Compazative Renal Function in Reptiles,
Birds, and Mammals
Eldon J. Braun, PhD
In this article, the regulation of the homeostasis of the
extracellular fluid is compared for reptiles, birds, and
mammals. The principle focus is on the role of the
kidneys in this process. Although the basic elements of
renal function are similar in the three classes, birds and
mammals are set apart from reptiles in that the kidneys
of these speeies have the ability to produce urines that
are hyperosmotic to plasma. Reptiles and birds are set
apart from mammals by the fact that these two groups
excrete nitrogen as uric acid and not urea as do mam-
mals. Reptiles and birds are further set apart from
mammals in that the kidneys of these two groups are
not the sole organs that function to regulate the compo-
sition of the extracellular fluid. In addition to having
functional salt glands, the lower gastrointestinal tracts
of reptiles and birds function in concert with thekidneys
in the maintenance of homeostasis. There is a much
greater range in body mass among mammals than in
the other two groups. This has necessitated that the
kidneys of mammals change size, shape, and internal
organization to be able to carry out their homeostatic
function. The kidneys of reptiles and birds do not follow
a similar pattern. It would appear that no one group has
the advantage over the other with respect to regulation
of the composition of the extracellular fluid because
representatjves of all groups inhabit a broad range of
environments and ecological habitats.
Key words: Reptiles, birds, Mammals, kidney, morphol-
ogy, physiology
@ lthough reptiles, birds, and mammals are all
amniotes (have a similar pattern of embry- onic
development), the kidneys of these three
vertebrate groups achieve their goal of maintain-
ing the homeostasis of the extracellular fluid
(ECF) in different ways. Although some of the
basic processes are similar, there are marked
differences in the extent and degree to which the
kidneys are involved in the regulation of the
composition of the ECF in each group. Before
from the Department of Physiology, College of Medicine, Unirer-
sitf o/Arizona, Tucson, AZ.
Address reprint requests to Eldon J. Braun, PhD, Department of
Ph.ysiology, College of Medicine, University of Arizona, Arizona
Health Science Ctr 4121, PO Box 245051, Tucson, AZ 85'724.
C,op righl °O 1998 by W.B. Saunders Company.
1055-937X/98/0’702-0002ff8.00/0
62 Seminars in Aatau and Exotic Pet Medicine, Vol 2, to 2 (April), 1998: pp 62-'71
discussing the similarities and differences in
renal function, it would be wise to review the
gross anatomy of the kidneys, nephron structure,
and histology for the three groups. The kidneys
of mammals will be described first, followed by
those of birds and reptiles.
Gross Morphology of Kidneys
The mammalian kidney is most typically de-
r icted as a unipapillate, bean-shaped organ. This
is true for the kidneys of small mammals (to a
body mass of about 5 kg).' 3 However, the exter-
nal form and internal organization of the kidney
change as body mass increases and as animals
from different habitats are examined. In general,
as the body mass of mammals increases, the
internal organization of the kidney changes. The
first change that is observed is a dividing of the
medullary region into subunits, although the
cortex remains undivided. This compound mul-
tirenculate kidney is seen in primates, including
humans.’‘3 In some mammals the renal medulla
remains undivided, but its depth decreases and
its anterior-posterior length increases. This form
of the kidney is referred to as a crest kidney and
is typical of the kidneys of carnivores (large cats
and the dog family) and some artiodactylids
(camels, wildebeests).' 3 As the body mass of
mammals increases further, the cortical tissue of
the kidneys also becomes subdivided. These
kidneys are called discrete multirenculate and
are the form observed in large mammals such as
the pinnipeds (seals) and cetaceans (whales).' "
Extreme examples of this kidney form are seen
in some of the large marine mammals, in which
the whole kidney is composed of a large number
of individual units that, when sectioned midsagi-
tally, resemble the kidneys of rodents in shape
and size.° Fig 1 depicts examples of the different
kidney types (shapes) found in mammals.
Why don’t the kidneys of mammals retain the
rather simple shape of those seen in rodents (the
unipapillate kidney) andjust become larger to fit
the demands of maintaining the consistency of
 Renal function
Figure 1. Schematic illustrations of the morphology
of the kidney types that occur in mammals. No
attempt has been made to draw the illustrations to an
appropriate scale. In total size, the (A) unipapillate
kidney is acmally the smallest kidney and the (D)
discrete multirenculate is the largest kidney. (B) crest;
(C) compound multirenculate.
the ECF? After all, the unipapillate kidney has
been suggested to be the most primitive kidney
form.' Part of the answer lies in the structure of
the nephrons. When a relationship between
nephron length and body mass is developed and
plotted, it is observed that the total length of the
nephrons does not continue to increase as body
mass increases.’ However, kidneys of elephants
and whales do not have extremely long nephrons
to match their body mass. These kidneys have a
large number of small nephrons that are pack-
aged in a different manner. However, the total
number of nephrons in the kidneys of mammals
does scale allometrically with body mass.4
What limits the absolute length of the neph-
rons of mammals as body mass increases? Exami-
nation of the factors that determine how much
plasma water is separated from the blood and
crosses the filtration barrier reveals that two
parameters function as the main determinates of
the process of ultrafiltration. These are the
hydrostatic pressure put on the blood by the
pumping action of the heart and the concentra-
tion of proteins in the blood. The hydrostatic
pressure forces fluid across the filtration barrier,
and the colloidal osmotic pressure exerted by
the plasma proteins opposes the filtration pro-
cess. When systemic blood pressure and plasma
protein concentration are examined for a wide
range of body masses of mammals, it is seen that
these two parameters do not scale allometrically
with body mass.‘ Large mammals do not have
63
extremely high blood pressures and protein
concentrations. When all the factors involved in
the process of ultrafiltration in mammals are
considered, there are only about 10 mm Hg
hydrostatic pressure to overcome the frictional
resistance of the filtration barrier. Therefore, the
nephron length cannot increase as body mass
increases, because the resistance to flow along
the nephrons would increase and the pressure
put on the system by the heart would be unable
to maintain flow along the nephron. The compro-
mise is that larger mammals have an increased
number of smaller nephrons. The increased
number of nephrons necessitates that they be
packaged in a different manner to facilitate the
flow of tubule fluid (urine) to the ureter and on
to the bladder.
The lengths of the nephrons within the kid-
neys of mammals may vary from species to
species and even within a given kidney, but they
are all composed of the same segments. A neph-
ron begins with the renal corpuscle (capsula
glomeruli) that leads into the proximal convo-
luted tubule (PT-Fig 2). Based on function (trans-
port characteristics), the PT can be divided into
three segments: S , St, and S3. The PT leads to
the descending limb of the loop of the nephron
[Ansa nephroni) , which makes a hairpin turn at
varying depths of the renal medulla and forms
the ascending limb of Henle (ALH) . The ALH
returns to the renal cortex and makes contact
with the renal corpuscle from which the neph-
ron originated. This point signals the beginning
of the distal convoluted tubule (DT). The DT
leads into the connecting tubule, which connects
the nephron to the cortical collecting duct
(CCD). The CCD descends straight to the renal
medulla, coalesces with other collecting ducts
(CDs), and finally terminates at the papillary tip.
The large ducts (collecting ducts) at the tip of
the papilla do not make a direct connection with
the ureter. The urine literally drips from the
collecting ducts and is collected by the renal
calyces, which coalesce to form the renal pelvis,
which narrows to form the ureter.
The lengths of the nephrons within a mamma-
lian kidney vary depending on the location of
the renal corpuscle in the cortex. At the ex-
tremes, there are renal corpuscles located near
the surface of the kidney, superficial cortical
nephrons, and renal corpuscles located at the
boundary between the cortex and medulla, juxta-
64
111 I C lllC t) 1 i\IC
Uist:il
Figure 2. Il)ustrations showing the different nephron
configurations that can be found in the kidneys of
reptiles, birds, and mammals. The nephrons are not
drawn to scale. (A) The nephrons in the kidneys of
reptiles have a rather long PT, a thin intermediate
segment, and a short DT. The DTs enter the CD at
right angles. (B) The loopless nephrons of bird
kidneys have a similar configuration to the nephrons
in reptilian kidneys, but are simpler in structure.
These nephrons have only a PT and DT and no
intermediate segment, but enter CDs at right angles as
do the nephrons in the kidneys of reptiles. These
loopless nephrons are very short, being only 4 to 5 mm
in total length. (C) The looped nephrons of avian
kidneys are quite similar to the looped nephrons in
the kidneys of mammals. The major difference is that
they do not have a thin ascending segment to the loop
of the nephron. These nephrons are quite long (ca. 15
mm) with highly convoluted PT and DT. (D) Except
for some of the shortest superficial cortical nephrons,
the nephrons of mammal kidneys are longer than
those found in the other groups. The looped neph-
rons of the avian and mammalian kidneys are ar-
ranged parallel to the CDs. This facilitates the opera-
tion of countercurrent multiplier systems to allow the
production of urine that is more concentrated than
the plasma (hyperosmotic urine).
Eldon J. Braun
medullary nephrons. With some exceptions, the
superficial cortical nephrons tend to be consider-
ably shorter than the juxtamedullary nephrons.
This structural difference may have a functional
correlate in the overall renal processing of so-
dium and water.
The kidneys of birds have some anatomical
features in common with the kidneys of both
mammals and reptiles. A stylized avian kidney is
depicted in Fig 3. Whereas all the nephrons
within the kidneys of mammals have a loop of
the nephron, only a small percentage of those in
avian kidneys have loops of the nephron. The
majority (70% to 90%) of nephrons have no
loops and more closely resemble those found in
the kidneys of reptiles. 5 All the nephrons within
the kidneys of reptiles lack the loop of the
nephron (Fig 2).^ The gross organization of the
avian kidney, as depicted in Fig 3, does not
change as dramatically with body mass as does
that of mammals. The same pattern of organiza-
tion appears to be retained as body mass in-
creases. If a parallel were to be drawn with the
mammalian kidney, the avian kidney probably
most closely resembles in internal organization
the compound multirenculate kidney. Although
the cortical region of avian kidneys is more
divided than that of the compound multirencu-
late kidney, it is less divided than the discrete
multirenculate kidney of mammals.
Another major difference between avian and
mammalian kidneys relates to the termination of
the collecting duct systems. As noted previously
for the kidneys of mammals, the collecting ducts
terminate at the papillary tip in rather large
openings. This discontinuity does not exist in the
collecting duct system of the avian kidney. The
end of each medullary cone is formed by one
large collecting duct. Several of these large
collecting ducts merge to form a primary ure-
teral branch, and several of these primary ure-
teral branches unite to form the ureter that runs
on the ventral surface of the kidney. The end
result is that within the avian kidney (and the
reptilian kidney), there is a continuous system of
ducts from the smallest loopless nephron on the
surface of the kidney to the entrance of the
ureters into the cloaca.
The kidneys of birds also differ from those of
mammals in the degree of morphological hetero-
geneity that is observed in the populations of
nephrons that make up these kidneys (Figs 2 and

Figure 3. An illustration
showing the internal organi-
zation of the avian kidney.
The whole kidney is shown
at the lower left with two
successive enlargements to
show the fine detail of the
kidney. (Reprinted with per-
mission 24)
3). There is a much greater extreme in nephron
structure in the avian kidney than the mamma-
lian kidney. All the nephrons of mammalian
kidneys have loops of the nephron, whereas only
10% to 30% of the nephrons in avian kidneys
have loops of the nephron. These loops, vase
recta, and collecting ducts form the medullary
cones of the avian kidney (Fig 3). Depending on
the species, the remaining 70% to 90% of the
nephrons in avian kidneys do not have a loop of
the nephron. These are small nephrons that fold
over themselves four times and their connection
to collecting ducts is at right angles. This anatomi-
cal arrangement does not permit these neph-
rons and their collecting ducts to function as a
countercurrent multiplier system. This means
that the tubule fluid (urine) elaborated by these
nephrons cannot be more concentrated than the
plasma. This organization of the avian renal
cortex is similar to the general organization of all
the nephrons in the kidneys of reptiles. The
functional result is the same for reptilian kid-
neys: a urine more concentrated than the plasma
cannot be produced. In the avian kidney, the
collecting ducts that drain the loopless nephrons
enter the medullary cones and merge with the
collecting ducts that drain the looped nephrons.
Thus, these collecting ducts deliver a large
amount of dilute to isosmotic fluid to the coun-
tercurrent multiplier system that operates in the
medullary cones. This may limit the capacity of
the avian kidney to concentrate the urine.
65
LONG LOOP MAMMALIAN -TYPE f4EPFIRON
Reptiles as a group of vertebrates display an
extreme variation in body form from the legless
Ophidians (snakes) to the tetrapod forms (Lacer-
tilia-lizards, Crocodilia-alligators and crocodiles,
and Chelonia-turtles and tortoises), and this
affects the gross shape of the kidneys. Those of
the tetrapod reptiles are all somewhat similar in
shape (oval, flattened, compact). In keeping
with their body form, the kidneys of ophidians
are long, narrow, rod-shaped structures. 5 Under
an external capsule, the kidneys of all reptiles
show a very distinct segmentation into lobules.
These tend to be wedge-shaped and fit in a
complementary manner with each neighboring
lobule along the long axis of the kidney. The
collecting ducts, which are oriented at right
angles to the long axis of the kidney, originate on
the dorsolateral surface of each lobule. They
tend to remain on the surface as they wrap
around the lateral margin of the lobule and pass
ventrally to enter the ureter, which lies on the
ventral-medial surface of the kidney. 5 This gross
organization of the reptilian kidney is very differ-
ent from that of both birds and mammals.
There is a definite pattern in which the
nephrons of reptilian kidneys are organized (Fig
2). The individual nephrons in each lobule are
oriented at right angles to the long axis of the
kidney and enter the collecting ducts at right
angles. The renal corpuscles lie in a circular
pattern near the midportion of each lobule. In
the tetrapod reptiles, there are two rows of renal
66 Eldon J. Braun

corpuscles near the center of each lobule of the Urine Concentration

kidney. In the ophidian kidneys, the nephron is
The differences between birds and mammals
gently folded on itself such that it traverses the
in structure of the loops of the nephron and in
complete thickness of the lobule three times.^ In
the medullary regions is expressed in the func-
the tetrapod reptiles, the nephrons appear to
tion of this region of the kidney for the two
have a similar folding pattern, but each nephron
groups. In mammals, the osmotic gradient that
traverses only half the thickness of a kidney
extends from the cortical-medullary boundary to
lobule.6
the tip of the medullary region is primarily made
A comparison of the structural organization
of two solutes, sodium chloride and urea. In
of the nephrons from the kidneys of the three
birds, this gradient is made of only sodium
classes of vertebrates is presented in Fig 2. A
chloride. The primary function of the renal
typical nephron from a reptilian kidney starts
medulla is to modulate the osmotic potential of
with the renal corpuscle, which is connected by a
the urine depending on the need to either rid
thin, ciliated neck segment to the proximal
the body of excess water or to conserve body
tubule. This is followed by a narrow, ciliated
water. The ability to conserve body water by
intermediate segment. This is followed by the
producing urine more concentrated than the
distal tubule, which leads to the collecting duct.
body fluid (plasma) is much greater in mammals
This pattern of organization is not followed in
than in birds (Table 1). Birds at best can gener-
either the avian or mammalian kidneys. As men- ate urine-to-plasma (U/P) osmolar ratios of about
tioned previously, the population of nephrons in 2.0 to 2.5, whereas some mammals can generate
the avian kidney is morphologically very hetero- U/P ratios as high as 25 to 30.
geneous, much more so than is observed in For several reasons, caution must be used
either the reptilian or mammalian kidneys. The when comparing birds and mammals with re-
small nephrons on the surface of the avian spect to U/P osmolar ratios. First, the plasma
kidney have just proximal and distal tubules and osmolality of birds tends to be more labile than
lack a neck and intermediate segment. These that of mammals. Humans and some standard
nephrons are stucturally very simple, with the laboratory animals (rats, rabbits) have plasma
tubule folded on itself three times. At the other osmolalities about 300 mOsm /kg HCO that
extreme, some of the nephrons of the avian
kidney have almost all the segments typically
Table 1. Urine to Plasma Osmolar Ratios for
found in the nephrons of mammalian kidneys.
Selected Birds and Mammals
These are (in sequence) the renal corpuscle,
proximal tubule, loop of the nephron, and distal Birds U/Pg Mammals U/P
tubule. Domestic Fowl 1.5 Long-nosed bat 1.1
The structure of the nephrons of the avian Senegaldove 1.7 Nutria 2.5
kidney has not been examined in the same detail Savannah Sparrow 1.7 Mountain beaver 2.7
as has the structure of the nephrons of the Budgerigar 2.3 Pig 3.6
mammalian kidney, except perhaps for the loop Singing Honey- 2.4 Hereford cow 3.9
eater
of the nephron and collecting ducts.’ For ex- King quail 1.8 Blue whale 4.5
ample, it is not known whether the avian proxi- House finch Y4 Bottle nose dolphin 6.1
mal tubule can be divided into three functional Zebra finch 2.8 Weddell seal 6.8
segments as has been done for mammals. With Stubble quail 2.6 Dog 8.7
Cat 10.8
respect to the loops of the nephron, the organiza-
COttOntail 11.0
tion of these tubule segments is different in Merriam’s kangaroo 21.2
birds. For the long-looped nephrons in the rat
mammalian kidney, there is a thin ascending House mouse 23.3
segment. The looped nephrons in the avian Desert pocket mouse 28.6
Australian hopping 31.2
kidney do not have this segment.* For all looped mouse
nephrons in avian kidneys, the epithelium thick-
ens before the hairpin loop is formed such that NOTE. The U/P„p values for mammals were computed
using data from Beuchat’ and assuming a plasma osmolality
there is a thick descending segment to the loop of 300 mOsm for all the species listed.
of the nephron.’ Data for birds are from Braun.**
 Renal Function
change little with water deprivation. On the
contrary, the plasma osmolality of birds tends to
increase with water deprivation, which prevents
the calculated U/P„p ratio from increasing.
Second, the form in which nitrogen is excreted
by birds (uric acid) contributes very little to the
pool of osmotically active solutes in the urine.
The similarities in renal function among this
group of vertebrates are in the processes of
glomerular filtration, reabsorption of solutes
and fluid, and the secretion of solutes by the
renal tubules. The fundamental mechanisms
underlying these functions are similar, but their
magnitude differs.
Blood Supply
The blood supply to the kidneys differs among
these three vertebrates. Typically, each mammal
kidney is supplied with blood by one renal artery
that branches from the abdominal aorta, and
each avian kidney is supplied with blood by three
renal arteris. The kidneys of reptiles are supplied
by multiple arteries; the number depends on the
size or body mass of the animal. In addition to
being supplied with arterial blood, reptilian and
avian kidneys receive a venous blood supply by
way of functional renal portal systems. This latter
blood supply facilitates secretion of substances
by the renal tubules.
Nitrogen Excretion
In animals, the metabolic pathways that lead
to the production of nitrogen compounds start
with the degradation of amino acids, which
depends on the degradation of protein. Ammo-
nia is the simplest form by which to excrete the
nitrogen produced by the metabolism of amino
acids. However, this molecule is very toxic to the
central nervous system and requires large
amounts of water for its rapid removal from an
organism. As animals moved from aquatic envi-
ronments to terrestrial habitats where water was
less abundant, different forms of nitrogen excre-
tion evolved. In reptiles and birds, the principle
form of nitrogen excretion that evolved was uric
acid. This form of nitrogen excretion is consid-
ered very e&cient with respect to the amount of
water required for its excretion because of its
very low aqueous solubility (0.386 mmol/L for
the acid form, but the salts of uric acid have
57
slightly higher solubilities) . Because the majority
of the uric acid in reptilian and avian urine is not
in solution, but exists as a colloidal suspension, it
does not contribute to the osmolality of the
urine. This suspension is made up of small
spherical structures, which range in diameter
from 0.5 to 15 pm, and rather large amounts of
protein.' The spheres are composed of about
65% uric acid.'0 These are not crystals and the
uric acid is not in a crystalline form within the
spheres, but the uric acid is chemically bound to
a matrix protein that forms the spheres.’
The urine of reptiles and birds contains rather
large amounts of protein, at least when the urine
of these two forms is compared with that of
mammals. Although I am not aware of measure-
ments on the urine of reptiles, avian urine
contains an average of 5 mg/mL of protein.' 0
The urine of mammals is relatively free of pro-
tein. Thus, reptiles and birds may not require as
much water to excrete nitrogen as mammals do,
but they require large amounts of protein to
maintain uric acid in colloidal suspension to
prevent the uric acid from precipitating from
solution. This has to be taken into account when
considering the efficacy of uric acid as a nitrogen
excretory product.
Mammals excrete nitrogen as urea, a com-
pound 40,000 times more soluble in water than
uric acid. Because of this solubility, it does
require water for its excretion. A small portion of
the urea is retained in the renal medulla, where
it plays an important role as a component of the
intramedullary solute gradient. This gradient is
necessary for the production of urine that is
hyperosmotic to plasma, which can conserve
water when an animal is deprived of water.
Which form of nitrogen excretion is more
efficient? Uric acid requires protein for its excre-
tion and urea requires water for its excretion,
both of which can “cost” animals in terms of
energy and survival. For reptiles and birds, the
protein in ureteral urine is not excreted (lost to
the animal) because the urine is moved from the
cloaca into the rectum by a reverse peristalsis."
In the rectum (lower gastrointestinal tract), the
protein of the urine is degraded and the pep-
tides and amino acids are absorbed and re-
cycled.'° Urea is highly soluble in water and does
not require large amounts of water for its excre-
tion (compared with ammonia). Therefore, both
68 Eldon J. Braun
forms of nitrogen excretion are efficient for the
purposes they serve in the different animals.
Response to Water Deprivation
For mammals, the kidneys are the sole organs
that function to regulate the com r osition of the
extracellular fluid. Water can be lost through
other routes (skin, lungs, gastrointestinal [GI]
system), but only through the kidneys is the loss
regulated for the purpose of maintaining the
consistency of the extracellular fluid. The kid-
neys of mammals respond to water deprivation
by extracting more water from the fluid within
the renal tubules and returning this fluid to the
plasma. This occurs in the medullary region of
the kidney, where the collecting ducts change
their permeability to water in response to the
antidiuretic hormone. In the case of mammals,
this is arginine vasopressin, which is released
from the posterior pituitary gland. The antidi-
uretic hormone causes the insertion of water
channels into the luminal membrane of the
collecting duct cells. These channels allow the
passage of water from the lumen to the medul-
lary interstitium, where it is picked up by capillar-
ies. The water moves out of the collecting ducts
on osmotic gradient, that is, the medullary inter-
stitium has a higher osmotic potential then the
tubule lumen. The hypertonicity of the medul-
lary interstitium is generated by the countercur-
rent multiplier- system. Urine concentrating abili-
ties of mammals range from the long-nosed bat
and nutria that at best can produce isosmotic
urines when water deprived, to some of the small
desert rodents of the southwestern United States
and Australia that can produce urines that are 25
to 30 times more concentrated than plasma.3
The response of birds to water deprivation is a
bit more complicated, as the kidneys are not the
sole organs that can function to regulate the
composition of the extracellular fluid. In all
birds, the urine enters the terminal portion of
the GI tract (the cloaca), because birds do not
have a urinary bladder in which to store this fluid
until it can be conveniently voided. This automati-
cally involves the lower GI tract in the regulation
of the composition of the extracellular fluid. In
addition, many birds have functional nasal or salt
glands that play a major role in normal water
balance and how these birds respond to the
stress of water deprivation. Thus, in this group of
vertebrates, the kidneys function in concert with
at least two other organs in the regulation of
fluid and electrolyte balance.
For birds with and without salt glands, the
urine enters the cloaca and is moved by reverse
peristalsis into the rectum." In general, fluid
moves across the epithelium of the lower GI tract
in an isosmotic fashion. That is, large osmotic
gradients cannot be maintained across this tis-
sue, and water flow follows the transport of
solutes. For this reason, the urine entering the
rectum should not be highly concentrated. The
avian kidney, like that of mammals, can produce
a urine that is more concentrated than the
plasma. As noted previously, some mammalian
kidneys have a remarkable capacity for this
function. However, the capacity of the avian
kidney to concentrate urine is rather limited, in
that at a maximum the urine can be two to two-
and-one-half times more concentrated than the
plasma. For reasons just mentioned, this is as it
should be. In response to water deprivation, the
osmolality of the urine tends not to increase a
great deal. Under most circumstances, the urine
is isosmotic or only slightly hyperosmotic (ca.
100 mOsm higher than plasma), and there is
evidence that if the urine becomes too concen-
trated, it will not be refluxed into the rectum."
This is supported by experimental evidence that
the epithelium of the rectum stops absorbing
water when the gradient across it reaches 100
mOsm.” In general, birds without salt glands
respond to water deprivation by slowly alloNng
the plasma osmolality to increase as the urine
osmolality increases such that a favorable os-
motic gradient is maintained across the epithe-
lium of the rectum.
Some birds and reptiles use functional nasal
salt glands to excrete excess salt consumed as a
normal part of the diet when the kidneys are
incapable of excreting these ions. As might be
expected, the response of birds with functional
salt glands to water deprivation is somewhat
different than that of birds that lack these or-
gans. Under circumstances of normal hydration,
the salt glands may not produce large amounts of
fluid, with the kidneys and lower GI tract doing
most of the work. When stressed (water deprived
or salt loaded), the plasma and urine osmolality
will increase, and when the urine osmolality
reaches about 400 to 450 mOsm/kg water, the
kidneys begin to decrease the amount of urine
 Renal Function
produced. At this point, the salt glands begin to
secrete larger amounts of concentrated fluid
(the primary solute being sodium chloride in
most birds). The decreased function of the
kidneys is regulated by the hormone arginine
vasotocin (AVT), and salt gland function is initi-
ated by the parasympathetic (cholinergic) ner-
vous system. The corticosteroids and the hor-
mones prolactin and AVT play permissive roles
in salt gland function.' 4
The pattern of response to water deprivation
in reptiles is similar to that of birds because of
similar anatomical characteristics, but with some
major differences. For reptiles, like birds, the
kidney is not the sole organ that functions in the
regulation of fluid and electrolyte balance. As in
birds, the urine enters the lower GI tract. Many
reptiles also have functional salt glands. A num-
ber of reptiles have urinary bladders, but this
organ serves a very different function than for
mammals. To a large extent in mammals, the
bladder serves purely a storage function. For
reptiles, the bladder also serves a storage func-
tion, but this storage is to conserve water so it can
be reabsorbed and used in periods of stress, ie, it
functions more as a canteen for these animals.
Reptiles are also set apart from mammals and
birds in that their kidneys can not produce urine
that is more concentrated than the plasma. At
best, the urine of reptiles is isosmotic with
plasma. Thus, they do not have this avenue
through which to conserve water. Reptiles are
also like birds in that most of them excrete
nitrogen in the form of uric acid, which allows
for the conservation of water. Moreover, reptiles
respond to water deprivation by allowing the
plasma and urine osmolalities to increase in
parallel, as is the case for birds. However, the
increases are more accentuated in reptiles. As is
the case with birds, a number of reptiles (many
lizards, turtles, tortoises, and some snakes) have
functional salt glands. The type of secretion
produced by these glands depends on the diet of
the animal. In most cases, the secretion is rich in
sodium chloride, but some herbivorous animals
primarily secrete potassium chloride.' 5
Endocrine Aspects of Renal Function
The kidneys of vertebrates play a prominent
role in the regulation of the composition of the
ECF through the processes of filtration, selective
69
reabsorption, and secretion. Closely associated
with this role is the endocrine function of the
kidney, as the kidney produces several hormones
that function either directly within the kidney or
indirectly (outside of the kidney) in the regula-
tion of the composition of the ECF. Among the
hormones produced by the kidney are renin,
urodilatin, dopamine, kallikrein, prostaglandins,
erythropoeitin, and a form of vitamin D (l,25-
dihydroxycholecalciferol). Brief descriptions of
the action of each of these hormones on the
kidney or other target organs follow.
Renin activity probably first appeared in the
bony fishes and has been conserved through the
aminoates, which means the renin-angiotensin
system is present in reptiles, birds, and mam-
mals. However, the presence of a juxtaglomeru-
lar apparatus (}GA) as exists in the kidneys of
mammals is questionable for reptiles and is
present in birds, but without the morphological
clarity that is present in mammals. For reptiles,
the distal tubule returns to the parent renal
corpuscle, but there appears to be no specialized
region of macula dense cells. For the avian
kidney, the J GA is well-developed for only the
looped nephrons. The renin-angiotensin system
functions primarily to regulate sodium balance,
either through stimulating the release of aldoste-
rone (which regulates sodium absorption by the
DT and CD) from the adrenal cortex, or by
affecting the amount of filtrate formed by control-
ling the resistance of the afferent and efferent
glomerular arterioles. 16
Urodilatin is a member of the atrial natri-
uretic peptide (ANP) family that is produced
and secreted within the kidney and does not
circulate in the systemic plasma. This 32—amino-
acid peptide differs by only four residues from
ANP.'° It is produced by the cells of the DT and
inhibits sodium transport by the cells of the CDs.
Thus, its action can be defined as being para-
crine (produced by one cell and acting on
neighboring cells). The stimulus for its release is
an excess of sodium in the body. At this point in
time, this hormone has only been isolated from
the kidneys of mammals. However, as members
of the ANP family have been isolated in both
birds and reptiles, it should not be too surprising
if urodilatin is found in the kidneys of these two
groups. 8
Dopamine is produced within the kidney and
acts as an intrarenal natriuretic hormone.' As
70 Eldon J. Braun
with urodilatin, the evidence for this is the large
amount of dopamine in the urine that is out of
proportion with the amount of noradrenaline or
adrenaline. Dopamine exerts is effects on the
vasculature and directly on the renal tubules. It
causes a dilatation of the arterial vasculature,
which increases blood flow and leads to a diure-
sis and natriuresis. The effect on the proximal
renal tubules is to slow the rate of ATP hydrolysis,
which leads to a decrease in sodium reabsorp-
tion and subsequently contributes to the diuresis
and natriuresis. These effects have been de-
scribed for the mammalian kidney, but little
comparative work has been done in this area.
The kallikrein system consists of a low molecu-
lar weight substrate (kininogen) and a family of
serine proteases (kallikreins) that cleave the
kininogens to produce the active end product,
bradykinin.°0 Bradykinin performs a wide range
of functions, including the regulation of blood
flow and the transepithelial transport of water
and electrulytes. The kinins (bradykinin) have a
very short half-life (<30 sec), suggesting that
they act more as paracrines than as classical
hormones. Because of this, circulating levels of
the kinins do not reflect activity of the kinins at
tissues levels. Within the kidney, kininogen is
produced in the early segments of the collecting
ducts (connecting tubule) and the targets of
bradykinin are the cortical and medullary collect-
ing ducts. The main action of bradykinin is to
cause a loss of sodium (natriuresis) . This is
thought to counter-balance the effect of the renin-
angiotensin system, which functions to re- tain
sodium. Although this system is well studied in
mammals (man and rat), there are few if any
comparative data in the literature. The presence
of this system has been identified in fish (Black
Sea bass),*' the African lungfish , 22 and amphib-
ians (Southern frog). 2' Thus, it is likely that the
system is present in reptiles and birds.
The kidneys produce a rather large number
of prostaglandins such as PGEt, PGE2„ PGDt,
thromboxane A2 and prostacyclin.°3 In the cor-
tex, the endothelial cells of the arteries and
arterioles produce the prostaglandins (PGs),
and in the medulla it is primarily the interstitial
cells and the cells of the collecting ducts that
produce these compounds. The PGs within the
kidney function primarily as modulators of the
activities of other hormones (or hormone sys-
tems) and of the nervous system to cause the loss
of sodium from the body. For example, the
renin-angiotensin system causes constriction of
the afferent arterioles, which would tend to
reduce the loss of sodium. But the renin-
angiotensin system also stimulates the release of
PGs, which cause dilation of the arterioles. Thus,
the two systems counter-balance each other. The
same is true of the action of antidiuretic hor-
mone (ADH) , which leads to the conservation of
water. However, ADH causes the release of PGs,
which feedback and, to a degree, inhibit the
action of ADH on the collecting duct cells.
Virtually all this information comes from experi-
ments on rats and some from human tests. It is
known that PGs are produced in the kidneys of
reptiles and birds, but very little is known about
how this complex hormone system functions in
these groups.
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