The Advantages and Disadvantages of Excreting Uric Acid
Shane R. Raidal1, BVSc, PhD, FACVSc (Avian Health)M. Scott Echols2, DVM, Diplomate ABVP - Avian Practice1.
2.

School of Agriculture and Veterinary Sciences, Charles Sturt University, Wagga Wagga, NSW,
2650, Australia
Westgate Pet and Bird Hospital, 4534 Westgate Blvd, Suite 100, Austin, Texas 78745, USA.

Summary
To understand and diagnose renal disease in birds it is first important to understand thebiochemical and physiological peculiarities of uricotely. The synthesis of uric acid andexcretion of urine with a high protein component is a metabolically expensive strategy thatmust have significant trade-offs to birds and other animals that have chosen this pathway for
excreting nitrogenous waste products. Birds rely heavily on post-renal modification of urine
to conserve water and salt balance so it is important to remember that damage to organs otherthan the kidney may present with signs that might be otherwise attributable to renal
dysfunction. In this paper we review the biochemical and physiological aspects of uricotelythat are important for understanding the normal function of the avian renal system.

Body Fluid Regulation and Nitrogenous Waste Excretion
Veterinarians graduate with a fairly good introduction to the physiology of the mammalianrenal system but in the animal kingdom mammals are odd (Braun 1998; Raidal and Raidal
2006). They have the capacity to produce concentrated urine containing potentially toxic
concentrations of soluble nitrogenous waste products as it leaves the kidney. Consequently
the mammalian ureter and bladder have to be impermeable to both water and urea to prevent
dilution of the urine and reabsorption of “excreted” waste. It is important to remember that
there is no post-renal modification of mammalian urine and the need for other solute secretoryorgans such as salt glands is redundant. This is primarily made possible by the enhanced urine
osmotic concentrating capacity achieved by the anatomical differentiation of renal cortex andmedulla along with the development of the loop of Henle to efficiently recycle soluble urea.
Mammals have the clever advantage of being able to utilise urea as a major osmolyte for theactual process of concentrating urine. The mammalian kidney is thus an efficient primaryorgan of osmoregulation and nitrogenous waste excretion and whilst it has 4 main functions:the removal of nitrogenous wastes (principally urea); regulation of water balance and bloodpressure; electrolyte homeostasis (particularly Na+, K+, Cl- and Ca+ ions); and acid-basehomeostasis it is the first that identifies it as unique amongst the vertebrates.
Other vertebrates including birds utilise multi-organ osmoregulatory mechanisms with
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87significant post-renal urine modification occurring to conserve water, ionic and pH
homeostasis and nitrogenous waste excretion (Figure 1). As it reaches the cloaca urine isrefluxed retrograde into the colon for resorption of water. If birds and reptiles excreted urea
as the chief nitrogenous waste product it would just be reabsorbed from the cloaca and colon.
Marine reptiles and birds also may possess nasal glands that excrete salt (Na+ and Cl- ions) tohelp them conserve water and sharks have rectal glands that perform a similar function. In fish
the gills and the opercular epithelium are important excretory and osmoregulatory organs withthe kidneys assuming a lesser role since they are able to excrete ammonia directly into theenvironment.
Elimination of Nitrogenous Wastes
Animals can be classed as ammonotelic, ureotelic or uricotelic, depending on whether they
predominantly excrete ammonia or the more metabolically expensive but less toxic urea oruric acid, respectively. However, this can be a loose distinction since many have the capacity
to excrete nitrogenous wastes in more than one form, or even all three when conditions areappropriate (Lee et al., 1991, Lim et al., 2004). These excretory strategies have evolved todeal with the elimination of ammonia (NH3) which is a highly toxic byproduct of amino acidmetabolism. Because it is a base, it rapidly accepts a H+ ion to form ammonium (NH4+) at
physiological pH and both NH3 and NH4+ are toxic (Cameron and Heisler, 1983). Hydrated
NH4+ has the same ionic radius as the hydrated K+ ion, and due to their K+-like behavior, NH4+
can affect the membrane potential of neurons and other cells (Binstock and Lecar, 1969;
Cooper and Plum, 1987) as well as result in toxic accumulations of glutamine and disruptionof essential cellular functions. Across the animal kingdom the ammonia concentration of body
fluids is typically low (50–400 µmol/L) (Cooper and Plum, 1987; Cameron and Batterton,
1978; Weihrauch et al., 2004) and concentrations exceeding 1 mmol/L total ammonia (NH3and NH4+) are usually toxic to mammalian cells (Hrnjez et al., 1999).
Reptilian Type Nephrons
To understand the avian kidney it is important to have some knowledge of reptilian-like
nephrons. Like in birds the kidneys of reptiles are the chief site of osmoregulation andnitrogenous waste excretion. And there is significant post-renal modification of urine in the
cloaca and or the urinary bladder, in those reptiles that have one. Reptilian nephrons have an
incipient juxta-glomerular apparatus, some aglomerular nephrons, and a thin very shortintermediate segment which connects the proximal and distal convoluted tubules. In reptiles(Bradshaw and Bradshaw 2002; Mahlmann et al., 1994), and birds, arginine vasotocin (AVT)
is the predominant antidiuretic hormone of the 10 neurohypophyseal hormones reported inother species (arginine vasopressin, arginine vasotocin, lysine vasopressin, glumitocin,
aspartocin, valitocin, isotocin, oxytocin and mesotocin). AVT may have a dual effect in thereptilian kidney, first to dilute the urinary fluid in the thin-intermediate segment, prior to its
entering the collecting duct system, and then facilitating water reabsorption along an osmotic
gradient as the urine passes through the final segments of the nephron. The intermediatesegment may thus prove to be the evolutionary homologue of the thin-ascending limb of theloop of Henle in the mammalian and avian kidney.
The relative length of the distal tubules is longer in reptiles adapted to dry environments and88

Association of Avian Veterinarians, Australian Committeetubular reabsorption of fluid is primarily from the distal segments of the nephron. In
freshwater turtles, the diuretic frusemide produces diuresis by doubling urine volume andincreasing Na+, Cl- and K+ excretion principally by inhibiting tubular reabsorption in the distalsegments of the nephron (Stephens and Robertson 1985). Turtles also lack a tubularmechanism for altering renin release but there is a well-developed renin angiotensin system
in reptiles (Cho et al 1987; Cipolle and Zehr 1984; Wilson 1984). Seasonal variations in reninlevels in relation to the physiological phase of the animals: active animals demonstrated highrenal and plasma renin concentration, while lower values were obtained in hibernating animals(Vallarino 1984).
The turtle urinary bladder is analogous to the collecting and distal tubules of the mammaliankidney and it has been used frequently as an experimental model in renal physiology(Drenckhahn et al, 1987; Henke et al., 1990). The epithelium of both the turtle bladder and the
mammalian collecting duct can generate a steep gradient for H+ ions between blood and urine.
Secretion of H+ into the urine is coupled to a basolateral efflux of HCO-3 that appears to beexchanged mainly against Cl-. Knowledge of the large urinary bladders in terrestrial chelonids
extends back to 1676 when the Parisian comparative anatomist Claude Perrault, observed theextraordinary size of the urinary bladder in the Indian giant tortoise (Jérgensen 1998). During
arid conditions desert chelonids do not void but store urine in the bladder where urine
osmolality gradually rises. Potassium ions are precipitated with uric acid as urates and the
bladder can thus function both to store nitrogenous waste and K+ as well as water which canbe reabsorbed as needed. However, plasma osmolality gradually rises (Dantzler and SchmidtNielsen, 1966) mostly due to and increase in urea concentration. Urine is only voided
following rain when copious drinking restores bladder volume with hyposthenuric urine. In
1799 Townson observed that dehydrated freshwater turtles imbibed water by anal drinking(Jérgensen 1998) but more recent evidence indicates that this is not a method of hydration but
rather so that the urinary bladder can supplement respiratory exchange of O2 and CO2 (Kingand Heatvole 1994a,b).
Uricotely in Birds and Reptiles
In reptiles and birds excretion of ammonia is achieved via the amino acid (andneurotransmitter) glutamate via its conversion to glutamine, glycine and aspartate forincorporation into the purine synthetic pathway. This pathway is much more energy expensive
than the urea cycle of mammals with the main advantage being the excretion of relatively
insoluble nitrogen-rich uric acid which is not reabsorbed from the cloaca in the adult or fromthe allantois in the avian embryo. In the egg urate occurs, not as a watery colloid gel as in theadult but as a crystalline anhydrous deposit in the allantois. This permits efficient recyclingof the transporting water and electrolytes and segregation of nitrogenous waste material. If
urea, about 40,000 times more soluble than uric acid, was the main nitrogenous waste productin avian and reptilian embryos it would readily diffuse back into the blood in potentially toxic
concentrations.

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Detoxification of Ammonia
In contrast to mammals the primary ammonia-detoxifying enzyme in avian liver is
mitochondrial glutamine synthetase (GS) and it is broadly distributed throughout mosthepatocytes (Smith and Campbell 1988), much like its counterpart carbamoyl-phosphatesynthetase I (CPS) in mammalian liver. With CPS, mammals are readily able to detoxify NH4
by converting it, along with two molecules of ATP and one molecule of CO2 into carbamyl
phosphate which combines with ornithine to enter the urea cycle as citrulline. Birds lack
mitochondrial CPS and so are unable to fuel the urea cycle in the same manner as mammals.
Birds instead use their mitochondrial GS to convert ammonia into glutamine. Both citrulline(mammals) and glutamine (birds) leave the mitochondria where they are then converted into
urea and uric acid, in mammals and birds, respectively.

Mammals

Birds

In mammals it is a then a relatively simple process to produce urea via the intermediates ofarginosuccinate and arginine. The final step which cleaves arginine into urea and ornithineis catalysed by the enzyme arginase and the regenerated ornithine can re-enter the
mitochondria thus completing the urea cycle. It takes 3 molecules of ATP to produce one
molecule of urea but there is efficient recycling of substrates and the by-product of 2 NADH
molecules from the conversion of glutamate to NH4+ and α-ketoglutarate and the recycling offumarate into malate can regenerate ATP. In effect the urea cycle releases slightly moreenergy than it consumes. In contrast the production of uric acid is a relatively complex andenergy expensive process consuming 5 molecules of ATP.

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Note that the predominant site of uric acid synthesis in birds is the hepatocyte and that
xanthine oxidase is an important cytoplasmic enzyme that is required first for the conversionof hypoxanthine to xanthine and then for converting xanthine to uric acid. Presumably avian
hepatocytes have high concentrations of this enzyme so it may well be that measurement ofplasma xanthine oxidase activity could be a sensitive and specific measure of hepatocellular
damage in birds.

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The Urea Cycle in Birds
It is important to note that birds do not lack any of the urea cycle enzymes and arginine, anessential amino acid in birds, can still be broken down by arginase to form urea. However,avian arginase is predominantly mitochondrial and not cytoplasmic as in mammals and thehighest concentrations occur in the kidney rather than the liver (Traniello et al 1975;
Kadowaki et al 1976; Kadowaki and Nesheim 1978). Avian arginase can be upregulated inbirds fed high protein diets and is inhibited by ATP so when energy is not limited urea is notproduced (Ruiz-Feria et al 2001; Koutsos et al 2001). In low ambient temperatures some birds
may conserve energy by increasing urea excretion and lowering uric acid excretion,
hummingbirds can even excrete up to 50% of waste nitrogen as ammonia provided that water
intake is not limited (Preest and Beuchat, 1997; van Tets et al 2001; Roxburgh and Pinshow
2002; McWhorter et al 2003).
In birds and reptiles most of the amino nitrogen and all of the purine nitrogen is excreted asuric acid (mainly by the liver) which at physiological pH forms soluble salts (urates) withammonia, Na+, or K+ ions. The molecule is relatively insoluble and this is a relatively risky
property for a waste product that has to be transported in the plasma from the liver to thekidney. Once it reaches the kidney uric acid is actively excreted by the tubular epithelial cells.
Most birds excrete about 80% of renal nitrogen as dihydrates of uric acid in a supersaturated
colloidal suspension with the remainder excreted as urea or ammonium which enters the urine
by glomerular filtration. Avian urine contains about 5 mg/mL of protein which helps, at a
metabolic expense, to maintain uric acid in colloidal suspension. These can be seen
microscopically as spheres of variable size but usually measuring 1-2 µm in urine and faecal
wet-preps. The spheres are made of lamellated colloidal material that sequester Na+ and K+
and which does not contribute to the urine osmotic pressure. The osmolality of the carrier fluid
component is largely due to Na+, K+ and Cl- . So this is whyurine specific gravity measurements are not a reliableindicator of “urine concentration capacity” in birds. Also
during times of dehydration, the urine can be refluxed fromthe cloaca into the colon for further water reabsorption. In
a bird that is polyuric it is worth checking the faeces forevidence of retrograde urine reflux by looking for urate
spheres in faecal wet-preps and they can also be seen incaecal contents, in those birds that have caeca (Roberts andBaudinette 1984).
Avian Renal Anatomy
For a comprehensive review of the comparative renal
anatomy of invertebrates and vertebrates see Holz andRaidal (2006). In birds, the kidneys lie symmetrically in therenal fossae of the synsacrum and extend as far as the lungs
cranially and to the end of the synsacrum caudally (Getty
1975). They are covered by a thin peritoneal serosa except
in extremely obese birds are surrounded by invaginations of
the abdominal airsac. The kidneys of birds are relatively
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larger than the kidneys of mammals and comprise 1-2.6% of avian body weight compared toonly 0.5% of mammalian body weight. Each kidney is divided into cranial, middle and caudal
divisions or lobes that are supplied by major blood vessels although in most passerines the
middle and caudal lobes are fused. In other species such as herons, puffins and penguins there
may be fusion of the left and right caudal lobes. Within each renal lobe there are 13 to 17
lobules, separated by interlobular veins.
Classical regions of renal cortex and medulla can be difficult to identify grossly in each lobe
because cortical-type tissue predominates but medullary cones can be identified histologically.
Each medullary cone receives collecting ducts from several adjacent lobules and the collecting
ducts coalesce to form medullary collecting ducts. These ducts then combine from several
adjacent lobules into a single cone shaped collecting duct and the lobules that drain into thisduct together comprise the renal lobe. These large collecting ducts coalesce to form the ureter
which is thus branched to service each medullary cone. The avian kidney thus resembles aseries of ice-cream cones lined up in parallel rows.
The ureter lies on the ventral surface of the kidney inassociation with the blood vessels, except in the
cranial division where it is embedded into theparenchyma. Distally, the ureter empties into theurodeum. There is no urinary bladder to store urine
instead much of the fluid is refluxed into the
coprodeum and from there into the lower alimentarytract. The one exception is in the ostrich whereby the
coprodeum does not receive faeces but insteadfunctions like an absorptive reptilian-like urinary
bladder with final modification of urinary solutes
occurring here. This is facilitated by a welldeveloped recto-coprodeal sphincter. Ostriches thus
can pass 2 types of droppings, one containing faeces
and one containing just urine (Deeming 1999).
Birds have two types of nephrons (Dantzler 1985).
The cortical nephron is similar to the reptilian
nephron because it lacks a loop of Henle, has ashort intermediate segment and is oriented
perpendicular to the collecting duct. The medullary
nephron has a loop of Henle inserted between theproximal and distal tubule and is similar to
mammalian nephrons being arranged parallel to thecollecting ducts. In the different species proportions
vary from 10% mammalian-type nephrons in
Gambel’s quail (Callipepla gambelii) up to 30% in
European starlings (Sturnus vulgaris). The
appearance of a loop of Henle means that birds, likemammals, can produce urine that is hypertonic
compared with blood.
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The kidney is provided with arterial blood via the cranial, middle and caudal renal arteries,
which provide blood to the cranial, middle and caudal kidney lobes respectively. These branch
to form intralobular arteries, which give rise to the afferent arterioles. The efferent arterioles
empty into the peritubular capillary plexus, which drains into the intralobular veins.
The cranial and caudal renal portal veins form a ring that encompasses both kidneys by joining
the external iliac and caudal renal veins. Venous blood enters this ring via the internalvertebral venous sinus, the caudal mesenteric vein, external iliac veins, ischiadic veins, andinternal iliac veins. The afferent renal branches leave this ring and penetrate the renalparenchyma where they become the interlobular veins, which drain into the peritubular
capillary plexus. From here blood enters the intralobular veins, efferent renal veins and finallythe cranial and caudal renal veins. These open into the common iliac vein (Canny 1998).
The renal portal valve is situated within the common iliac vein. When this valve is open bloodis diverted away from the kidneys into the caudal vena cava, and when it is closed blood isshunted through the kidneys. The valve is inhibited by adrenaline and stimulated byacetylcholine (Benson and Forest 1999).
Avian Renal Physiology
At first reckoning avian kidneys seem to have a limited capacity to concentrate urine
compared to mammals. There are two types of nephron, each composed of a glomerulus anda tubular system. Cortical or reptilian type nephrons (RTNs) are the main type (60 to 90%)
and they lack a loop of Henle. Juxtamedullary or mammalian type nephrons (MTNs) are lessnumerous, they possess a loop of Henle with thick and thin limbs; convoluted proximal anddistal tubules; and are arranged parallel to each other, their loops of Henle are bound with thevasa recta into medullary cones to allow for countercurrent exchange. Thus, urine can beconcentrated to some extent as it passes through the loop of Henle. In contrast RTNs are notarranged in parallel and are confined to the renal cortex, they can only produce urine which
is isotonic or hypotonic to plasma. However, all collecting ducts pass through a medullary
cone in their path towards a ureteral branch, so that urine can be concentrated to some extent,
regardless of which nephron it originated from. Desert-dwelling species generally have more
MTNs (up to 40%) than birds with ready access to water. Many desert and water bird species
also have a nasal gland which actively secretes salt. In these species the nasal gland is the
major site of sodium ion secretion. Sea-birds can survive by drinking salt water and may
refuse to drink fresh water.
Individual avian nephrons have a low GFR compared to mammals but the number of nephrons
per kidney is much higher in birds so that overall GFR is similar. Normally more than 95%
of the water of the original filtrate is reclaimed by tubular reabsorption. Variations from thisare achieved by regulation of GFR or reabsorption both of which are controlled by AVT. AVT
release from the neurohypophysis is stimulated greatly by a rise in ECF osmolality but only
moderately by a decrease in ECF volume, such as due to haemorrhage. Considerable recent
research has been done to investigate the value of using AVP in mammals with hypovolaemic
shock (Lurie et al 2002; Voelckel et al 2003). In birds that have experienced blood loss or
injury AVT or AVP may prove to be a treatment for restoring blood pressure and improving
survival rates. This is because AVT release from the neurohypophysis is stimulated greatly
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by a rise in ECF osmolality but only moderately by a decrease in ECF volume, such as due
to haemorrhage. Endotoxin induced pyrexia also significantly increases circulating AVT
concentrations in ducks (Gray and Maloney 1998) which led to speculation that it might havesome antipyretic action. Alternatively such elevations might be involved in stimulating thepituitary-adrenal (PA) axis. As in some mammals (Oritz et al 2003) it is noteworthy that AVP
is a potent stimulator of the PA axis in pigeons (Westerhof et al 1996) and it might prove to
be a safer way of increasing circulating endogenous corticosterone concentrations as analternative to exogenous glucocorticoids in those clinical situations where such treatment may
be warranted.
It is also worth noting that AVT is also responsible for controlling ovipositioning in hens withthe highest concentrations associated with the onset of uterine contractions. In this respect
AVT does the function of mesotocin which is the avian equivalent of oxytocin (Goldstein and
Skadhauge 1999).
The avian nephron has a juxtaglomerular complex and with salt and volume depletion thisreleases renin to stimulate the conversion of angiotensin-I to angiotensin-II which promotes
aldosterone mediated Na+ absorption, K+ excretion, decreased GFR and decreased urine flow.
Unlike in mammals the alternative release of aldosterone from the adrenal gland is notstimulated directly by elevations in blood K+. Birds also produce atrial natriuretic peptide
which acts to increase Na+ excretion.
The renal-portal system is a feature which birds share with reptiles (Goldstein and Skadhauge1999). It consists of a ring of veins which receive blood from the pelvic limb, colon and someof the structures in that region. The renal-portal ring is connected to the hepatic portal system,
the caudal vena cava and the intervertebral venous sinuses. The renal-portal system isseparated from the systemic circulation by a valve which is innervated by adrenergic andcholinergic fibers. When the valve is closed it prevents blood from directly entering the caudal
vena cava and therefore most of the blood enters the kidney or the hepatic portal system.
Much of the blood flows into the kidneys, where it mixes with arterial blood from the efferent
glomerular arteriole and participates with perfusion of the peritubular network but does not
supply the glomeruli. Up to two thirds of the blood supply to the kidney comes via the renal
portal system and up to 50% of renal blood flow can come from the ischiac and external iliac
veins (Goldstein and Skadhauge 1999).
In response to hypovolaemia, shock or with sympathetic stimulation (ie flight or fightresponse) the valve opens and blood is diverted into the vena cava. The plasma osmolality
rises and stimulates AVT which causes constriction of the afferent glomerular arterioles of the
RTNs. Thus the nephrons with the least capacity to concentrate urine are no longer
functioning. The shunting of blood to the peritubular network, allows the kidney to continue
excreting uric acid even though the GFR is greatly reduced. The MTNs, not all of which arefunctional during normal hydration are recruited so that glomerular filtration occurs in thosenephrons best capable of producing concentrated urine.
The high protein diet of carnivorous birds such as raptors and penguins leads to them having
higher reference blood uric acid ranges and postprandial elevations can also occur. Avian
urine is usually acidic because there is very efficient reabsorption of bicarbonate (Goldstein
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95and Skadhauge 1999).
Dehydration usually does not notably elevate blood uric acid concentrations until GFR isdecreased to the point that uric acid is not able to be flushed through the nephron. Dehydration
can be difficult to assess in birds because even in closely related some species the primaryeffect may be haemoconcentration or a rise in plasma osmolarity. In one study that compared
the effects of water deprivation between a desert adapted quail species (stubble quail) and aclosely related but wet grassland adapted quail species (king quail) the desert adapted species
was better able to cope with dehydration in terms of being able to maintain normal plasma
osmolarity but still had evidence of haemoconcentration (Roberts and Baudinette 1984). The
king quail on the other hand suffered considerable weight loss associated with a 20% rise inplasma osmolarity after a much shorter period of water deprivation (Table 1) and could notsurvive even when green food was supplemented in the face of total water deprivation.
Stubble quail, on the other hand, were able to survive and maintain body weight without theavailability of drinking water, providing supplementary green food was provided.
Table 1.
The effects of water deprivation on body weight and plasma
ionic concentrations in stubble quail (Coturnix pectoralis) and king quail(Coturnix chinensis) fed seed only for 20 days (Roberts and Baudinette 1984)

Days without water
Body weight
Plasma osmolarity
PCV
Plasma ClPlasma Na+
Plasma K+

Stubble quail (n=8)

King quail (n=16)

20
85.6
101.2
115.5
100
115.8
134.8

10
80.5
119.9
102.1
115.9
96.6
127.4

* Note that final values are expressed as a percentage of original values.
The kidneys, intestinal tract, salt glands, skin and respiratory tract all contribute toosmoregulation in birds.
Conclusion
The avian renal system is perhaps the most divergent from mammals and the underlying
physiology and biochemistry of uricotely needs to be understood by the avian clinician inorder to investigate the pathophysiology of renal failure. Mammalian concepts such as prerenal, renal and post-renal azotaemia may not be applicable to birds because they have unique
physiological mechanisms that are counter-intuitive to such paradigms. In most cases ofhyper-uricaemia in birds the lesion will reside in the kidney.

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