Available online at www.sciencedirect.

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Comparative Biochemistry and Physiology, Part A 149 (2008) 246 254

www.elsevier.com/locate/cbpa

Review

Adaptive strategies for post-renal handling of urine in birds

Gary Laverty a,, Erik Skadhauge b
a

Department of Biological Sciences, University of Delaware, Newark, DE 19716, USA

Department of Basic Animal and Veterinary Sciences, Faculty of Life Sciences, University of Copenhagen, DK-1870 Frederiksberg C, Denmark
Received 23 August 2007; received in revised form 15 January 2008; accepted 15 January 2008
Available online 18 January 2008

Abstract
Birds are a diverse vertebrate class in terms of diet and habitat, but they share several common physiological features, including the use of uric
acid as the major nitrogenous waste product and the lack of a urinary bladder. Instead, ureteral urine refluxes from the urodeum into the more
proximal coprodeum and portions of the hindgut (colon or rectum and ceca). This presents a potential problem in that hyperosmotic ureteral urine
in contact with the permeable epithelia of these tissues would counteract renal osmotic work. This review describes and provides examples of
different strategies used by avian species to balance renal and post-renal changes in urine composition. The strategies described include: 1. a
reptilian mode, with moderate renal concentrating ability, but high rates of post-renal salt and water resorption; 2. the mammalian strategy, in
which the coprodeum effectively functions like a mammalian urinary bladder, preserving the osmotic concentrating work of the kidney; 3. an
interaction strategy, in which post-renal transport processes are hormonally regulated in order to optimize renal function under varying conditions
of salt or water stress; 4. the salt gland strategy seen in marine or estuarine birds with functional salt glands, in which post-renal transport
mechanisms are used to conserve urinary water and to recycle excess NaCl to the nasal salt glands. Finally, we also describe some features of an
as-yet unstudied group of birds, the birds of prey. At least some species in this group are relatively good renal concentrators, and would be
predicted to have post-renal mechanisms to preserve this work. This new synthesis illustrates the marked diversity of adaptive mechanisms used
by avian species to maintain osmotic homeostasis.
2008 Elsevier Inc. All rights reserved.
Keywords: Avian lower intestine; Cloaca; Domestic fowl; Emu (Dromaius novae-hollandiae); Kookaburra (Dacelo gigas); Nasal salt gland; Osmoregulation; Ostrich
(Struthio camelus)

Contents
1.

Introduction . . . . . . . . . . . . . . . . . . . . .
1.1. The reptilian strategy . . . . . . . . . . . .
1.2. The mammalian strategy . . . . . . . . . .
1.3. The interaction strategy (granivorous birds)
1.4. The salt gland strategy . . . . . . . . . . . .
1.5. Birds of prey . . . . . . . . . . . . . . . . .
2. Summary . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . .

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246
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251
252

1. Introduction

Corresponding author. Tel.: +1 302 831 8180; fax: +1 302 831 2281.
E-mail address: Laverty@udel.edu (G. Laverty).
1095-6433/$ - see front matter 2008 Elsevier Inc. All rights reserved.
doi:10.1016/j.cbpa.2008.01.014

Birds and some reptilian groups excrete the majority of their

nitrogen waste products as uric acid/urate salts. This enables
these phyla, in the absence of a urinary bladder, to store ureteral

G. Laverty, E. Skadhauge / Comparative Biochemistry and Physiology, Part A 149 (2008) 246254

urine in the lower part of the gut and upper part of the cloaca: the
colon (rectum) and coprodeum, respectively. These organs have
an absorptive and permeable epithelium, bounded by a single
layer of transporting columnar cells (Skadhauge, 1981; 1993;
Dantzer, 1989; Clauss et al., 1988; 1991; Elbrnd et al., 1991,
1999; Laverty and Skadhauge, 1999; Laverty et al., 2001;
Goldstein and Skadhauge, 2000; Laverty et al., 2006). In spite
of this, the uric acid/urate salts can be refluxed into the lumen
without initially adding to the osmotic pressure of this compartment. This is because in the kidney the urates, with low
solubilities, form amorphous concrements (spheres) in supersaturated colloidal suspension, thus not contributing significantly to the osmolality of the ureteral urine (Skadhauge, 1981;
Braun, 2003). Studies suggest that these urate spheres are
degraded in the lower intestine by resident microbial populations, and that much of the protein associated with the spheres is
reabsorbed, possibly in the form of peptides and amino acids
(Barnes and Impey, 1974; Lind et al., 1980; Mortensen and
Tindall, 1981a,b; Campbell and Braun, 1986; Moret et al.,
1991; Boykin and Braun, 1996; Braun, 2003; Casotti and Braun,
2004). Retrograde peristalsis may also allow for movement of
urine into the paired ceca, which are highly developed in many
avian species (Dantzer, 1989; McLelland, 1989). Here, further fermentative degradation and substrate absorption may
take place, along with significant water absorption (Rice and
Skadhauge, 1982a; Thomas, 1982; Thomas and Skadhauge,
1989a,b). Some of the nitrogen derived from urate degradation
may be excreted as ammonium ions and some may be absorbed
in the ceca, thus allowing for further nitrogen recycling in the
lower intestine (Karasawa, 1999).
This mode of urine storage in the permeable lower intestine
may create problems however. The avian kidney, like the mammalian kidney, possesses a countercurrent multiplier system,
allowing formation of a urine hyperosmotic to plasma (Skadhauge, 1981; Goldstein and Braun, 1989; Nishimura, 1989). This
process is simpler in birds compared to mammals, since there is no
significant osmotic contribution from urea, and has been described in the form of a mathematical model (Layton et al., 2000).
In addition the degradation of urate spheres, described above, may
add to the osmotic load in the lower intestine. This poses an
osmotic challenge when birds are water deprived. Will the
hyperosmotic urine, when refluxed into the coprodeum and colon,
draw water from the plasma, thus counteracting the osmotic work

247

of the kidney (see Table 1 for a summary of urine concentrating

abilities of species discussed in this review)? Similarly, in water
replete or water-loaded birds, low urine osmolality might lead to
backflux of water into the plasma, across the lower intestinal
epithelium.
A survey of a variety of different avian species suggests that
there are four basic strategies that birds may use to overcome
this consequence of storage of ureteral urine in the lower intestine, in contact with an absorptive epithelium (Skadhauge,
1989). These strategies, to be described and exemplified below,
will be referred to as: 1.reptilian, 2. mammalian, 3. an interaction mode, and 4. salt-recycling (marine birds with salt
glands). In terms of NaCl and water conservation, the cloacal/
colonic sojourn of ureteral urine may be viewed as an afterburner effect, or a mechanism for post-renal modification of
urine. In this context, the reptilian solution implies limited
urinary concentrating ability with extensive absorption of ions
and water into the blood during the period of storage in the lower
intestine. The mammalian solution is the condition of no or very
minimal lower intestinal modification, analogous to the storage of
urine in the mammalian urinary bladder. The third strategy,
referred to as the interaction strategy, allows for varying degrees
of lower intestinal modification of the urine (Skadhauge, 1981),
which helps to offset osmotic water loss, but is also sensitive, at
least in some species, to dietary salt intake (Lind et al., 1980;
Skadhauge and Dawson, 1980; Skadhauge, 1981; Thomas and
Skadhauge, 1982; rnason and Skadhauge, 1991; Goldstein,
1993; Skadhauge, 1993). This pattern has been studied extensively, particularly in granivorous birds (vide infra). The final
strategy is characteristic of birds with functional salt glands, as
first hypothesized by Schmidt-Nielsen et al. (1963).
1.1. The reptilian strategy
Computer modeling by Skadhauge and Kristensen (1972)
suggested that an effective post-renal recovery of ureterally
excreted salt and water (allowing uric acid to be continuously
excreted) could exist, even with moderate renal concentrating
ability and consequently high rates of ureteral urine flow,
provided that the absorptive capacity for ions and water of the
lower intestine was large. This predicted strategy was observed
in the Australian emu, Dromaius novae-hollandiae, which has
the lowest urine to plasma osmotic ratio (1.41.5, Table 1)

Table 1
Urine concentrating abilities in selected species
Species

Strategy

Condition

UOsm

U/POsm

Reference

Emu

Reptilian

Water deprived

Ostrich
Domestic fowl
Galah
House sparrow
Domestic duck

Mammalian
Interactive
Interactive
Interactive
Salt gland

Glaucous-winged gull
Kookaburra

Salt gland
Bird of prey

Salt loaded
Water deprived
Water deprived
Water deprived
Acute salt load
Chronic salt load
Seawater acclimated
Water deprived

459
506
846
538
982
825
462
444
548
944

1.4
1.5
2.6
1.6
2.5
2.1
b1.5
1.4
1.6
2.7

Skadhauge, 1974a,b
Dawson et al., 1991
Skadhauge et al., 1995
Skadhauge and Schmidt-Nielsen, 1967
Skadhauge, 1974a,b
Goldstein and Braun, 1988
Skadhauge and Schmidt-Nielsen, 1967
Holmes et al., 1968
Goldstein et al., 1986
Skadhauge, 1974a,b

UOsm values are given in units of mOsm/kg water. U/POsm = urine to plasma osmotic ratio. Data for many of these species can also be found in Skadhauge, 1981.

248

G. Laverty, E. Skadhauge / Comparative Biochemistry and Physiology, Part A 149 (2008) 246254

encountered in a study of Australian birds (Skadhauge, 1974a).

Subsequent in vivo perfusion studies (Dawson et al., 1985) and
collections of ureteral urine, combined with dissection of the
lower intestine (Dawson et al., 1985, 1991; Skadhauge et al.,
1991) demonstrated that this species had a remarkable ten-fold
higher absorptive capacity than other birds, due to a particularly
large colonic absorptive surface area. This, in turn, is attributed
to a large degree of mucosal folding, resulting in a mucosal to
serosal surface area ratio of more than 5. This finding thus
confirms the existence of the reptilian strategy for avian
renalintestinal interaction, particularly notable for a species
adapted to arid conditions, yet with low renal concentrating
ability.
1.2. The mammalian strategy
This model would predict both a mechanism for separation
of feces and urine, and little or no post-renal modification of the
urine (although the bladder epithelia of some mammalian
species do transport ions and water to a limited extent (Lewis
and Diamond, 1976)). Furthermore, it would allow for excretion
of urine with a higher osmolal concentration, since osmotic
water loss could be minimized by an impermeable epithelium.
A species that at least partially fits this description is the African
ostrich (Struthio camelus). Birds of prey may also fit this model
(vide infra).
The ostrich has a very long colon (more than 11 m in the
adult male), which serves as a huge fermentation chamber with
production of short chain fatty acids (SCFA) (Skadhauge et al.,
1984b; Skadhauge and Dawson, 1999). The subsequent absorption of these solutes is secondarily coupled to colonic water
absorption, an important component of the ability of the ostrich
to survive without drinking (see Musara et al., 2002). However,
there is no retrograde movement of urine into the colon in this
species, due to the presence of a strong sphincter between
coprodeum and terminal colon (Skadhauge et al., 1995;
Skadhauge and Dawson, 1999). Ureteral (coprodeal) urine is
therefore voided separately from defecation of feces from the
terminal colon. Fig. 1 (Wari and Skadhauge, in preparation)
illustrates this process. The coprodeum seems to function,
therefore, as a separate compartment for the storage of urine
(i.e., like a bladder), thus fulfilling one of the predicted
criteria for the mammalian model. Furthermore, in its natural
arid or semi-arid environment, the ostrich is frequently exposed
to dehydrating conditions, and compensates for this with a welldeveloped renal concentrating ability, producing urine of approximately 800 mOsm (i.e., 500 mOsm hyperosmotic to
plasma, Table 1) (Skadhauge and Dawson, 1999).
More recently, the transport properties of the ostrich
coprodeum were studied in vitro by electrophysiological methods (Skadhauge et al., 2003). These animals (3 month chicks)
were first adapted to a low salt diet, but with free access to
deionized water. Somewhat surprisingly, the coprodeal tissue
was found to have a relatively low transepithelial resistance
(230 + 55 cm2, n = 5). There was also a significant shortcircuit current established across the tissue, the majority of
which could be attributed to amiloride-sensitive, electrogenic

Fig. 1. Schematic diagram of the ostrich (Struthio camelus) cloaca and lower
intestine. The 3 panels show the movement of feces and urine during rest (A),
defecation (B) and urination (C). Urine and feces are clearly separated due to the
presence of a well-developed sphincter between the terminal rectum and
coprodeum (plica recto-coprodealis). In A, urine is shown entering the urodeum
(U) from the ureters and then into the ventral part of the coprodeum, which
serves as the equivalent of a mammalian urinary bladder in this species. During
defecation, relaxation of the rectal-coprodeal sphincter allows feces to be
expelled (dark arrows, B) via the protodeum. Urination occurs by contraction of
abdominal muscles, pushing the urine out through the urodeum and proctodeum
(light arrows, C). Because the recto-coprodeal sphincter is closed, there is no
retrograde movement of urine and no mixing of urine with feces. Ph, phallus.
Illustration courtesy of C.N. Wari, Department of Veterinary Anatomy,
University of Nairobi (see also Skadhauge and Dawson, 1999).

sodium absorption, as well as a theophylline-stimulated chloride secretion current (Skadhauge et al., 2003). These transport
properties are very similar to those of the domestic fowl coprodeum (Choshniak et al., 1977; Thomas et al., 1980; Rice
and Skadhauge, 1982b; Clauss et al., 1988; rnason and
Skadhauge, 1991).
At first glance, the low electrical resistance, usually reflecting leaky tight junctions, and active transport of the
ostrich coprodeum seem to contradict the prediction of low
osmotic permeability for a bladder-like epithelium. However,
two factors may help to minimize osmotic water loss into the
coprodeum. First, the coprodeal surface (a cuboidal epithelium)
has only irregular folds and projects a relatively small surface
area, on a body mass basis (Skadhauge et al., 2003). Second, the
epithelium includes an unusually large proportion of mucussecreting goblet cells. It is considered that the secreted mucus
helps to establish a thick unstirred layer at the epithelial surface,

G. Laverty, E. Skadhauge / Comparative Biochemistry and Physiology, Part A 149 (2008) 246254

thus lowering the effective osmotic permeability and accounting

for the ability of this species to maintain a steep osmotic
gradient between coprodeal urine and plasma. To summarize,
the ostrich coprodeum effectively functions like a mammalian
urinary bladder in physically separating the urine and preserving osmotic work done by the kidney.
1.3. The interaction strategy (granivorous birds)
In the domestic fowl urine flows in a retrograde direction
from the ureteral openings into the coprodeum and colon, there
surrounding a central feces core (Skadhauge, 1981). In this
species, hens adapted to a low NaCl intake and subjected to
dehydration are able to recover most of the ureterally excreted
Na+ ions through an electrogenic sodium absorption process in
both colon and coprodeum (Lind et al., 1980; Thomas and
Skadhauge, 1982; Clauss et al., 1988; 1991; rnason and
Skadhauge, 1991; Elbrnd et al., 1991; Laverty et al., 2001). In
the colon, but not in the coprodeum, this sodium absorption is
accompanied by solute-linked water absorption (Bindslev,
1981; Rice and Skadhauge, 1982b). The hyperosmotic urine
that enters the coprodeum (see Table 1) is initially diluted by
osmotic flow of water from plasma into the gut lumen, but this
water and more is absorbed back into the blood in the colon, as
the solute-linked water flow overcomes the osmotic loss into the
coprodeum lumen. This sequence of events is depicted in Fig. 2.
The experimental work leading to this concept has been summarized in monographs by Skadhauge (1973, 1981) and in
several recent review chapters (Goldstein and Skadhauge, 2000;
Skadhauge, 1989, 1993). An almost identical pattern of postrenal urine modification is seen in the Australian parrot (galah),
Cacatua roseicapilla (Skadhauge, 1974b; Skadhauge and
Dawson, 1980). In fact this basic strategy may be very common
among avian species; dietary salt intake clearly affected the
pattern of transport in the lower intestine of house sparrows
(Goldstein, 1993).

Fig. 2. Schematic diagram of the cloaca and lower intestine of the domestic fowl
(Gallus gallus). Arrows indicate the direction of net transepithelial water and
electrolyte movements, as well as the retrograde movement of ureteral urine
from the urodeum to coprodeum and colon. Note the initial dilution of urine in
the coprodeum (entry of water) and the subsequent resorption of water via
solute-linked transport in the colon (and ceca). This pattern of post-renal urine
modification is representative of the interaction strategy, in which lower
intestinal transport rates are affected by dietary salt intake and aldosterone.
Retrograde transport and post-renal modification of urine also take place in
species such as the emu, representing the reptilian adaptation, as well as in
birds with salt glands, but with differences in the regulatory aspects of transport
(see text for details). Drawing taken from Skadhauge, 1981.

249

Quantitative computer simulations have outlined the important parameters of this interaction strategy (Skadhauge and
Kristensen, 1972). These include not only flow rate and
osmolality of ureteral urine and the osmotic permeability coefficient of the walls of the exposed segments of the gut, but also
the rate of sodium absorption and the coupling ratio for solutelinked water flow. The most variable of the gut transport parameters is the sodium absorption rate, which in both coprodeum and colon is regulated by the functional opening and/
or expression of an apical sodium channel. This channel has
been precisely characterized by electrophysiological methods
(Christensen and Bindslev, 1982) and has been studied extensively in the amphibian oocyte expression system (Asher
et al., 1992; Weber et al., 1992). When RNA from the lower
intestine of low salt-adapted hens was injected into oocytes, an
amiloride-blockable Na+ channel was expressed, but this
expression is not seen with RNA from high salt-adapted hens.
This channel is presumably the avian homolog of the epithelial
sodium channel (ENaC) found in a wide variety of tight epithelia. These studies and many others, both in vivo and in vitro
with Ussing chambers, have demonstrated that the activity and
expression of these channels are largely regulated by the plasma
levels of aldosterone (see Skadhauge, 1993; Laverty et al.,
2006), which in turn is controlled by the NaCl intake of the bird
(rnason et al., 1986; rnason and Skadhauge, 1991). It has
recently been shown that it is the Na+ intake per se that regulates
channel activity in the hen lower intestine (Bindslev et al., 1997;
Skadhauge, 1996).
When low salt-adapted hens are resalinated they rapidly lose
amiloride-sensitive electrogenic Na+ transport in the lower
intestine, and high salt-adapted hens show almost no amiloridesensitive transport (Thomas and Skadhauge, 1982; Clauss et al.,
1988, 1991; Laverty et al., 2001). In the coprodeum transport
activity is essentially abolished, and the tissue resistance markedly increases (Thomas and Skadhauge, 1982). However, in the
more proximal colon sodium transport continues, but is now
mediated by apical Na+-organic substrate cotransporters (Lind
et al., 1980; Thomas and Skadhauge, 1982; Clauss et al., 1991;
Laverty et al., 2001). Thus, Na+ currents can be induced in the
Ussing chamber by apical addition of hexoses (glucose or
galactose) and by several amino acids, a transport pattern reminiscent of the small intestine. Sugars and amino acids are likely
present in the lower intestine, derived from small intestine
influx, from breakdown of urate spheres, which contain protein
(Boykin and Braun, 1996; Braun, 2003; Casotti and Braun,
2004) and from fermentation processes (Annison et al., 1968;
Gasaway, 1976). The Na+-linked cotransport activity also supports significant solute-linked water absorption (Bindslev,
1981; Bindslev and Skadhauge, 1971; Rice and Skadhauge,
1982b; Goldstein, 1989).
Recent studies have shown that aldosterone injections, given
to hens undergoing acute resalination, can maintain the low salt
pattern of Na+ transport (i.e., ENaC channel activity) and suppress the activity and protein expression levels of cotransporters, specifically a form of the sodiumglucose luminal
transporter (SGLT) that has been detected in the hen colon
(rnason, 1997; Bindslev et al., 1997; Laverty et al., 2001).

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G. Laverty, E. Skadhauge / Comparative Biochemistry and Physiology, Part A 149 (2008) 246254

Thus, elevated aldosterone during salt deprivation induces a

switch in the mode of colonic sodium transport, from organic
substrate-linked cotransport on high salt intake to amiloridesensitive ENaC-mediated transport on low salt.
Decreased expression of colonic SGLT protein, and of
hexose transport have also been demonstrated in brush border
membrane vesicles (BBMV) derived from low salt acclimated,
compared to high salt acclimated hens (Barfull et al., 2001;
Garriga et al., 1999, 2001), and this effect is rapidly reversed
following acute resalination (Garriga et al., 2000). Interestingly,
SGLT mRNA was not affected by dietary salt intake, suggesting
that aldosterone effects on this cotransporter may be posttranscriptional (Barfull et al., 2001). Additional BBMV studies,
using blockers of angiotensin converting enzyme and mineralocorticoid receptor leave no doubt that aldosterone mediates
the decreased expression of SGLT during low salt acclimation
(Garriga et al., 2001). However, it has also been shown that both
water deprivation (De la Horra et al., 1998) and direct preincubation of colonic tissue with arginine vasotocin (De la
Horra et al., 2001) increase BBMV hexose transport, suggesting
that other hormones may play a role in the regulation of colonic
transport. The physiological significance of these changes in
transport mode are not completely understood, but it seems
likely that the low salt pattern represents an adaptation for salt
conservation, whereas the high salt/cotransporter mode may be
optimal for minimizing osmotic water losses into the hyperosmotic colonic lumen.
Low salt acclimation not only affects transport activity, but
also induces a remarkably extensive remodeling of the coprodeum. Thus, with chronic low salt intake, there are increases
in cell number and in microvillous length and density that
collectively increase the apical surface area by more than twice
that seen in high salt hens, and which correlate nicely with the
Na+ transport activity measured in vitro (Elbrnd et al., 1991,
1999; Mayhew et al., 1992). These changes can be partially
mimicked with aldosterone treatment of high salt hens, and can
be reversed with resalination (Elbrnd et al., 1999). Low salt
acclimation has also been shown to specifically increase the cell
number and microvillous height of mitochondria-rich (MR)
cells in the coprodeum, which appear to be involved in proton
secretion (Elbrnd et al., 1997, 1998, 2004).
Granivorous birds typically possess well-developed paired
ceca, in which production of short chain fatty acids takes place.
However, it is also proven that ureteral urine enters these
structures by retrograde movement, thus allowing for further
absorption and modification of urine (see Skadhauge, 1981,
Chapter 3). While only semi-quantitative measurements of inflow into the ceca in vivo have been made (see Skadhauge, 1981,
p. 35), the resorptive capacity of domestic fowl ceca seems to
match that of coprodeum and colon combined (Thomas and
Skadhauge, 1989a,b).
1.4. The salt gland strategy
Functional nasal salt glands are found primarily in marine
birds and in salt-tolerant estuarian birds such as mallard ducks
(Schmidt-Nielsen et al., 1963; Simon, 1982; Skadhauge et al.,

1984a; Hughes, 2003). These glands typically excrete a NaCl

solution, with few other accompanying ions, that can be twice
the maximal urine osmolality (see Skadhauge, 1981, chapters 7
and 8). Thus, they are able to excrete excess salt loads from diet
or drinking water, that the kidneys, with limited concentrating
ability (see Table 1), are incapable of eliminating. This process
effectively generates free water for the birds. The importance of
this desalination mechanism has been demonstrated in ducks
drinking seawater (Holmes, 1975). Ducks with intact salt glands
had a positive net water balance, whereas those without salt
glands clearly had net losses of water. Since the kidneys must
continuously excrete some water in order to eliminate nitrogenous waste, birds with salt glands may benefit from cloacal
reabsorption of ureteral urine; NaCl could be absorbed by the
lower intestine along with solute-linked water absorption, with
subsequent excretion of the NaCl by the salt glands in concentrated solution. This sequence of events was proposed by
Schmidt-Nielsen et al. (1963). In domestic ducks Skadhauge
et al. (1984a) found that there was little effect of salt intake on
colonic Na+ and water absorption; this constant and relatively
large transport by the lower intestine seems to confirm the
Schmidt-Nielsen hypothesis. Likewise, in the more marine gulls
(Larus glaucescens), Goldstein et al. (1986) found by in vivo
perfusion methods no differences in Na+, Cl or water transport
rates in birds acclimated to freshwater versus seawater. However, these authors argue that the small size and surface area of
the colon in this species, as well as the already low Na+ concentrations in ureteral urine, do not support a large role for
lower intestine in NaCl recycling to the salt glands, as proposed
by Schmidt-Nielsen. On the other hand, saline acclimation in
young gulls, and to a lesser extent in ducks, caused increased
Na+ and water transport in small intestine segments (Crocker
and Holmes, 1971; Roberts and Hughes, 1984). In adults both
species maintained the same Na+ transport rates with either
freshwater or seawater acclimation (Hughes and Roberts, 1988).
Hindgut transport may nevertheless be important in driving
solute-linked water absorption in order to offset the potential loss
of water into the hyperosmotic contents of the lumen. In saline
acclimated ducks, Hughes and Raveendran (1994) provided
evidence for substantial reflux of ureteral urine into the lower
intestine, even as far as the ceca. Cloacal fluid osmolality in these
studies was more than 100 mOsm/kg hyperosmotic to plasma.
In vitro studies of another marine bird, the common murre
(Uria aalge) also found a very small colonic surface area, which
was nevertheless elaborated with villi and columnar absorptive
epithelial cells (rnason et al., in preparation). In the Ussing
chamber, tissues from these birds (which had been on natural
diet and salt intake) showed low initial short-circuit currents,
which could however be stimulated by apical addition of amino
acids, but which were insensitive to amiloride. The coprodeum,
also small in surface area, was of very high resistance, and
showed little transport activity. These studies further support the
idea that the lower intestine of marine birds functions mainly to
minimize osmotic water loss by solute-linked water reabsorption, in this case mediated by cotransporter activity. The NaCl
taken up through these processes would eventually be
eliminated by the nasal salt glands.

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It is not clear whether aldosterone plays any role in the

regulation of lower intestinal transport in birds with salt glands.
As noted above, NaCl intake has minimal effects on colonic
transport in ducks and gulls (Skadhauge et al., 1984a; Goldstein
et al., 1986). Some studies have presented data suggesting
elevated plasma aldosterone in high salt acclimated ducks
compared to those on normal salt intake (Simon and Gray, 1989;
Hughes, 2003). This effect would be opposite of that found in
domestic fowl, and might provide a mechanism for maintaining
high rates of colonic NaCl absorption for recycling to the salt
glands. However, the data cited above, for normal and salt
loaded ducks, are taken from two separate studies (Radke et al.,
1984; Simon and Gray, 1989) and should be interpreted with
caution. In this regard, the threshold of dietary salt intake for
changes in circulating aldosterone should be determined for each
species (rnason and Skadhauge, 1991). Radke et al. (1984)
found that plasma aldosterone increased markedly, in both ducks
and domestic fowl, with low salt intake (0.018% sodium in
feed), and that ducks on high salt intake (1.9% sodium) had
similar or slightly lower aldosterone levels than ducks maintained on the normal salt intake (0.4% sodium); i.e., the normal
0.4% level of salt intake in this study had already reduced
aldosterone levels to basal or near basal concentrations. Similarly, Harvey et al. (1984) demonstrated decreased plasma aldosterone in ducklings transferred from freshwater to 0.1 or
0.2 M NaCl drinking water for up to 4 days, although levels had
returned to baseline by 7 days.
Attempts to demonstrate direct effects of aldosterone on
lower intestinal transport in birds with salt glands have not been
conclusive. Holmes et al. (1983) used chronically colostomized
ducks to study effects of aldosterone and corticosterone on
cloacal excretion rates during water or salt loads. The results
actually showed the same or greater antinatriuretic effects of
aldosterone in colostomized ducks compared to those of intact
ducks, suggesting either enhanced renal or post-renal (coprodeum) sodium absorption rates following colostomy.
It should also be mentioned that nasal salt glands were found
in ostriches, despite the lack of urinary reflux into the lower
intestine (Technau, 1936; Schmidt-Nielsen et al., 1963;
Skadhauge and Dawson, 1999). Schmidt-Nielsen et al. (1963)
claimed to induce nasal fluid secretion of varying ionic composition (no measurements given) when the ostrich was
subjected to thermal stress and water deprivation. It is possible
however, that mucous formed by gular flutter has been taken for
nasal secretion. Furthermore, the small mass-specific size
of these glands in the ostrich compared to marine birds (see
Skadhauge and Dawson, 1999), suggests minimal function in
osmotic regulation. In addition, neither acute nor chronic salt
loading was able to induce nasal secretion in this species (Gray
and Brown, 1995; Skadhauge and Dawson, 1999).
1.5. Birds of prey
One group of birds remains unstudied, although posing special
problems for renocloacal interaction: birds of prey. In these
species the urine is fluid and well mixed with feces, both stored in
the joint coprodeum/colon compartment. This would seem to

251

preclude segmental differences with oppositely directed water

flows as depicted for granivorous seed eaters in Fig. 2. Furthermore, the ceca are vestigial or not present, which gives no
additional site for recuperation of urinary water (McLelland,
1989). The interesting question is, therefore, whether the wall of
the coprodeum/colon epithelium is more water impermeable than
in other species. Few measurements of urine osmolality or of the
composition of cloacal droppings have been made in carnivorous
birds. Of those measured (Skadhauge, 1981) the best concentrator
would seem to be the Australian kingfisher, the Kookaburra
(Dacelo gigas). In the dehydrated state, these birds have an
average urine (cloacal dropping) osmolality of 944 mOsm
(Table 1) and an osmotic urine to plasma ratio of 2.7 (Skadhauge,
1974a). The large predatory birds do not need to drink water
(Bartholomew and Cade, 1963), so the water as compared to ion
content of the prey is of interest. Eating whole young mice, water
will comprise nearly 70% of the body weight of the prey, whereas
when eating raw meat or liver the potassium load would seem
larger than the NaCl intake. Only intake of crustaceans or other
invertebrates with body fluids similar to the composition of seawater would seem to present a substantial salt load. It would
therefore be of interest to study whether carnivorous birds like the
Kookaburra actually regulate coprodeal/colonic epithelial transport of Na+ or K+ ions. No carnivorous bird has been studied in
this respect. The possible regulation of cloacal transport parameters during food deprivation would be of further interest, as
this represents the alternative physiological condition to feeding.
2. Summary
It is interesting to note that August Krogh, in his 1939 book
(Krogh, 1939), discussed the problem of marine birds drinking
seawater and speculated that they would therefore excrete urine
with a very high osmotic pressure. We now know that marine
birds are no better than terrestrial species in their renal concentrating ability (urine to plasma osmolality ratios of 23 are
typical) (Goldstein et al., 1986; Goldstein and Skadhauge, 2000;
Hughes, 2003), a fact attributed to the predominance in avian
kidneys of reptilian-type or non-looped nephrons (Braun and
Dantzler, 1972; Wideman, 1988; Goldstein and Braun, 1989;
Braun, 1993; Goldstein and Skadhauge, 2000). Nevertheless,
because birds lack a true urinary bladder (except for the mammalian strategy, as discussed above), and because ureteral urine
empties into and may reflux into water permeable segments of
the lower intestine, even this moderately hyperosmotic urine
could result in a loss of the water conserved by the urine
concentration mechanism. In the case of marine birds, with the
later discovery of functional nasal salt glands, it was proposed
that salt and water absorption by the lower intestine would
prevent this loss, with the NaCl absorbed by this transport
eventually eliminated by these salt-secreting glands (SchmidtNielsen et al., 1963). This mechanism seems to have been
validated by the few studies performed on marine birds, although some controversy still exists regarding the extent to
which this lower intestinal recycling contributes to osmotic
balance (Goldstein et al., 1986), and represents only one of
several strategies that birds use to overcome this problem.

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G. Laverty, E. Skadhauge / Comparative Biochemistry and Physiology, Part A 149 (2008) 246254

In this review we have provided examples of species with 1.

modest urinary concentrating ability and a marked post-renal
absorption capacity (the reptilian strategy, exemplified by the
emu); 2. relatively high renal concentrating ability and essentially no post-renal modification (the mammalian strategy,
exemplified by the ostrich); 3. the interaction strategy (granivorous birds, such as the domestic fowl), in which water loss
into the coprodeum is counteracted by retrograde movement of
urine into the colon and ceca with solute-linked water absorption
in those segments, and with adjustments in transport mediated
by dietary sodium intake; and 4. the already mentioned mode of
salt-recycling in marine birds with functional salt glands. The
kookaburra represents an as-yet unstudied group of birds, the
birds of prey, which may use a mode like that of the ostrich, or
may have other, unique adaptations for post-renal urine modification. Studies of representatives of this group would be of
considerable value. In total, these examples illustrate the
diversity of adaptations in renocloacal interactions in birds
and in mechanisms for the maintenance of osmotic balance.
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