THE ANATOMICAL RECORD 212:33-40 (1985)
Structure of the Avian Kidney
I. MORTLD, A. BOHLE, AND J.A. CHRISTENSEN
Department of Pathology, The Gade Institute, University of Bergen, N-5016 Haukeland
Hospital, Norway (Z.M.,J.A.C.)and Institute of Pathology, University of Tubingen, 0-7400
Tubingen, Federal Republic of Germany (A.B.)
ABSTRACT
The kidneys from 6 domestic fowl were fixed in situ by perfusion
from the left ventricle. In the bird there are two types of nephrons. One reptiliantype without Henle’s loop and medullary tissue, and one mammalian-type with
Henle’s loop lying in medullary tissue. Serial sections from kidney tissue embedded
in plexiglass or in paraffin were used to study the architecture of eight reconstructed
reptilian-type nephrons from different cortical levels. All reconstructed nephrons
had four major bends, but particularly in the subcapsular nephrons additional bends
parallel to the kidney surface were found. There was no loop of Henle, but before
entering the collecting duct the distal tubule usually had a very thin-walled segment. No proximal convoluted part was found in the reptilian-type nephrons. The
length of the tubules varied between 3,000 pm and 6,000 pm. In the distal tubule a
macula densa segment was found in all nephrons of the reptilian and mammalian
type. The capillary network between the inter- and intralobular veins was composed
of increasingly larger capillaries towards the intralobular vein. Segments of the
distal tubule were indented into these capillaries and completely surrounded by
them. In the nephrons of the mammalian type the proximal tubule was found to be
convoluted as is usual for mammalian species.
The morphology of the avian kidney has been studied
with casts, light microscopy, and electron microscopy
(Edwards, 1940; Feldotto, 1929; Hodges, 1974; Johnson
et al., 1972; Johnson and Mugaas, 1970; Kurihara and
Yasuda, 1975; Ogawa and Sokabe, 1971; PakPoy and
Robertson, 1957; Siller, 1981; Siller and Hindle, 1969;
Sokabe et al., 1969; Sokabe and Ogawa, 1974; Spanner,
1925; Sperber, 1948, 1960),but so far only a few studies
have been made on avian kidney structures from the
domestic fowl fixed by perfusion (Kjaerheim, 1969;
Wideman et al., 1981).
In the literature there is general agreement on the
kidney architecture in birds. In the avian kidney there
are two different types of nephrons: a reptilian type
without Henle’s loop and medullary tissue, and a mammalian type with both Henle’s loop and a renal medulla
(Huber, 1917;Johnson et al., 1972; Johnson and Mugaas,
1970; Siller, 1971; Sperber, 1960). The reptilian-type
nephrons are found in all areas of the kidney; in particular there is a very characteristic arrangement of the
structures in the subcapsular cortex where the glomeruli lie in a semicircular array around the intralobular
vein. In the deeper cortex, the reptilian-type glomeruli
lie scattered between tubules and mammalian-type glomeruli (Dantzler and Braun, 1980; shoemaker, 1972;
Siller, 1981; Sperber, 1948, 1960). The latter are only
found in the deeper parts of the cortex. There are fewer
of them than of the reptilian type and they are always
located in the vicinity of the medullary cones (Johnson
and Mugaas, 1970; Sperber, 1960).
0 1985 ALAN R. LISS, INC.
The vascular supply of the avian kidney is double; an
arterial supply from the renal arteries that terminates
in the afferent arterioles of all glomeruli, and a venous
supply terminating in the peritubular capillaries to the
entire reptilian-type nephrons and at least the proximal
tubules of mammalian-type nephrons (Kurihara and Yasuda, 1975; Siller and Hindle, 1969; Sokabe et al., 1969;
Spanner, 1925; Sperber, 1948). The venous blood originates from the portal venous system (Akester, 1967;
Wideman et al., 1981).
The relationships between the portal venous system
and the nephrons have recently been studied by injection of ferrocyanide and gelatin in the veins of the back
limb (Wideman et al., 1981). However, the finer morphology of the reptilian-type nephrons is not fully understood despite one recent study with reconstruction of
two reptilian-type nephrons (Wideman et al., 1981).Neither are there any reliable measurements of the kidney
structures in the avian kidney.
As the quality of the histological sections has been a
problem in the past in connection with obtaining accurate information and measurements, the present study
was performed on serial sections after whole-kidney
fixation by perfusion.
MATERIALS AND METHODS
The kidneys from 6 domestic fowl (white Leghorns,
Gallus gallus u. domesticus) were used for this study.
Received August 21, 1984; accepted November 28, 1984.
I. MORILD, A. BOHLE, AND J.A. CHRISTENSEN
34
The birds had been fed on a standard diet (Vestlandske
Felleskjbp, Bergen, Norway), which contained 2 gm of
sodium per kilogram of diet, and had free access to
tapwater. They were 1.5-2 years old and weighed 1,2001,500 gm.
Fixation by Perfusion
On the day of sacrifice, the birds were anesthetized with
sodium phenemal, 100-200 m g k g (NAF Laboratories,
Oslo, Norway), injected i.v. in the alar vein. Tracheotomy was performed, and the birds were ventilated artificially. This was necessary as thoracotomy was needed
to gain access to the heart, from which the kidneys were
perfused (Kjaerheim, 1969).
The rinsing fluid was 1.0 M phosphate buffer with 1%
formaldehyde (pH 7.0). This fluid was infused for 2-3
min, and then fixation was continued with 2% glutaraldehyde and 2% formaldehyde in 0.1 M phosphate buffer
(pH 7.0) for 5-6 min. The bottles with rinsing fluid and
fixative were connected to each other and to a metal
cylinder of compressed air. The perfusion pressure was
monitored from the left ventricle with a medical transducer (SE 4-88) and amplifier (SE 4919; SE Labs EM1
Ltd., North Feltham Trading Estate, Feltham, Middlesex, England) connected to a calibrated oscilloscope
(Hewlett Packard 78303A). The perfusion pressure
ranged between 80 and 110 mm Hg (the mean arterial
pressure in the fowl being 115 mm Hg).
Histological Procedure
After perfusion, kidneys were removed, cut into slices
1-2 mm thick, and placed in additional fixative for 2-3
days. Thin slices from these blocks were embedded in
paraffin, sectioned serially (100-150 consecutive sections, 7-8 pm thick), and stained with periodic-acid-Schiff
reagent (PAS). Similarly, a n equal number of consecutive sections from small tissue blocks embedded in plexiglass were cut (1-2 pm thick) on a h i c h e r t Jung Rotocut
microtome and impregnated with silver by Movat’s
method (1961). TOseparate reptilian-type from mammalian-type nephrons, tissue for semithin sections was
taken from subcapsular and juxtamedullar regions of
renal cortex, respectively.
Fig. 1. Reconstructed reptilian-type nephron. Two-dimensional
view from “above.” Black line is positioned centrally in the tubular
lumen. Star indicates glomerulus. Arrow indicates beginning of the
collecting duct.
Reconstructions
The entire tubule of eight mammalian-type nephrons
was followed in serial sections from the glomerulus to
the collecting duct and the course of the tubule was
drawn. Four of these were selected from the subcapsular
cortex and four from the deeper cortex, about halfway
between the kidney surface and the renal medulla. For
this purpose two schematic drawings were made of each
tubule in which the tubules were seen from two angles
90” apart (from “above” and “laterally”). On the horizontal axis the distance from the interlobular to the
intralobular vein was plotted on the sheets and hence
the position of glomeruli, tubuli, collecting ducts and
arteries were drawn. On the vertical axis the number of
the sections were listed. All measurements were to scale.
In this manner two-dimensional drawings like Figure 1
and Figure 2 were made. By combining the two views
in Figure 1 and Figure 2, three-dimensional drawings
were made (Fig. 3).
Measurements
Measurements on the sections were made with a morphometric program from MTS (Medizinisch Technische
Apparate, D-7400 Tiibingen, FRG). This was used in
connection with a computer (Commodore Computer
CMB 3032, Commodore Business Machines, Santa
Clara, California) and a digitizing plate (Bit Pad One
TM, Summagraphics Corporation, Fairfield, Connecticut). The measurements were performed on the digitizing plate with a cursor that was equipped with a light
diode. The light point from the diode was projected into
the section in the microscope (Leitz Dialux 20 EB) with
a tracing device.
Thickness
The thickness of the PAS-stained sections was estimated from the spherical glomeruli. The diameters were
measured in all sections where the glomerulus was seen,
35
STRUCTURE OF THE AVIAN KIDNEY
Fig. 2. Same nephron as in Figure 1 seen from a “lateral” view
and the maximal diameter was divided by the number
of sections. These measurements were carried out on 6
glomeruli each in 2 different series. The average thickness of the sections was 6.98 pm in one series and 7.02
pm in the other. The individual results are listed in
Table 1.
The thicknesss of the semithin sections was determined with a Zeiss instrument for interference microscopy using the method of Jamine and Lebedeff with
Senarmont compensation (Hale, 1958)(Table 2).
Measurements of the diameter of proximal and distal
tubules were carried out on PAS-stained series. Fifty
cross-cut proximal and 50 cross-cut distal tubules were
measured. The sections were deliberately chosen from
all 6 animals.
Finally, the distance between the interlobular and
intralobular veins was measured in the areas with reptilian-type nephrons. As these nephrons constantly
showed the same pattern of primary foldings, the distance between the two veins could be used to calculate
the approximate minimal length of the nephron. For
this purpose we measured the distance between the inter- and intralobular vein in 180 nephrons from all 6
animals. In addition, the extent of the nephrons was
estimated to obtain an impression of the area covered
by a single nephron.
Fig. 3. Model of the reptilian-type nephron shown in Figures 1 and
2. Note folds parallel to kidney surface at the top. Star indicates
position of glomerulus. Arrowhead indicates transition from the proximal to the distal tubule. Arrow indicates beginning of the collecting
duct.
The mammalian-type nephrons were followed from
the glomerulus through the promimal labyrinth and
into, but not through, the medulla, as these nephrons
had been found to be similar to the nephrons in mammalian species (Dantzler and Braun, 1980).
RESULTS
The avian kidney is incompletely divided into three
major parts (the cranial, middle, and caudal). The structure of the kidney tissue, which is the same in all three
parts, is lobular, and each lobule is outlined by the
ramifications of the interlobular veins of the renal portal system.
This lobular subdivision of the kidney was found in
the subcapsular and middle areas of the cortex. Here all
nephrons were of the reptilian type arranged in a horse-
I. MORILD, A. BOHLE, AND J.A. CHRISTENSEN
36
TABLE 1. Average thickness of PAS-stained sections
estimated from the diameters of reptilian-type glomeruli
No. of
Avg. thickness
glomeruli of sections (fim)
X+SD Series No.
H.3 28.01.82
H.2 04.02.82
6
6.3,g.l
6.5, 5.6
6.7, 7.7
6.1,6.9
7.4, 6.6
7.5. 7.6
6
6.98 k 1.24
7.02
0.59
TABLE 2. Thickness of semithin sections measured by
interference microscopy
Measured values
Sections cut at 1pm
Sections cut at 2 pm
n
=
n
in fim
10
1.0, 1.0,1.0,1.0,
1.0, 1.2, 1.0,
1.1,1.0, 1.1
2.0, 2.3,2.3,2.1,
2.1, 2.2, 2.2
2.2,2.1,2.2
10
X
SD
-
1.04
0.07
2.17 f 0.09
Number of sections measured.
shoe pattern around the intralobular vein (Fig. 4). The
reptilian-type glomeruli were found about halfway between the interlobular and intralobular veins. Originating from the glomerulus, the proximal tubule first ran
peripherally in the lobule to the interlobular vein. Here
it turned and ran to the center of the lobule, turned
again, and ran all the way back to the interlobular vein.
The proximal tubule of the reptilian-type nephrons thus
had no convoluted part (Fig. 5). However, this pattern
could be modified to a very great extent. In the subcapsular nephrons the proximal tubule in particular often
ran parallel to the kidney surface for more than 300 pm
(Fig. 3). Despite this variation, the major bends were
always present. After having turned once more, the
tubular lumen became wider. The epithelial lining was
then flatter and the cells had a lighter staining cytoplasm. This was the junction between the proximal and
distal tubule, and the change occurred often, but not
always, very abruptly from one cell to the next. No loop
of Henle could be identified, but the distal tubule always
ran to the glomerular hilus, where it had direct contact
with the vascular pole. On the side of the distal tubule
where it was attached to the vascular pole, the epithelial
cells had a different appearance from that seen elsewhere in the distal tubule. The cells were somewhat
taller and more narrow, with closely packed nuclei. The
cytoplasm of these cells mostly stained lighter than that
of the neighboring cells. Thus these cells showed the
characteristics of macula densa cells (Fig. 6). Postglomerularly the distal tubule often became very thin-walled
and was almost always convoluted. However, as in the
proximal tubule large variations were seen. These
ranged from a U-shaped loop to a labyrinth of folds. This
part of the nephron always ran close to the intralobular
vein with large venous branches that came from the
interlobular vein between the segments of the distal
tubule (Fig. 4). As the distal tubule of the deeper glomeruli turned the last time, it was almost within the
Fig. 4. Cortical lobule with reptilian-type glomeruli arranged in a
horseshoe pattern around the intralobular vein (i). Note large venous
channels between distal tubules in the center of the lobule. Micrograph
X 70, silver methenamine.
intralobular vein. From this point it ultimately ran towards the collecting duct, which it reached in the outer
third of the lobule. On the way between the central vein
and the collecting duct, the distal tubule exhibited a
thin segment with a n extremely flat epithelium reminiscent of the thin loop of Henle (Fig. 7). After some
distance (50-150 pm) the epithelium was higher again
and finally the distal tubule drained into the collecting
duct. This composition of the reptilian-type nephron resulted in a long structure lying between the two great
veins (Figs. 2,3).We found the outer and inner diameter
of the tubule to change frequently within the same tubular segment, between different tubular segments, and
from tubule to tubule.
The venous drainage from the interlobular to the intralobular vein occurred via a venous capillary network
between the tubular segments. In the periphery of the
lobule the tubules lay close together and the veins were
narrow. More centrally the tubules were separated by
large capillaries with increasing lumina that eventually
resulted in large venous channels towards the intralobular vein. The distal convoluted tubule was always surrounded by these venous channels. The termination of
STRUCTURE OF THE AVIAN KIDNEY
37
these peritubular venous channels in the intralobular
vein from many different directions created a picture in
which segments of the distal tubule were found indented
into the intralobular veins (Fig. 8).
The average area covered by one reptilian-type nephron was about 880 pm long and 115 km wide (Table 3).
The diameter of the proximal tubule was 40.8 pm, that
of the distal tubule 23.1 pm, and that of the collecting
duct 38.2 pm. The total length of the nephron was difficult to estimate because of the convoluted parts and
because the sections will always be at an angle to the
nephron, but it was found to be at least 2,400 pm long
(Table 3). The length of the tubule was also measured
by means of the reconstructions. Here it was found to be
slightly more than 6,000 pm in the longest and most
complicated folded nephron (Fig. 3) and approximately
3,000 pm in the shortest nephrons with few secondary
folds.
In the mammalian-type nephrons the proximal tubule
was convoluted, as is usual in mammalian species. The
distal tubule showed a definite macula densa with taller
and more narrow cells on the glomerular side of the
lumen. Other typical hallmarks of the macula densa
such as crowding of their nuclei and lighter-staining
cytoplasm were also present (Fig. 9).
DISCUSSION
loop
W
Fig. 5.
Schematic drawing of the basic folding pattern of the
reptilian-type nephron in the avian kidney. For better orientation the
tubular loops are drawn side by side. Glomerulus and proximal tubule
dotted. Distal tubule white. Arrowheads indicate interlobular and
intralobular veins.
The work of Huber (1917) on corrosion casts revealed
many important features of the avian nephrons. However, the fine relationships of the tubular segments could
not be disclosed because the technique Huber had used
forced him to tear the nephrons apart from each other.
The work of Wideman et al. (1981)was very comprehensive in this respect and we were able to confirm the
basic folding pattern of the reptilian-type nephrons described by these authors (Fig. 5). The conclusions in
their study, however, were drawn mainly on the reconstruction of two subcapsular nephrons. The present study
Fig. 6. Reptilian-type glomerulus with juxtaglomerular apparatus. Macula densa in the
distal tubule between arrowheads. Between the distal tubule and the glomerulus the Goormaghtigh cells are seen (Christensenet al., 1982). Micrograph ~ 4 5 0silver
,
methenamine.
38
I. MORILD, A. BOHLE, AND J.A. CHRISTENSEN
Fig. 7. Reptilian-type distal tubule with transition of epithelium from cuboid to flat type
(arrowheads).Micrograph ~ 4 5 0PAS.
,
Fig. 8. Intralobular vein with distal tubular segments in large venous channels splitting
up the boundary of the vein. Arrow points to an endothelial nucleus. Micrograph ~ 2 8 0silver
,
methenamine.
analyzed the nephrons more precisely, as we reconstructed 8 nephrons from different birds and in different
regions of the renal cortex. The basic architecture was
maintained in all the reconstructed nephrons, but the
individual variations were very large. No single explanation was found for these variations, but the cortical
location may be a n important factor because the largest
loops were seen in the subcapsular nephrons. It seemed,
however, more likely that the secondary folds, i.e. those
additional to the basic pattern, were determined by
many factors such as neighboring nephrons and the
distance between the glomeruli and the renal surface.
STRUCTURE OF THE AVIAN KIDNEY
39
Fig. 9. Mammalian-type glomerulus with distal tubule and juxtaglomerular apparatus on
the top. Macula densa indicated with arrowheads. Between the distal tubule and the glomerulus are the Goorrnaghtigh cells. Micrograph ~ 2 8 0silver
,
methenamine.
TABLE 3. Measurements of reptilian-type nephron outlines
and tubular diameters
Nephron outline
length
Nephron outline
breadth
Diameter prox.
tubule
Diameter dist.
tubule
Diameter coll.
duct
n
=
n
Observations
per animal
6
30
6
30
6
50
6
50
6
50
Mean
per animal
890,946, 727,
921,959,875
105,108,116
102,125,126
43.6,40.7,37.6,
41,7,45.7,35.4
27.9,21.8, 19.1,
25.5, 24.5, 19.7
45.5, 35.6, 33.7,
36.2,44.8,33.6
Mean of
group SD
886 & 84.4
114 k 10.3
40.8
+ 3.8
23.1 f 3.5
38.2 & 5.5
Number of animals. All figures in microns.
The distance between the glomeruli and the intralobular veins may also be of significance to the secondary
tubular foldings. The size of the glomeruli is another
parameter that may influence the glomerular filtration,
and secondary tubular length and foldings. This means
that a certain tubular length is of functional importance
with respect to reabsorption and excretion and will always be established even if the tubules have to make
the most peculiar bends, loops, and foldings. Particularly in the subcapsular region of the cortex, the proximal tubule was folded parallel to the kidney surface
(Fig. 3).
In our reconstructions we found much greater variation of the tubular architecture than did Wideman et al.
(1981).We, too, found an abrupt transition between the
proximal and distal tubule but not in all nephrons.
The measurements of tubular diameter showed that
the proximal tubule and the collecting duct were approximately the same size. The distal tubule had a diameter
half that of the proximal tubule. We also found conspicuous variations of the outer tubular diameter on all
levels of the nephrons. These changes were combined
with variations in epithelial differentiation. Thus, narrow tubules had a more flattened epithelium than wide
tubular segments. Very often, but not always, the distal
tubule of the reptilian-type nephrons in all regions of
the cortex had a very thin segment (Fig. 7). Here the
epithelium was so flat that the nuclei elevated the luminal surface of the cells. This segment was found
shortly after the distal tubule had made its last bend
close to the intralobular vein and was running towards
the collecting duct. This segment was reminiscent of the
40
I. MORILD, A. BOHLE, AND J.A. CHRISTENSEN
thin loop of Henle, but as Henle’s loop is located between
the proximal tubule and the distal part of the tubule in
mammalian-type nephrons, anatomically the thin segment of the reptilian-type nephron in the bird belonged
to another part of the tubule.
The length of the tubule did not correspond to the
results of Huber (1917), as his figures are much higher
than ours. Wideman et al. (1981) calculated the length
of the nephrons from their reconstructions. Their nephron lengths were 2,016 pm and 2,375 pm. However,
when the given scale in their publication is compared
with the illustrations of the reconstructed nephrons, it
seems as if the nephron lengths were approximately
20% shorter. These discrepancies may be caused by the
fact that we measured on the reconstructions, whereas
Wideman et al. (1981) may have measured on serial
sections, although this is not stated in the text.
When the distal tubule reached the glomerular hilus,
a macula densa was always present. This was true for
both the reptilian-type and mammalian-type nephrons.
This finding is in accordance with most of the others
reported (Berger, 1966;Edwards, 1940;Johnson and Mugaas, 1970; McKelvey, 1963; Schoemaker, 1972; Siller,
1971).However, in these studies the reptilian-type nephrons were not distinguished from the mammalian-type.
A recent publication (Wideman et al., 1981) on renal
tissue fixed by perfusion failed to demonstrate a macula
densa. This may have been caused by the fact that their
study was made on semithin sections alone. In our opinion it is difficult to recognize the macula densa on semithin sections without the experience of serial sections
from material embedded in paraffin.
Ogawa and Sokabe (1971) found the macula densa
cells in birds to be intermediate in structure between
macula densa cells and ordinary tubular cells. They did
not distinguish between reptilian- and mammalian-type
nephrons and used fixation by immersion. Unpublished
data from our laboratory indicate that the subcellular
organization of the distribution of microchondria and
folds of the basal labyrinth is similar in both macula
densa cells and in other distal tubular cells. There are
only narrower and taller cells in the macula densa
segment.
ACKNOWLEDGMENTS
This study was supported by the Gade Foundation and
the German Research Foundation. I. Sdborg prepared
all the serial sections with great care and L. WieseHansen typed the manuscript.
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