Biologia 68/3: 546—558, 2013
Section Zoology
DOI: 10.2478/s11756-013-0181-7
Comparative histological, histochemical and ultrastructural studies
of the nephron of selected snakes from the Egyptian area
Ahmed A. Allam1,2 & Rasha E. Abo-Eleneen2
1
King Saud University, College of Science, Zoology Department, P.O. Box 2455, Riyadh 11451, Saudi Arabia;
e-mail: [email protected]
2
Beni-Suef University, Faculty of Science, Zoology Department, Beni-Suef 65211, Egypt
Abstract: The present study was aimed to compare and contrast the histochemical, histological and ultrastructural variations (microanatomical differences) in the nephrons of selected snake species, Eryx jaculus (Boidae), Psammophis sibilans
(Colubridae), Naja haje (Elapidae) and Echis pyramidum (Viperidae) from Egypt. The structural studies were carried out
by conventional light and electron microscopy. The nephron, the renal unit of snakes, consists of renal corpuscle, proximal
tubule, intermediate segment, distal tubule and collecting tubule. The renal corpuscles have large capillaries with clear and
dark fenestrated endothelial cells. The proximal tubule showed long microvilli, cytoplasmic vacuoles, developed endoplasmic
reticulum and abundant mitochondria. The intermediate segment was lined by ciliated cells. The lining cells of the distal
tubules showed few microvilli, abundant dense mitochondria and clear vesicles of mucous appeared in the terminal portion. The collecting tubules consisted of mucous cells. In summary, the ultra-structure studies of nephrons revealed several
interspecies similarities and also some intra-species differences in species of snakes.
Key words: Eryx jaculus; Psammophis sibilans; Naja haje; Echis pyramidum; kidney
Introduction
The kidney is the main organ of excretion in snakes.
The kidney regulates the fluid balance of the body and
the electrolyte in the urine (Gambarian 1994). In recent
years the reptilian kidney has been increasingly studied due its pivotal role in the phylogenetical scale of
this group of vertebrates (Anderson 1960; Roberts &
Schmidt-Nielsen 1966; Davis & Schmidt-Nielsen 1967;
Schmidt-Nielsen & Davis 1968; Davis et al. 1976; Gabri
1983a, b; Gabri & Butler 1984; Soares & Fava de
Moraes 1984; Solomon 1985). The previous reports described the reptilian nephron as composed of renal corpuscle, proximal, intermediate and distal tubules and
collecting duct (Bishop 1959; Kahlil et al. 1974a, b;
Gabri 1983a). Marked variations have been found in
the ultra structure of the tubular cells which has been
attributed to the enormous variety of species and habitats of the animals (Gabri 1983a). The first histological
description of a squamate nephron was made on the
European natricine snake Natrix natrix (L., 1758) by
Gampert (1866).
Reptile kidneys have some similarities and also
major differences with mammalian kidneys. Important anatomical similarities in the tubular system include the renal Bowman’s capsule, proximal convoluted tubule, distal tubule, collecting duct and ureter.
Reptiles lack the loop of the henle and instead have
a short intermediate segment. A reptile kidney contains a few thousand nephrons whereas a human kidc 2013 Institute of Zoology, Slovak Academy of Sciences
ney has about one million nephrons (Peek & McMillian
1979a).
The anatomy of the renal and urinary system
of both birds and reptiles is markedly different from
that of mammals (Canny 1998). Whatever type of kidney particular vertebrate may have, all kidneys consist
of morphologic and functional units called nephrons.
Structural modifications of nephrons have enabled vertebrates to solve the problems of their environmental conditions whether in fresh or salt water or on
land (Gambarian 1978). Carbohydrate content in the
nephron plays a significant role in the renal physiology
of mammals (Schimming & Vicentini 2000).
The reptilian kidney has been studied by classical histological and physiological techniques (Gampert
1866; Regaud & Policard 1903; Huber 1906; Bishop
1959). More recently, several ultrastructural studies
on the renal corpuscles have been published (Fernández et al. 1978; Gabri & Butler 1984; Solomon 1985).
Reptiles have simple glomeruli whereas others species
lack glomeruli. The glomerular ultrafiltration of reptiles does not show the complex capillary network as
seen in the mammalian glomeruli (Beyenbach 2004).
Many adaptations of reptiles to their environmental
conditions are the production of hypertonic urine and
the ability to secrete uric acid which is the major end
metabolic product of nitrogenous compounds. These
adaptations indicate that nephrons play an important
role in coping with the extreme conditions of water deprivation (Dantzler 2005).
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Figs 1A–D. Light micrographs (H&E, ×100) of the kidney illustrating proximal tubule (PT), intermediate segment (arrow head),
glomeruli (G), distal tubule (DT) and collecting tubule (CT, arrow). A: E. jaculus; B: P. sibilans; C: N. haje; D: E. pyramidum.
Kidneys play an essential role in fluid ion balance. The mechanisms of renal handling of water vary
depending on structural organization of kidneys and
the environment. The excretion of excess water is by
forming dilute urine whereas terrestrial tetrapods require water conservation by the kidney for survival
(Nishimura & Fan 2003; Dantzler 2003).
The present study was aimed to investigate the
histochemical, histological and ultra structural variations of nephron in Eryx jaculus (L., 1758) (Boidae),
Psammophis sibilans Boie, 1827 (Colubridae), Naja
haje (L., 1758) (Elapidae) and Echis pyramidum (Geoffroy Saint-Hilaire, 1827) (Viperidae) found in the
Nile valley, Delta, Faiyum and desert, respectively. An
attempt was made to correlate the nephrons microscopic structure and its chemical contents with the
body fluid, water regulation and renal physiology of
these snakes.
Material and methods
Snake species
10 adult specimens of each species were used. The species
were from different families. The first snake used was the
javelin sand boa E. jaculus (Boidae) found in sandy areas
near cultivated land and collected from Nile Delta, lower valley and northern Sinai. The second species was the striped
sand snake (Abu essuyur snake) P. sibilans (Colubridae) a
snake of riverine found in agricultural fields usually in gardens and cultivated areas. It appears to climb trees occasionally and its distribution includes the Nile Valley and Delta.
The third is the Egyptian cobra snake N. haje (Elapidae)
which inhabits in agricultural fields of the Nile Delta. It is
most frequently encountered on densely vegetated banks of
rivers or irrigation canals and is distributed in the Nile Valley, Delta and Faiyum regions. The fourth is Egyptian sawscaled viper E. pyramidum (Viperidae) is commonly called
the Haiya ghariba snake that inhabits in sandy desert in
the northern oases of the western desert including western
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A.A. Allam & R.E. Abo-Eleneen
Figs 1E–H. Higher magnification of the kidney light micrographs (H&E, ×400) show the renal corpuscle formed of parietal epithelium
(PE) and visceral epithelium consisting of podocytes (P) and capillaries (CP) lined by endothelial cells (E). E: E. jaculus; F: P. sibilans;
G: N. haje; H: E. pyramidum.
area of Faiyum and Cairo. The distribution of the snakes
examined in this study has been earlier described by Saleh
(1997).
Chemicals
The chemicals were purchased from Sigma chemical Company (St Louis, MO, USA). All other chemicals used were
of analytical grade.
Histological and histochemical studies
Snake kidney segments (5 mm in size) were fixed in 10%
buffered formalin (pH 7.4) for 24 h. The tissue was dehydrated in ethyl alcohol followed by two changes of xylene.
The tissue was impregnated in paraffin wax and then embedded in paraffin wax. Sections (4–5 µm) were cut, de-waxed,
hydrated and stained in Mayer’s haemalum solution for 3
min. The sections were stained in eosin for 1 min, washed
in tap water and dehydrated in ethanol as described above.
Haematoxylin and Eosin stained sections were prepared according to the method of Mallory (1988). The sections were
stained by periodic acid / Schiff’s (PAS) for polysaccharides investigations according to McManus (1946). To differentiate neutral mucopolysaccharides from the acid mucopolysaccharides, PAS/AB method was employed according to Mowry (1956). The bromophenol blue was used for
proteins (Mazia et al. 1953). The sections were examined
and photographed using Leitz microscope.
Transmission electron microscope (TEM) studies
The kidneys were cut into small pieces measuring 1 mm3 and
immediately fixed in fresh 3% glutraldehyde-formaldehyde
at 4 ◦C for 18–24 h (pH 7.4) and then post-fixed in isotonic
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Figs 2A–D. Light micrograph of the kidney (PAS, ×400). A: Strong amount of PAS positive material in glomerular tuft (G), distal tubule
(arrow) and collecting tubule (CT) in E. jaculus. B: Neutral mucosubstances in the glomerulus (G) in P. sibilans. C: Accumulation
of PAS positive material in the glomerulus (G), proximal tubule (PT) and collecting tubule (CT) in N. haje. D: Large amounts of
positive material in the glomerulus (G) and moderate amount in the proximal tubule (arrow head) in E. pyramidum.
1% osmium tetraoxide for one hour at 4 ◦C. Serial dehydration in alcohol was carried out in the following order: 30
min in 50% alcohol, 2 times in 70% alcohol each for 15 min,
in 80% alcohol for 15 min, in 90% alcohol for 15 min, then
2 times in absolute alcohol each for 30 min. The specimens
were then passed through propylene oxide solutions 2 times
each for 10 min.
The specimens were embedded in spur resin started by
passing the specimens in propylene oxide then in propylene
oxide-resin mixture at the ratio of 1:1 for 1 hour then in
propylene oxide-resin mixture at the ratio of 1:3 overnight.
The samples were left in fresh pure resin at room temperature overnight. In the next day, the specimens were transferred to capsules containing fresh resin and placed in an
oven at 60 ◦C for one day so that polymerization would
harden the blocks. Semithin sections were cut from these
blocks at 1 µm thickness by ultracut Reichert-Jung ultramicrotone with the aid of glass knives, stained with toluidine
blue and examined by light microscope. To detect the area
of interest, ultrathin sections were then prepared using the
ultramicrotome glass knives, stained with uranylacetate and
lead citrate and examined with a Joel CX 100 transmission
electron microscope operated at an accelerating voltage of
60 KV.
Results
Histological and histochemical studies
The nephron of E. jaculus, P. sibilans, N. haje and
E. pyramidum consisted of renal corpuscle, proximal
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Figs 2E–H. Light micrograph of the kidney (PAS-Alcian, ×400). E: Both acid and neutral mucosubstances in the intermediate segment
(IS) and collecting tubule (CT) in E. jaculus. F: Strong amounts of PAS and Alcian blue in the collecting tubule (CT) in P. sibilans.
G: Strong amounts of PAS and Alcian blue stained material (mixed polysaccharides) in the collecting tubule (CT) in N. haje. H:
Accumulation of mixture of acid and neutral polysacchaides (magenta colour) in the intermediate segment (IS) and collecting tubule
(CT) in E. pyramidum.
tubule, intermediate segment, distal and collecting
tubules (Figs 1A–H). The renal corpuscle of the present
species is varied in its size. In P. sibilans and N. haje,
glomerulus is large and urinary space is wider than in
E. jaculus and E. pyramidum. The renal corpuscle in
the species appears as dense round tuft of capillaries
and formed of parietal epithelium and visceral epithe-
lium consisting of podocytes and capillaries lined by
endothelial cells (Figs 1E–H).
In the four snake species, the proximal tubule is
lined by simple columnar epithelium. This epithelium
has abundant clear vesicles and basophilic granules in
the apical cytoplasm. The cell apex exposed to the lumen of the tubule exhibits a brush border. The upper
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Figs 2I–L. Light micrograph of the kidney (Bromophenol blue, ×400). I: Moderate reaction for total protein in E. jaculus. J: High
levels of protein containing materials in the glomerulus (G), the intermediate segment (IS) and the proximal tubule (PT) in P. sibilans.
K: Weak reaction for total protein in N. haje. L: Moderate reaction for total protein in E. pyramidum.
portion of intermediate tubules is lined by columnar
cells larger than those observed in the proximal tubule
while the lower portion is lined by cubodial cells. All
cells of intermediate tubules have a brush border in
their apical poles. The distal tubule is a short segment
which shows a wide lumen and is lined by cuboidal
epithelium. No brush border is observed in the distal
tubule epithelium. The collecting tubule is composed
of large columnar cells with basally located nuclei. The
apical pole of the cells is very irregular showing small
processes towards the lumen (Figs 1A–D). The large
diameter of the collecting tubule in N. haje (Fig. 1C) is
noted.
Histochemically, the renal corpuscle of the four
species shows a similar positive PAS reaction in the
basal lamina and the visceral epithelia (Figs 2A–D).
The collecting tubule of E. jaculus (Fig. 2A) and N.
haje (Fig. 2C) are strongly PAS-positive while the collecting tubule of P. sibilans (Fig 2B) and E. pyramidum
(Fig. 2D) are moderately PAS-positive.
The application of PAS-Alcian blue revealed a
strong magenta color indicating the presence of neutral
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Figs 3A–D. Glomerulus electron micrograph. A: Podacytes (P), urinary space (US), rounded nucleus (N), mitochondria (M), mesangial
cells (MS) and lysosomes (L) in E. jaculus (Scale 10 µm). B: Podacytes (P) resting on the basal lamina (arrow). The podocyte give rise
to primary processes (PP) which in turn gives numerous secondary foot processes (FS) that rest on the basal lamina, irregular nucleus
(N), mitochondria (M), mesangial cells (MS) and lysosomes (L) in P. sibilans (Scale 2 µm). C: Podacytes (P) give rise to primary
processes (PP) which give a rise to numerous secondary foot processes (FS) resting on the basal lamina, urinary space (US), irregular
nucleus (N), mitochondria (M), mesangial cells (MS) and lysosomes (L) in N. haje (Scale 2 µm). D: Podacytes (P) resting on the
basal lamina (arrow). The podocyte give rise to primary processes (PP) which in turn gives numerous secondary foot processes (FS),
urinary space (US), irregular nucleus (N), mitochondria (M), mesangial cells (MS) and lysosomes (L) E. pyramidum (Scale 2 µm).
and acidic mucin in the intermediate segment and in the
collecting tubules of the four species (Figs 2E–H). Bromophenol blue staining was used to reveal the protein
distribution in the renal sections of the present snakes.
In P. sibilans, kidney revealed intense reaction for total proteins as indicated by the resulting intense blue
color (Fig. 2J). The kidney of E. jaculus (Fig. 2I) and
E. pyramidum (Fig. 2L) showed a moderate amount of
protein. In N. haje (Fig. 2K), the kidney showed weak
protein stain.
Ultrastructure studies
The renal corpuscle of the four species was small
and consisted of glomerulus (capillary endothelium,
glomerular basement membrane and mesangium) and
Bowman’s capsule. The glomerulus extended from the
podacyte cell body and the finest branches of one cell.
The pedicles were interdigitated with those of an adjacent cell. Capillary endothelium was composed of endothelial cells with a central nucleus protruding into the
capillary lumen (Figs 3A–D). The cytoplasm contained
the typical organelles and some small rod-shaped bodies. In E. jaculus (Fig. 3A), the capillary endothelium
usually presented a reticulated appearance although
typical fenestrated region was found in P. sibilans, N.
haje and E. pyramidum. The mesangium or central intercapillary region of the four species were embedded
in a collagenous matrix and composed of a fine filamentous material similar to and continuous with the
glomerular basement membrane. The podocytes of P.
sibilans, N. haje and E. pyramidum showed irregular
nuclei with peripheral aggregations of heterochromatin
(Figs 3B–D) while nucleus of podocytes of E. jaculus
was round in shape and heterochromatin appeared fragmented (Fig. 3A).
In all the species, the proximal tubule consisted
of large, clear and dark columnar cells with a welldeveloped brush border (Figs 4A–D). The cell membrane is without basal infoldings. The cell junctions
and some narrow intercellular spaces are also found.
The luminal surface of the proximal tubule of E. jaculus (Fig. 4A) has long microvilli. The apical aspect
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Figs 4A–D. Proximal tubule electron micrograph. A: The cells have tightly packed microvilli (MV), few vacuole (V), lysosomes (L) and
mitochondria (M) in E. jaculus (Scale 2 µm). B: Microvilli (MV), numerous mitochondria (M), endoplasmic reticulum (ER), vacuole
(V), nucleus (N) and lysosomes (L) in P. sibilans (Scale 2 µm). C: Microvilli (MV), mitochondria (M), vacuole (V), rounded nucleus
(N) and lysosomes (L) in N. haje (Scale 10 µm). D: Microvilli (MV), mitochondria (M), vacuole (V), nucleus (N) and lysosomes (L)
in E. pyramidum (Scale 10 µm).
of the cytoplasm showed numerous lysosomes and vacuoles in E. jaculus and P. sibilans (Figs 4A, B) but in
N. haje and E. pyramidum (Figs 4C, D) the apical aspect of the cytoplasm was filled with circular profiles of
endoplasmic reticulum, few vacuoles and lysosomes. In
all species, each cell had a large, oval, centrally located
nucleus. Mitochondria with an electrodense matrix and
few cristae were scattered throughout the cytoplasm.
In all species, intermediate segment had a transitional region between the proximal tubule and distal
tubule. Three regions of clear and dark ciliated cells
were found. The upper and lower transitional regions of
the intermediate segment had cells with similar features
to those of the proximal and distal tubules, respectively.
The ciliated cells had an irregular or indented nucleus
and few organelles (Figs 5A–D).
The apical pole of the lining cells of the distal
tubule showed few microvilli. In E. jaculus and E. pyramidum (Figs 6A, D), the mitochondria were small,
dense and concentrated at the apical part. Also, there
were few mitochondria scattered in the cytoplasm while
in P. sibilans and N. haje, the cytoplasm showed abundant dense mitochondria and occasionally some lysosomes (Figs 6B, C).
The collecting tubules of the four species were consisted of mucous cells. These cells showed a basal nuclei and interdigitations between the lateral margins of
adjacent cells (Figs 7A–D). The cytoplasm was filled
by mucous granules and few mitochondria. In N. haje
(Fig. 7C), the mucous cells were more abundant than in
other species. Mucous cells were seen in E. pyramidum
(Fig. 7D) having a clear granular content while in the
others species (Figs 7A–C) these cells contained dense
granular.
Discussion
The results of this study demonstrate that the nephrons
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Figs 5A–D. Electron micrograph of the intermediate segment. A: Ciliated cells (C) in E. jaculus (Scale 2 µm). B: Mitochondria (M),
lipid droplet (LD) and cilia (C) in P. sibilans (Scale 2 µm). C: Cilia (C), mitochondria (M), endoplasmic reticulum (ER) and nucleus
(N) in N. haje (Scale 2 µm). D: Cilia (C), vacuoles (V) and nucleus (N) in E. pyramidum (Scale 2 µm).
of E. jaculus, P. sibilans, N. haje and E. pyramidum
have simple glomeruli, longer distal tubules, wide inner
medullary insulation and high medullary cortical ratio.
These structural modifications might help in maximizing re-absorption of the glomerular filtrate to prevent
water loss in the snake’s dry environment. Collecting
tubules are longer in animals adapted to a limited water supply as compared to animals which have unlimited
access to water (Gambarian 1978). These snakes obtain
water from its food plus that produced in its body by
cellular respiration and burning of fat. Uric acid excretion allows hyperosmolarity of urine which requires
tubular re-absorption for osmoregulation and enhancing concentration ability (Dantzler & Braun 1980).
The renal corpuscle varied in size among snake
taxa. In P. sibilans and N. haje, glomerulus is larger
and urinary space is wider than in E. jaculus and E.
pyramidum. The size of renal corpuscles was directly
correlated to filtration rate (Davis & Schnerman 1971).
Davis et al. (1974) stated that the filtration of the juxamedullary nephron is significantly higher than the superficial nephrons.
The fine structure of the renal corpuscle of the
present species does not differ greatly from that described for the lizard Podarcis taurica (Pallas, 1814)
(Gabri 1983a). The renal corpuscles are composed
of visceral and parietal layers. The epithelial cell
(podocytes) of the visceral layer bear trabeculae connected to pedicles. The glomerular capsule with its attenuated epithelium encloses a tuft of capillaries. These
findings are in agreement with Fox (1977) who recorded
that the few and small renal corpuscles of lacertilia are
composed of a tuft of three or four capillaries (glomerulus), Bowman’s capsule and mesangium.
In all these species, the glomeruli contain neutral
mucosubstances. The neutral mucosubstances are associated with the glomerular basal membranes to provide structural support and play a major role in surface
transformation process of the glomeruli (Viotto et al.
1988; Bashir 2006).
The structural modification and carbohydrate content of both the glomeruli and renal tubules of the current species might indicate a role in the nitrogenous
waste excretion and the production of hypertonic urine.
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Figs 6A–D. Distal tubule electron micrograph. A: The cells display nuclei located in a basal position, apical microvilli (MV), basal
mitochondria (M) and thick basal membrane (BM) in E. jaculus (Scale 2 µm). B: Short microvilli (MV), nucleus (N) and basal
membrane (BM) in P. sibilans (Scale 2 µm). C: Microvilli (MV), nucleus (N) and basal membrane (BM) in N. haje (Scale 2 µm). D:
Short microvilli (MV), nucleus (N) and basal membrane (BM) in E. pyramidum (Scale 2 µm).
These might be considered as a mechanism to facilitate excretion, conserve water and maintain body fluid
balance especially in the extreme conditions of water
deprivation in the hot habitat of these snakes.
Podocytes of E. jaculus, P. sibilans, N. haje and
E. pyramidum are large, have irregular pedicels and
few fenestrae and occasionally having a diaphragm.
These characteristics limit the glomerular filtration
rate. These podocytes did not contain the bundles
of microfilaments as described by Peek & McMillan
(1979b). The mesangial cells of these species are numerous. Similar observations were recorded in other reptilian species (Davis et al. 1976; Fernández et al. 1978;
Peek & McMillan 1979b; Gabri & Butler 1984; Soares
& Fava de Moraes 1984; Galaly 2008).
The epithelial cells of the proximal tubule showed a
well developed brush border. Marked protrusions of the
apical cytoplasm were observed in some cells (Anderson 1960; Davis & Schmidt-Nielsen 1967; Gabri 1983a).
These protrusions have been related to the secretion
of uric acid by the cells and may be important in the
exchange of fluids (Gabri 1983a). No segmentation of
the proximal tubule of the four species has been found
as in the case of other reptiles (Gabri 1983a; Soares
& Fava-De Moraes 1984; Solomon 1985). In the basal
portion, marked intercellular spaces were observed similar to those described in other reptiles (Anderson 1960;
Roberts & Schmidt-Nielsen 1966; Davis & SchmidtNielsen 1967; Schmidt-Nielsen & Davis 1968; Davis et
al. 1976; Solomon 1985).
In E. jaculus, P. sibilans, N. haje and E. pyramidum, the brush border of the proximal tubules had
long and densely packed microvilli similar to that
found in Tiliqua scincoides Smith, 1937 (SchmidtNielsen & Davis 1968) and Crocodylus acutus Cuvier, 1807 (Davis & Schmidt-Nielsen 1967). There was
no basal labyrinth as in frogs (Meseguer et al. 1978;
Taugner et al. 1982). The mitochondria were scattered throughout the cytoplasm as in desert and tropical lizards (Roberts & Schmidt-Nielsen 1966; Soares
& Fava-De Moraes 1984). The adaptations of cells
engaged in solute-linked water transport. The abundant presence of mitochondria was in water and
ion-transporting cells where mitochondria had a few
cristae and a dense matrix containing dense granules.
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Figs 7A–D. Collecting tubule electron micrograph. A: Mucous granules (MU), nucleus (N) with dense scattered patches of heterochromatin and intercellular canaliculus (IC) in E. jaculus (Scale 2 µm). B: Mucous granules (MU), mitochondria (M), lipid droplets (arrow
head) and nucleus (N) in P. sibilans (Scale 10 µm). C: Mucous granules (MU) fills the apical region of the cells and intercellular
canaliculus (IC) in N. haje (Scale 10 µm). D: Mucous goblet with clear granular content (MU) and nucleus (N) with dense scattered
patches of heterochromatin in E. pyramidum (Scale 10 µm).
The morphology of the intermediate segment of the
current species is similar to Henle’s loop of mammals
(Soares & Fava de Moraes 1984) and intermediate segments of other reptiles (Davis et al. 1976; Fernández
et al. 1978). Ciliated cells were frequently observed in
this segment of the nephron of lower vertebrates. The
role of ciliated cells might be related to the low blood
pressure of these animals which produces a low filtration pressure in the kidney. Cilia are known to have a
propulsive action of the ultrafiltrate (Davis et al. 1976).
In higher vertebrates, where the blood pressure increases, no cilia are usually found in the nephron (Marshall 1934; Giebrish 1973; Soares & Fava de Moares
1984).
The small microvilli observed in the distal tubule
in all four species indicated that the absorptive function of this segment is very low (Fernandez et al. 1978).
The cytoplasmic features and the apical surface of the
distal tubular cells resembled those seen in other reptiles (Davis & Schmidt-Nielsen 1967; Davis et al. 1976).
The numerous small apical vesicles are thought to be
involved in the re-absorption processes (Malnic et al.
1966a, b; Giebisch 1971; Danzler & Holmes 1974).
The collecting tubule of E. jaculus, P. sibilans, N.
haje and E. pyramidum, is formed by mucous cells.
In N. haje mucous cells are as abundant as in some
lizards and snakes (Bishop 1959; Gabe 1959; Anderson 1960; Fernández et al. 1978; Gabri 1983b; Soares
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& Fava de Moares 1984) and contain both sialo-and
sulpho-mucins. In some turtles, the mucous cells are located in the distal portion of the intermediate segment
and not in the collecting duct (Solomon 1985).
The mucins in the nephron of reptiles have been
implicated in the excretion of non-soluble urates. The
urate crystals are surrounded by mucus which acts as a
lubricating agent and avoids any injury to the epithelium (Minnich 1972; Davis et al. 1976; Peek & McMillan 1979b; Gabri 1983b; Solomon 1985). In the fish
the collecting tubules have cells with mucous droplets
(Ottosen 1978; Zuasti et al. 1983). The clear and dark
cells with mucous goblets observed in all the species of
snakes. The mucous secretion could produce a luminal
layer that either limits water permeability or prevent
the precipitation of inorganic salts thus facilitating the
excretion of insoluble urates (Hickman & Trump 1969;
Gabri 1983b).
In conclusion, the results of this study showed that
the differences in snake nephron microstructure and histochemical data may be dependent on their habitat.
The observed structural similarities between P. sibilans
and N. haje may also be related to their environmental
conditions.
Acknowledgements
This project was supported by King Saud University, Deanship of Scientific Research, college of Science Research Center.
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