BIO 554/754
Ornithology

Urinary System, Salt Glands, and Osmoregulation

The role of bird kidneys, like the kidneys of other vertebrates is filtration, excretion or secretion, and absorption. They filter water and some substances from blood, as waste products of metabolism and ions, which are voided in the urine. Kidneys also play an important role in conserving water and reabsorbing needed substances (like glucose).

Avian kidneys
http://137.222.110.150/restricted/gallery/album181

The urinary organs of birds consist of paired kidneys and the ureters, which transport urine to the urodeum of the cloaca. Avian kidneys are divided into units called lobules. Each lobule has a cortex (outer area) and medulla (or medullary cone). In terms of volume, the avian kidney is primarily cortex (71-81%), plus a relatively small medulla (range 5-15%) & blood vessels larger than capillaries (range 10-13%). The functional unit of the kidney is the nephron. Nephrons filter the blood plasma to eliminate waste products, but, in doing so, must not lose needed materials (like glucose) or too much water. Blood enters nephrons via small arteries called afferent arterioles. This blood enters the glomerulus (a collection of capillaries) under high pressure and 'filters' through the walls of the capillaries and the walls of a surrounding structure called a capsule. The filtrate that moves from the glomerular capsule into the proximal tubules is basically plasma without protein (the protein molecules are too large). That filtrate, therefore, contains lots of important substances. In the proximal convoluted tubules, those needed substances such as vitamins and glucose are reabsorbed into the the blood. Even sunbirds, with a diet rich in glucose, are able to reabsorb almost all (98%) of the glucose that filters into the kidney tubules (McWhorter et al. 2004).

Nephron components: 1 = glomerular capsule, 2 = glomerulus, 3 = afferent arteriole, 4 = efferent arteriole, 5 = proximal convoluted tubule, 6 = distal convoluted tubule, 7 = collecting duct, 8 = loop of Henle, & 9 = peritubular capillaries (or vasa recta). Plasma is filtered from the glomerular capillaries into the glomerular capsule. Filtrate then travels through the tubules and loop of Henle before entering the collecting duct.

Glomeruli of an Anna's Hummingbird. In some cases (A), the glomerular capillary is twisted
into a spiral (scale bar = 17 micrometers), but more typically (B) is bent into one or two
loops that fold back on themselves (scale bar = 20 micrometers). From: Beuchat et al. (1999).

Anna's Hummingbird 

Reabsorption of materials from the proximal convoluted tubule back into the blood.
Image source: http://www.uic.edu/classes/bios/bios100/lecturesf04am/lect21.htm

Avian nephrons are also involved in maintaining water balance and this process involves the loops of Henle in the medulla of the kidney.

Image from Sherwood et al. (2005).

The medullary cones include the loops of Henle and collecting ducts of nephrons plus a number of capillaries called the vasa recta.
The avian renal medulla is cone shaped because the number of loops of Henle decreases toward the apex of the medullary cones.

A: scanning electron micrograph of a methyl methacrylate cast of the collecting ducts in a single medullary cone
of a quail kidney. Arrows show points of convergence of collecting ducts. Note that the collecting ducts coalesce at
distinct levels within the cone structure. B: scanning electron micrograph of a methyl methacrylate cast of the pattern of
nephron loops within an avian medullary cone (Gambel's Quail). Arrows show the turning points of looped nephrons. Note that
the loops of Henle turn at differing depths within the medullary cone (Image from Casotti et al. 2000).

Avian kidneys have two kinds of nephrons. The reptilian-type, with no loops of Henle are located in the cortex, and the mammalian-type with long or intermediate length loops, are located in the medulla. In birds, only a small percentage of nephrons (10-30%) contain a loop of Henle (i.e., looped nephrons).

Most loops of Henle are rather short and the lengths of the thin limb and prebend
segment vary among nephrons. The length of the thin limb of Henle is greater in longer nephrons,
and the length of the prebend segment is independent of the length of the loop of Henle (Casotti et al. 2000).

Other than mammals, birds are the only vertebrates that conserve body water by producing urine osmotically more concentrated than the plasma from which it is derived. However, the ability of birds to concentrate urine is limited compared to mammals. Typically, water-deprived birds produce urine that is 2.0-2.5 times more concentrated than plasma, whereas some mammals can produce urine 20-25 times more concentrated than plasma. This 'concentrating capacity' resides within the medullary cones, where a countercurrent multiplier system is located. Solutes are actively transported out the ascending limb of the Loop of Henle (see diagram below), where they become concentrated in the medulla. In birds, sodium chloride is the solute that makes up the major portion of the osmotic activity in the medullary cones. When urine passes throughout the osmotic gradient in the medulla, water leaves the tubules by osmosis and the urine become concentrated. Because only the looped nephrons contribute to the intramedullary osmotic gradient, the presence of loopless nephrons may limit the ability of the kidneys to produce hyperosmotic urine. Thus, the concentrating ability of avian kidneys is more limited than in mammals.

Source: http://faculty.plattsburgh.edu/thomas.wolosz/turbinates.htm

Nasal respiratory turbinates are complex, epithelially lined structures in nearly all birds (and mammals) that act as intermittent countercurrent heat exchangers during respiration. Respiratory turbinates also allow birds to conserve significant amounts of water (by helping to 'dehumidify' air during exhalation).

How do birds drink?-- Birds generally drink by what's called 'dipping and tipping' (below) or by suction drinking.. Within each of these two main categories, however, there are several kinds of mechanisms. For example, water is taken into the mouth by scooping water with the lower beak in cockatoos (Cacatuinae). Mallards drink using a complex interplay of capillary action and pressure changes in different areas of the mouth. Among the suction drinkers, parakeets ladle water with the tip of the tongue and some parrots drink with a suctioning action. Pigeons and doves, on the other hand, use a "double-suction mechanism" in which capillary action is responsible for bringing water between the slightly gaping tips of the beak and then the tongue acts as a piston to pump the water into the pharyngeal cavity.

Drinking by a Bengalese Finch. Water runs between the beak tips as a result of adhesion and capillary action.
The bill then tips up and that, along with tongue movements, moves water into the pharynx (Heidweiller and Zweers 1990).

 
Sandhill Crane drinking

 
Mourning Dove drinking
(notice that doves don't have to tip their heads up like most other birds)

 
Ostriches drinking

In the avian loop of Henle, NaCl is transported out of the
ascending limb and this increases the solute concentration
in the medulla (as indicate the the numbers; the higher the number the
higher the solute concentration (almost entirely NaCl). When water
moves through the collecting duct or tubule, it can then be reabsorbed by
way of osmosis (Figure from Kere 1999).

Left: A proposed model for urine concentration in the mammalian-type nephron of quail Coturnix coturnix, showing
transport of NaCl and water in various nephron segments. NaCl is actively exported out of the thick ascending limb (TAL)
and some re-enters the descending limbs (DLs) by simple diffusion without the osmotic accompaniment of water (because the membrane is
not permeable to water); the NaCl is recirculated for maximum operation of a single-effect countercurrent multiplier system. Right: Hypothetical cascade
transport of NaCl in the medullary cone, showing that more NaCl export occurs near the tip of the cone, which may enhance the osmotic gradient (Nishimura and Fan 2003).

THE SWEET CHALLENGE by Jane Qiu --The sugar found in floral nectars may be sweet, but it comes at a price. Birds that feed on nectar can consume a huge amount of fluid compared to their body weight. And the more dilute the nectar, the higher the volumes ingested. Although the birds derive nutrients and energy from nectar, they have to get rid of the large amounts of water taken in. Failing to do so can have devastating consequences. Palestine Sunbirds have somehow overcome the problems of life on liquid diet, so McWhorter et al. (2004) decided to examine how they dispose of their excessive water intake.

In the kidney, water is filtered out of blood by specialized structures called glomeruli, and some of the eliminated water is later reabsorbed in the nephron and collecting duct. The researchers set out to test how these processes respond to water intake in Palestine Sunbirds. Although following the birds around and measuring their nectar intake is difficult, McWhorter and his colleagues came up with an ingenious solution to the problem. They discovered that the birds adjust the amount they consume according to the concentration of sucrose solutions they are fed: the more dilute the solution, the higher the volumes ingested. In this way, the team could vary the bird's water intake and measure the rates of renal filtration and reabsorption.

McWhorter explained that when the team began investigating this nectarivorous bird's approach to fluid management, it was thought that renal filtration changes according to water status; decreasing in response to water shortage, but increasing only moderately as the birds take on water. But this was based on ideas developed for birds that do not regularly cope with a large intake of water. McWhorter and his team also knew that when the birds are on dilute diets, water is shunted through the gut without being absorbed. So, how would Palestine Sunbirds' kidneys cope?

The team found that renal filtration is not exceptionally sensitive to water loading in sunbirds; it increased only slightly in response to a dramatic decrease in sucrose concentration. On the other hand, the fractional water reabsorption - a measure of the proportion of the eliminated water that is reabsorbed by the kidney - dropped significantly when the birds were on the most dilute diet. The sunbirds' kidney responds to the elevated water levels by decreasing reabsorption, rather than by raising the filtration rate.

The team also found that the glucose and osmotic concentrations in the final excreted fluids were significantly lower than those in the ureteral fluids released by the kidney. Because the gut and urinary tracts of birds join at the cloaca, the researchers conjecture that the dietary water that shunts through the gut might have diluted the ureteral fluids. They conclude that Palestine Sunbirds deal with large amounts of water intake by not absorbing it in the first place.

From an economical standpoint this makes sense, as eliminating water by increasing renal filtration rate can be energetically costly for birds. Sugar and other metabolites lost during filtration may only be retained by reabsorption, possibly overwhelming the kidney's ability to prevent solute loss. But how the gut could absorb nutrients without taking in dietary water is still a mystery, as the two processes normally come hand in hand (Click on the photo to check out Peter Jones' website).

 
Sunbirds and other birds feeding on nectar from Aloe Erythrina (Erythrina livingstoniana) flowers.

An important part of the diet of all birds is protein. Proteins are composed of subunits called amino acids, and those amino acids are sometimes used as a source of energy or are converted into fats or carbohydrates. When amino acids are used for energy or converted to fats or carbohydrates, the amine (NH₂) group must be removed. These amine groups are toxic and must be eliminated. Some organisms excrete these nitrogenous wastes as ammonia (e.g., aquatic animals like bony fishes and amphibians) or urea (e.g., terrestrial amphibians and mammals). Birds (and reptiles) excrete these wastes primarily as uric acid. Although excreting nitrogenous wastes as uric acid has its advantages (e.g., not very toxic, not soluble in water so it can be excreted without using lots of water, and it can be stored in eggs without damaging embryos), uric acid is a more complex molecule than either ammonia or urea and synthesizing it requires more energy

Source: http://faculty.clintoncc.suny.edu/

The homeostasis of fluid and ions in birds involves several organ systems and is a more complex phenomenon than in other vertebrates. In birds, the kidneys and lower gastrointestinal tract (cloaca, rectum, and ceca) are involved in the regulation of extracellular fluid composition. Many birds also have functional salt glands (see below).

Osmoregulatory organs of birds (Hughes 2003).

As noted above, the avian kidney has a limited capacity for the conservation of body water and electrolytes via elimination of hyperosmotic urine. This low capacity to concentrate urine is not a liability because urine formed by the kidneys travels along the ureters into the cloaca. From there, it may move by retrograde peristalsis into the lowere intestine and cecae. Fluid from the upper gastrointestinal tract also enters the cloaca. Therefore, the cloaca receives an influx of water from the kidneys and the small intestine. The influx of water into the cloaca can be reabsorbed through the epithelium of the lower intestinal tract to maintain hydration. In the lower intestine and cecae, water and sodium chloride are reclaimed by the process of sodium-linked water reabsorption. In other words, positively-charged sodium ions are actively transported out of the intestine and negatively-charged chloride ions follow. Water then follows by osmosis. Uric acid is, as a result, concentrated and excreted as a relatively dry mixture with feces (Hildebrandt 2001).


Cloaca and lower intestine of an Ostrich (Duke et al. 1995)

The predominate form in which nitrogen is excreted by birds (uric acid) requires little water for excretion because it isn't very soluble in water. However, it does require a significant amount of protein to maintain it in a colloidal suspension in the urine (i.e., urine spheres; see photo below). The source of some of this protein is the plasma, as significant amounts pass through the glomerular filtration barrier. This protein is not lost because it is broken down when the urine enters the lower colon (Goldstein et al. 1999). In the colon, the composition of the urine is altered in several ways. The urine spheres are broken down, as is the protein that aided the formation of those spheres. Much of this degradation is accomplished by bacteria. The amino acids or peptides that result are either used by the bacteria or absorbed by the epithelium of the colon (Braun 1999).

"Urine spheres" showing differences in size.
Top photo = domestic chicken; Bottom photo = Wood Thrush.
(From: Casotti and Braun 2004).

Possible role of ceca in fluid & electrolyte homeostasis -- Because birds do not have a urinary bladder, the kidneys and lower gastrointestinal tract must function in concert to maintain fluid and electrolyte homeostasis. In birds, urine is conveyed to the cloaca, and moved by reverse peristalsis into the colon and digestive ceca. Digestive ceca have been well studied for non-passerine birds and have been shown to absorb substrates and water. The ceca of passerine birds have been suggested to be non-functional because of their small size. Three-dimensional reconstruction of the ceca of House Sparrows (Passer domesticus) from serially-sectioned tissue showed that the ceca have a central channel with a large number of side channels. Electron micrographs indicated that all of the channels are lined by epithelial cells with a very dense microvillus brush border as well as a region densely packed with mitochondria just below the brush border. It is possible that the row of mitochondria below the brush border is present to provide ATP to power substrate transport. Although the importance of small ceca for fluid homeostasis remains to be determined, these data suggest that the small ceca of passerine birds may function in fluid and electrolyte (e.g., sodium) homeostasis (Reyes and Braun 2005).

Light micrograph and electron micrographs of a House Sparrow cecum. A) A light micrograph of a cecum cut in sagittal section.
The image shows one central channel with a proximal opening to the colon (upper right of section). Side channels (arrows) can be seen branching
from the central channel. B) Higher power light micrograph of a cecum. The image illustrates the columnar cells that line the channels (bracket) with their
well developed brush border (arrow). C) Electron micrograph of a House Sparrow cecum. The image shows a portion of the epithelial cells that line channels
of the ceca. Evident is a dense microvillus brush border on the apical surface of the cells and tight junctions (TJ) between the cells. Just below the brush border is
a very dense layer of mitochondria (bracket). 7400 × (From: Reyes and Braun 2005).

The coordinated action of the kidneys, lower GI tract, and the salt glands (see below) in the regulation of fluid and ion balance is a classic example of the integration of organs required to maintain homeostatic balance. No single organ appears to have an outstanding capacity to conserve ions and water, but instead they all function in concert to maintain total body fluid homeostasis to allow birds to inhabit a wide range of environments (Braun 1996).

Modification of urine in lower GI tract of birds
(Source: http://eebweb.arizona.edu/courses/Ecol437/EldonBraun_Ecol%20lect%2004.pdf)

Arginine vasotocin (AVT; stored and released from the posterior pituitary) is considered the avian ADH (antidiuretic hormone). Circulating concentrations of AVT rise when birds are dehydrated, and infusion of the hormone in birds reduces urine production. In mammals, ADH enhances the permeability to water of the medullary collecting ducts. However, in birds, the mechanism of AVT remains unclear. One consistent action of AVT on the avian kidney is to reduce the rate of glomerular filtration. The consequent reduction in fluid flow through the renal tubules could lead to enhanced solute and water reabsorption from the renal tubules, processes that are sensitive to rates of solute delivery. Hence, an AVT-induced increase in fractional water reabsorption could be a secondary effect to the reduced GFR, rather than representing a direct action of the hormone on the renal tubules. On the other hand, several lines of evidence do suggest a direct action of AVT on the avian renal tubule. First, in some studies, the AVT-induced antidiuresis occurs, at least at low doses of hormone, with little or no change in GFR. Second, in house sparrows, a chemical analog of ADH was able to enhance the antidiuretic actions of AVT without any effect on the GFR. Thus the present findings are consistent with this growing body of evidence for a tubular action of AVT in birds (Goldstein et al. 1999).

Can birds be ammonotelic?? -- Most birds are thought to excrete nitrogen as uric acid and, therefore, are referred to as uricotelic. Uric acid is a relatively non-toxic nitrogen end product. It is relatively insoluble and hence excreted with little water. Uricotely, however, is costly. More energy is needed to excrete a unit of waste nitrogen as uric acid than as urea or ammonia. In contrast to uric acid, ammonia is highly soluble, cheap to synthesize, but fairly toxic. It can only be used as a nitrogenous waste by animals with high rates of water turnover that permit almost continuous elimination, such as in aquatic animals (Tsahar et al. 2005).

Preest and Beuchat (1997) suggested that it might be advantageous for birds that ingest large amounts of dilute, protein-poor nectar to shift from uricotely to ammonotely. Thus, ammonia can be voided rapidly, and the costs of synthesizing urates can be reduced. Preest and Beuchat (1997) called the shift from uricotely to ammonotely in hummingbirds `facultative ammonotely' In their study on Anna's Hummingbird (Calypte anna; see photo to the right), Preest and Beuchat concluded that these birds were facultatively ammonotelic. At low ambient temperatures and high water intakes, Anna's Hummingbirds excreted more than 50% of their total nitrogen excretion as ammonia (i.e. they became ammonotelic), whereas at higher ambient temperatures and lower food intake they were uricotelic). Thus, Preest and Beuchat (1997) proposed that high energy demands and high water fluxes favor ammonotely.

Subsequently, Roxburgh and Pinshow (2002) found that the Palestine Sunbirds also switched from uric acid to ammonia excretion under some conditions. However, Roxburgh and Pinshow (2002) noted that in sunbirds with high water intake, the concentration of urate was higher in the ureters (the tubes that carry urine from the kidneys to the cloaca) than in excreta. They argued that ammonotely in Palestine Sunbirds was only 'apparent' because it was not a result of excessive excretion of ammonia, but rather the result of a reduction in excreted urate resulting from post-renal modification of urine. Recently, Tsahar et al. (2005) then found that Yellow-vented Bulbuls (Pycnonotus goiavier), a frugivorous species, appeared to switch from uricotely to ammonotely when they ingested large amounts of water and when their protein intake was low. These authors, like Roxburgh and Pinshow (2002) found that protein concentration was lower in excreta than in ureteral urine, and hypothesized that some of the protein associated with urate spheres was digested in the lower intestine and recovered. Why would it be advantageous for birds to recover a nitrogenous metabolic waste? Although uric acid is considered primarily a nitrogenous waste, it also has a major function as a powerful antioxidant in both birds and mammals (Tsahar et al. 2005).

So, can birds be ammonotelic? Apparently, yes. In some cases, as with Anna's Hummingbirds, ammonotely may be a response to the ingestion of lots of water (facultative ammonotely). In other cases, ammonotely may simply be 'apparent', with urine produced by the kidneys being urotelic but the actual excreta being ammonotelic because of reabsorption of uric acid in the lower intestine or colon prior to defecation.

Because the kidneys of birds cannot produce a hypertonic urine (with lots of ions like sodium), the excretion of excess salt is a potential problem. Even quicker than humans, birds would be severely dehydrated after drinking saltwater and ingesting salty food. However, many species of birds, especially marine birds and shorebirds, can drink seawater as their only source of water. This is possible because these birds have another way (other than the kidneys) to eliminate excess salt - salt glands.

Salt glands of birds likely evolved from nasal glands of reptiles, probably in the late Paleozoic. They lie immediately under the skin in supraorbital depressions of the frontal bone in the skull of Charadriiform birds, but in other groups they may be located above the palate or within the orbit of the eye. Skulls of fossil birds, Ichthyornis and Hesperornis, have similar depressions, suggesting these birds lived in marine habitats. The salt glands of marine birds (and some falconiform and desert birds) secrete excess NaCl via the salt glands using less water than is consumed, which generates free water (Hughes 2003).

Hesperornis skull (note depression above eye socket where salt gland would be located)

Salt glands have been reported in several avian orders (Spheniciformes, Procellariformes, Charadriiformes, Pelecaniformes, Anseriformes, and Phoenicopteriformes). Even though most studies of osmoregulation in birds have been conducted with marine taxa, nasal secretions are not to be restricted to these species. The presence of functional salt glands has been documented in several terrestrial orders. For example, Roadrunners (Geococcyx californianus) and Savanah Hawks (Heterospizias meridionalis), have active salt glands and can produce hypertonic secretions in response to their protein-rich diets. Although these species are not stressed by high saline load, the active secretions of salt gland allows them to minimize water losses. Other desert birds, such as the Sand Partridge (Ammoperdix heyi) and the Ostrich (Struthio camelus), have functional salt glands that are stimulated in response to high temperature. Thus, salt glands are not restricted to birds that live in saline or maritime habitats, but are also present in some terrestrial forms that consume little water (Sabat 2000).

Salt glands have a system of countercurrent blood flow to remove and concentrate salt ions from the blood. The paired, crescent-shaped glands each contain several longitudinal lobes approximately 1 mm in diameter and each lobe contains a central duct from which radiate thousands of tubules enmeshed in blood capillaries. These tiny capillaries carry blood along the tubules of the gland, which have walls just one cell thick and form a simple barrier between the salty fluid within the tubules and the bloodstream. It is here that salt excretion occurs.

Source: http://www.kcl.ac.uk/ip/christerhogstrand/courses/hb0223/water&io.htm

When a bird drinks seawater, sodium enters the blood plasma from the intestine and the solute concentration of the blood plasma increases.
This causes water to move out of cells (osmosis), increasing the extracellular fluid volume (ECFV). The increases in blood plasma solute concentration
and ECFV stimulate salt gland secretion (Hughes 2003).

It has been proposed that the enzyme Na⁺-K⁺-ATPase provides energy (by breaking down ATP) for the co-transport of
Na⁺ and Cl^- through the folded basal membranes. Chloride then moves passively through the apical membrane and Na⁺ flows
between the principal cells, through the tight junctions and into the tubular lumen. Water movement may follow solutes via the cellular
or paracellular route to yield a hypertonic fluid composed primarily of NaCl together with smaller amounts of K⁺ and traces of other ions (Butler 2002).
Black sphere = active transport; red sphere = cotransport of sodium, potassium, and chloride ions.

Literature cited

Beuchat, C. A., M. R. Preest, and E. J. Braun. 1999. Glomerular and medullary architecture in the kidney of Anna's Hummingbird. Journal of Morphology 240:95-100.

Braun, J. 1996. An overview of osmoregulation in birds. Abstract - VI International Symposium of avian endocrinology. Chateau Lake Louise, Alberta, Canada.

Braun, E. J. 1999. Integration of organ systems in avian osmoregulation. Journal of Experimental Zoology 283:702-707.

Butler, D. G. 2002. Hypertonic fluids are secreted by medial and lateral segments in duck (Anas platyrhynchos) nasal salt glands. Journal of Physiology 540.3: 1039-1046.

Casotti, G. and E. J. Braun. 2004. Protein location and elemental composition of urine spheres in different avian species. Journal of Experimental Zoology 301A: 579-587.

Kere, J. 1999. Kidney kinetics and chloride ion pumps. Nature Genetics 21:67-68.

McWhorter, T. J., C. Martínez del Rio, B. Pinshow, and L. Roxburgh. 2004. Renal function in Palestine Sunbirds: elimination of excess water does not constrain energy intake. J. Exp. Biol. 207: 3391-3398.

Nishimura, H. and Z. Fan. 2003. Regulation of water movement across vertebrate renal tubules. Comp. Biochem. Physiol. - Part A 136: 479-498.

Preest, M. R. and C. A. Beuchat. 1997. Ammonia excretion by hummingbirds. Nature 386:561 -562.

Reyes, L. and E. J. Braun. 2005. The functional morphology of the english sparrow cecum. Comparative Biochemistry and Physiology - Part A: Molecular & Integrative Physiology 141: 292-297.

Roxburgh, L. and B. Pinshow. 2002. Ammonotely in a passerine nectarivore: the influence of renal and post-renal modification on nitrogenous waste product excretion. J. Exp. Biol. 205:1735 -1745.

Sabat, P. 2000. Birds in marine and saline environments: living in dry habitats. Rev. Chil. Hist. Nat. 73:.401-410.

Sherwood, L., J. Klandorf, and P. Yancey. 2005. Animal physiology - from genes to organisms. Brooks/Cole, Pacific Grove, CA.

Tsahar, E., C. Martínez del Rio, I. Izhaki, and Z. Arad. 2005. Can birds be ammonotelic? Nitrogen balance and excretion in two frugivores. J. Exp. Biol. 208: 1025-1034.

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