ortho +meta - +ortho
pH 3 + meta + ortho + fmeta - + ortho
pH 4 + meta + +ortho -
+ + +meta + + meta + +ortho
pld 5 + meta 7+ ortho + + +meta + + +meta + +ortho
Mallory's Helly's fluid Paraffin Jones 1950 +B1 + +OR + B1 + B1 +++R
triple stain
Sudan black B 10% neutral Frozen Casselman +B - ++B IkB -
formalin, 1959
form01
calcium
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838
CAN. J. ZOOL. VOL. 53. 1975
 MITTAL AND BANERJEE: SKIN OF CHANNA STRIATA. 1. EPIDERMIS
glands: the mucous cells and the sacciform
granulated cells. Between the gland cells were
polygonal cells (Tables 1 and 2; Figs. 1 and 3)
which were often vertically elongated as a result
of the lateral pressure of the glands. Fine inter-
cellular spaces were discernible between these
cells. Using Heidenhain's and Regaud's methods
for mitochondria, a few minute black granules
were seen inside polygonal cells. They did not
give positive color reactions for mucopoly-
saccharides, lipids, or calcium. Weak succinic
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dehydrogenase and alkaline phosphatase activi-
ties were, however, discernible (Table 2).
Mucous Cells
The mucous cells were large (Table l), very
often reaching up to the basal layer (Figs. 3, 6,
and 8) and opening on the surface by small
pores through which they voided their secre-
tions to form a thick coat over the surface of the
epidermis (Figs. 3 and 8). Because of the heavy
accumulation of secretory products, the cyto-
plasm and nucleus formed a thin rim at the
periphery of each cell (Fig. 3). Secretions were
basophilic, refringent, vacuolated, and con-
tained strongly acidic sulfated mucopolysac-
charides (Table 2; Fig. 8). The peripheral areas
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of these cells gave positive color reactions for
calcium, phospholipids (Fig. 6), and alkaline
phosphatase activity (Table 2).
Sacciform Granulated Cells
These unicellular glands (Table 1; Fig. 1)
attained voluminous dimensions, often extend-
ing from the stratum germinativum and opening
to the surface by narrow pores (Figs. 4 and 6).
Secretory contents of these cells showed shrink-
age in most of the fixatives used and were
granular when observed in tissues fixed in
Regaud's and Helly's fluid (Fig. 4). In Bouin's
fluid and 10% neutral formalin the contents
appeared more or less homogeneous and partly
eosinophilic and partly basophilic in haematoxy-
linleosin preparations (Fig. 1). The granular
contents were acidophilic and orthochromatic,
stained bluish black in iron haematoxylin
preparations, and gave strong reaction for basic
proteins and calcium (Table 2). The thin peri-
pheral areas of these cells gave positive color
reactions for calcium and phospholipids (Fig.
6), and showed moderate alkaline phosphatase
activity (Table 2).
Outermost Layer
This consisted of a single layer of polygonal
839
or roughly triangular cells (Figs. 1 and 3), each
having a flat outer cell boundary. Orifices of
slime glands from the middle layer were discern-
ible in this layer. Cells showed an accumulation
of minute sudanophilic granules (Fig. 5). The
free cell margins stained comparatively dark,
gave a strong positive reaction for phospholipids
(Fig. 6) and succinic dehydrogenase, and showed
moderate alkaline phosphatase activity (Fig. 7).
The same areas also gave moderate color reac-
tions for calcium and sulfated acid mucopoly-
saccharide (Table 1). Between these polygonal
cells some small mitochondria-rich gland cells,
the chloride cells (Table l), opened to the sur-
face by narrow pores. These cells have been
described separately by Banerjee and Mittal
(1974).
The epidermis of Channa striata was non-
keratinized and did not give positive reactions
with the DDD technique for cysteine-bound
sulfhydryl groups and Papanicolou's stain for
keratin. Pear-shaped taste buds lying directly
on the basement membrane were also present.
Discussion
The following features of the stratum ger-
minativum of C. striata are noteworthy. Moder-
ately high levels of metabolic activity are sug-
gested by dense populations of mitochondria.
A strong positive alkaline phosphatase test is
probably indicative of active cell division
(Bevelander and Johnson 1945; Symons 1955;
Mori et al. 1960). Moderate levels of succinic
dehydrogenase probably indicate comparatively
low rates of cell division. Because an outer
keratin layer is not formed in this species, the
rate of cell replacement may be slower than in
species where a keratinized layer is continuously
sloughed off (Mittal and Banerjee 1974~).
A well-defined lymphatic plexus between the
cells of the basal layer of the epidermis is
present in C. striata. Mittal and Munshi (1971)
and Mittal and Banerjee (1974b) also reported
the presence of lymphocytes within well-defined
lymphatic spaces in the epidermis of various
fishes. Photomicrographic preparations of the
epidermis of Cottus pollux, Myoxocephalus sp.
(Sato 1967), and Carassius carassius (Yamada
1968; Henrikson and Matoltsy 1968a) clearly
showed the presence of such structures between
the cells of the stratum germinativum, although
these authors made no reference to them in their
descriptions. Percy (1970) described lymphoid
 CAN. 1. ZOOL. VOL. 53, 1975

TABLE 3
Names proposed by various authors for the sac-like cells having
acidophilic granular contents

Author Nomenclature
Studnicka (1906) Sackforrnige serose Driisen
Rauther (1907) Kornerd~sen
Hase (1911) Offene Kolben
Bhatti (1938) Sac cells
Bertin (1958) Sacciform cells
Sato (1967) Eosinophilic vesicles
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Henrikson and Matoltsy (19686) Granular cells

Mittal and Munshi (1971) Sacciform glands

cells, mainly distributed in the lower layer of priate since the cytoplasmic contents of mito-
epidermis of Carassius auratus. However, he chondria-rich chloride cells found in fish skin
could not establish the presence of lymph spaces are also granular (Banerjee and Mittal 1974;
between the basal cells. Mittal and Munshi Mittal and Banerjee, unpublished data) and the
(1974) reported the enlargement of lymphatic mucous cells in C. striata are also voluminous
spaces which became gorged with lymphocytes and sac-like in outline.
during wound-healing experiments in Rita rita The contents of sacciform granulated cells in
(Siluriformes, Bagridae). C. striata are acidophilic, siderophilic, contain
The epidermis of C. striata is mainly com- basic proteins, and do not give positive reac-
posed of three types of gland cells: the chloride tions for mucopolysaccharides and lipids (Table
cells (Banerjee and Mittal 1974), the mucous 2). Mittal and Banerjee (unpublished data) made
cells, and the sacciform granulated cells. Islam similar observations in the skin of Tetraodon
(1951) reported the complete absence of mucous fluviatilis (Tetraodontiformes, Tetraodontidae).
For personal use only.

glands in the epidermis of another species of the These cells in the epidermis of M. pancalus and
genus Channa (Ophicephalus (Channa) gachua) A. cuchia also show the absence of mucopoly-
and pointed out that the sac cells are the only saccharides (Mittal and Munshi 1971) and in
glandular elements present. His conclusions Blepsias cirrhosus stain more easily with acid
were not based on cytochemical analyses. dyes than basic (Sato 1967). Further investiga-
According to Van Oosten (1957), fishes having tions are needed to fully elucidate their cyto-
scales are provided with few mucous glands. chemical nature.
Mittal and Munshi (1971) described large Mittal and Banerjee (1974~)pointed out that
numbers of mucous cells in Mastacembelus there is an inverse relationship between the
pancalus (Perciformes, Mastacembelidae) and degree of keratinization and the abundance and
Amphipnous cuchia (Synbranchiformes, Am- types of various slime-secreting glands. The
phipnoidae). Both have thin and rudimentary large number of mucous glands and voluminous
scales, with those of A . cuchia imbedded deep sacciform granular cells in the unkeratinized
in the dermis. The present investigation also epidermis of C . striata support this hypothesis.
revealed the presence of many mucous glands in In addition to the various unicellular glands,
the skin of C. striata along with well-developed the epidermis of C. striata is mainly composed
scales (Mittal and Banerjee 1975). Mittal and of numerous polygonal cells. Henrikson and
Munshi (l970), on'the other hand, reported very Matoltsy (1968a), Kitzan and Sweeny (1968),
few mucous glands in a scaleless siluroid fish, and Yamada (1968) demonstrated the presence
Bagarius bagarius (Siluriformes, Sisoridae). Thus, of bundles of long filaments in the cytoplasm of
Van Oosten's (1957) hypothesis is not tenable. similar cells in the epidermis of various fishes and
A new term, sacciform granulated cells, is labelled them 'filament containing cells.' The
proposed for the cells, which are invariably sac- polygonal cells in the outermost layer of the
like in outline having coarse or finely granular epidermis of C. striata showed comparatively
contents. Names proposed by various authors higher succinic dehydrogenase activity than the
for these (Table 3) do not seem to be appro- underlying cells in the epidermis, indicating their
 MITTAL AND BANERJEE: SKIN OF CHANNA STRIATA. I. EPIDERMIS

TABLE 4
Thickness of the epidermis in various fish and amphibians

Fish or amphibian Reference Av. thickness of the e~idermis.um

Mastacernbelus pancalus Mittal and Munshi

(1971)
Amphipnous cuchia 119.0
Anguilla anguilla Jakubowski(l960a) 263.3
Misgurunus fossilis Jakubowski (1 958) 338.7
Channa striata Present authors 32.0 (general surface of the scale)
18.0 (posterior free margins of the scale)
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6 . 0 (below the scale)

Bombina bombina Czopek (1955) 22.8
vide Jakubowski
(19606)
Triturus cristatus
Hyla arborea
Leiopelma hochstetteri
Xenopus laevis
Rana temporaria
Bufo bufo
Pelobates fuscus
Bombina uariegata

metabolically active state. No succinic dehydro- The presence of lipids (Table 2) in the poly-
genase activity was observed in the most super- gonal cells in the outermost epidermal layer of
For personal use only.

ficial layer of the epidermis of B. bagarius (Mittal
and Banerjee 1974a), which is a dead keratinized
layer.
The present investigations show sulfated acid
mucopolysaccharides in the polygonal cells of
the outermost layer of epidermis. Mittal and
Banerjee (1974a, 1974b) made similar observa-
tions in the epidermis of Notopterus notopterus
(Osteoglossiformes, Notopteridae) and B. baga-
rius. Kitzan and Sweeny (1968) reported the
presence of electron-dense PAS-positive mucous
granules in the outermost epidermal layer of
Protopterus annectens. Yamada (1968) and
Whitear (1970) also reported electron-dense
vesicles in the cells of the outer layers of the
epidermis of several species of fishes. The
presence of mucus in the polygonal filament-
containing cells may be an adaptation for the
aquatic mode of life, since mucus has also been
reported in the epidermal cells of amphibians
(Parakkal and Matoltsy 1964; Farquhar and
Palade 1965) and a turtle (Matoltsy and Huszar
1972). Such granules have not been observed in
epidermal cells of terrestrial Squamata (Bryant
et al. 1967), mammals, or birds (Matoltsy and
Huszar 1972).
C. striata is very significant. Mittal and Banerjee
(1874a) aEso reported phospholipids in the most
superficial, cornified Iaycr of the epidermis of
8, hagarius and correlated their presence with
the slowing down of water movement through
the skin in accordance with Berenson and Burch
(1951), Blank (1952), Blank et al. (1967), Onken
and Moyer (1963), Blank and Scheuplein (1964),
and Matoltsy et al. (1968), who pointed out that
bound phospholipids may play an important
role in retarding the rate of water exchange
through the skin.
Slime on the skin of C . striata is mainly com-
posed of mucus secreted from the mucous
glands and surface polygonal cells, along with
basic proteins from the sacciform granulated
cells and lipids from the surface polygonal cells.
The phospholipid cantent of the slime may link
the neutral lipids to the mucoid and protein
components (Lewis 1970) to form a thick vis-
cous coat. According to Lewis (1970), a shift
towards greater polarity of the mucous lipids
appears to be an adaptation to aquatic conditions
and may protect the skin from bacterial and
fungal attacks, as with surface lipids of human
skin, described by Rothman (1954). Letterer
 842 CAN. J . ZOOL. VOL.
(1959) and Rogers (1961) have shown that
mucus can bind large amounts of water. A thick
coating of slime on C, striata may facilitate
respiration by keeping the skin moist and may
also protect it from desiccation as ponds dry up.
Machin (1965) reported that the freshly secreted
mucus in snails lessens water loss from the skin
surface by evaporation and concluded that con-
tinuous production of fresh mucus was essential
for preventing otherwise unprotected epithelial
cells from drying out. The presence of lipids in
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the slimy secretions of C. striata may play a role
in retarding the rate of water loss by evaporation
in dry conditions.
The thick coat of slime of C. striata may also
be correlated with its peculiar burrowing habits
by reducing surface drag during burrowing and
protecting the skin from mechanical injury.
Mittal and Munshi (1971) reported a copious
amount of slime secretions on the skin of A .
cuchia and M. pancalus and correlated this with
their burrowing modes of life. Slimy skin secre-
tions may also assist in swimming by reducing
drag (Rosen and Cornford 1971).
Mittal and Munshi (1971) suggested the
possible importance of cutaneous respiration in
For personal use only.
M. pancalus and A. cuchia, for which the epi-
dermis is thin (Table 4) and the skin richly
supplied with blood capillaries. Krogh (1904)
and Jeuken (1957) have reported that fish such
as eel and pond-loach are able to meet nearly
all of their oxygen demands through their skin.
Both eel (Anguilla anguilla) (Anguilliformes,
Anguillidae) and pond-loach (Misgurunus fos-
silis) (Cypriniformes, Cobitidae) have a very
thick epidermis (Table 4). In C. striata the skin
is richly supplied with blood capillaries (Mittal
and Banerjee 1975) and the epidermis is even
thinner than the epidermis of some of the
amphibians that also respire through the skin
(Table 4), suggesting that the skin is an import-
ant organ of respiration.
Aicknowledgments
We are grateful to Prof. J. S. Datta Munshi,
Head of the Postgraduate Department of
Zoology, Bhagalpur University, Bhagalpur,
India, for encouragement and his keen interest
in the work. We also thank Prof. J. P. Thapliyal,
Head of Zoology Department, Banaras Hindu
University, for providing necessary laboratory
facilities.
53, 1975
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