The Salt-Secreting Gland of Marine Birds
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The Salt-Secreting Gland of Marine Birds
By KNUT SCHMIDT-NIELSEN, PH.D.
Marine birds possess salt-secreting nasal glands which produce hypertonic solutions of
sodium chloride in response to osniotic loads such as ingestion of sea water. The concen-
tration of the secreted fluid is always high, several times as high as the maximum urine
concentration in birds. The presence of this gland must be considered a necessary adapta-
tion to marine life in animals whose kidney cannot excrete high salt concentrations. The
structure and blood supply to the gland indicate a countercurrent flow, but at the moment
it is not possible to explain the high concentrations of the secreted fluid as the result
of a countercurrent multiplier system. The gland is under parasympathetic nerve control;
its secretory function is blocked by anesthesia and certain drugs, including carbonic
anhydrase inhibitors.
The Comparative Viewpoint per cent salt, and the body fluids of all ver-
THE SUBJECT which I am going to deal tebrates contain around 1 per cent.* This
with can, I think, be referred to as com- poses serious physiologic problems of osmotic
parative physiology. Renal physiologists have loss of water, as well as influx of salt from
more sophistication in comparative physiology the more concentrated medium. In fresh wa-
than most other physiologists. They are used ter, the problems are reversed. Since the water
to discussing animals such as alligators and contains very little salt, the fresh-water ver-
frogs and the very interesting and unique tebrates face a steady influx of water and a
aglomerular fish, which has a kidney but no loss of salt to the dilute surrounding medium.
glomeruli. Names such as Marshall, Smith, Dr. Wald suggested yesterday evening that
Forster and others testify to the value of a the vertebrates have evolved in fresh water.
comparative approach in relnal physiology. That may or may not be so. At this time I
This leads me to say, without hesitation, don't think we know, but it is convenient to
something which might have seemed startling start our discussion with fresh-water verte-
a few years ago, but, I am sure, will not be brates. In fresh-water fish and Amphibia, the
very surprising to most of this audience; that kidney is important because it eliminates, as
is, that the kidney is not always the most a very dilute urine, the water which enters
important organ of excretion, and, in fact, the body due to osmotic inflow. However, one
that the mammals constitute the only class of could say that their major organ of osmotic
vertebrates in which the kidney is always the regulation is not the kidney, for the fresh-
major organ of osmoregulation. water fish makes up for the loss of salts
To explain this statement, it is helpful to through active uptake of ions in the gill, and
review briefly the physiologic conditions for the amphibian has a similar mechanism in
life in the sea and in fresh water. Earlier in the skin. In fact, the frog skin has become a
this symposium Dr. Fishman quoted from classical object of study because it is so emi-
Thales of Miletus that "YWater is best," but nently suited for experimental work on ionic
he made the comment that salt is also good. transport mechanisms, and has permitted the
To be specific, this is a matter of concentra- *The most primitive vertebrates, the cyclostomes,
tion. As you know, the ocean contains over 3 are exceptions; they are in osmotic equilibrium with
and have salt concentrations similar to sea water.
From the Department of Zoology, Duke University, The elasmobranchs are in osmotic equilibrium with
Durham, N. C. sea water, but a major part of the solutes in their
Supported by National Institutes of Health Grant body fluids is urea and trimethylamine oxide, and
H-2228 and Office of Naval Research Contract NONR- the salt concentration of their body fluids is similar
1181 (08). to that of other vertebrates.
Circulation, Volume XXI, May 1960 955
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development of Ussing's ingenious method of are not as highly developed as in mammals.
measuring the ion flux by means of the short- Reptiles have no loops in their kidneys, there
circuit current. is no countercurrent multiplier system, and
Salt-water fish have an osmotic loss of wa- their urine cannot be concentrated above the
ter to the concentrated surrounding medium plasma concentration. As a consequence, ma-
and compensate by drinking sea water. The rine birds and reptiles cannot rely on the
excess salt is eliminated by the pump in the kidney for osmoregulation, and they appear
gill, which, compared to the fresh-water fish, to have a choice between avoiding the drink-
has been turned around. Again, we have a ing of sea water and acquiring some means
case in which the kidney is not the major for salt excretion more efficient than their
organ of osmoregulation. No amphibian has kidneys.
been reliably reported to live in salt water, Marine Birds
and it seems that the amphibians as a group Many birds and a few reptiles have adapted
are unable to solve the physiologic problems to marine life. Some birds come to land only
of adaptation to life in salt water. to breed, and spend most of the year on the
Other vertebrates, reptiles, birds and mam- ocean; others, such as the penguins, have be-
mals are, of course, mostly terrestrial. In come excellent swimmers and have lost the
these the kidney is the major organ of excre- power of flight. The emperor penguin is said
tion, and, as such, a very efficient organ. The never to come on land, not even to breed, but
mammals, in particular, have evolved a kid- this statement is merely a play on words, for
ney with a high concentrating ability, which, the emperor penguin hatches its eggs standing
as Marshall pointed out, undoubtedly is re- on the antaretic ice during the cold polar
lated to the presence of the loop of Henle. winter. Many marine birds eat fish, which
More recently, the role of the loop structure contain much water; this circumstance re-
has become clear with the understanding of duces their problem of salt excretion. In fact,
how it functions as a countercurrent multi- on a diet of fresh fish, cormorants have plenty
plier system. of water to spare and do not need to drink
Some mammals, birds and reptiles have at all.' But other birds eat inivertebrates
evolved a secondary adaptation to a marine which are in osmotic equilibrium with sea
habitat. Seals and whales can handle the water; gulls eat mussels, sea urchins and
problem of life in salt water because their crabs, eider ducks filter small organisms out
kidney can produce a highly concentrated of the water, some penguins eat large quanti-
urine. Elimination of the salts from sea wa- ties of krill, and so on. How do these birds,
ter is well within the capacity of the mamma- with their inefficient kidney, eliminate the
lian kidney. Desert rodents, such as kangaroo salt that is present in their food and in the
rats and jerboas, which have to conserve wa- water they may drink? The aniswer is that
ter, have kidneys that can excrete urine more they possess an accessory organ, a gland in
than twice as concentrated as sea water. The the head, which produces a concentrated salt
reason that sea water is toxic to man is pri- solution that drips off from the tip of the
marily that his kidney is not very efficient in beak.
comparison to other mammalian kidneys. This salt-seereting gland is highly devel-
The kidneys of birds and reptiles have a oped in all marine birds, as opposed to ter-
concentrating ability which is considerably restrial birds. The gland has long been known
less than that of the mammalian kidney, ap- to anatomists as the nasal gland; it is present
parently because they contain no typical loops in all birds, but in terrestrial species it is
of Henle. Birds, which can excrete a urine very small.2 The size of the gland in marine
which is about twice as concentrated as the birds is 10 to 100 times as large, a striking
plasma, have some looped nephrons, but these differenee that was noticed long ago. The
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usual interpretation has been that the fune- the salt gland in living marine birds, its pres-
tion of the gland should be to rinse away the ence in fossil forms can safely be taken as an
irritating and harmful effects of sea water indication of a marine habitat. Some fossil
that might penetrate into the nasal cavity. birds, such as Ichthyornis and Hesperornis
However, in all the marine birds that we have from the Cretaceous period, have clear im-
examined, the gland secretes a solution of so- pressions on the skull where a large gland
dium chloride which is more concentrated has been located.5 These birds were fish eat-
than sea water, and the exclusive function of ers, and supposedly marine, and the presence
the gland seems to be that of osmoregulation. of the large gland in the same location as the
The species which we have examined, which salt gland of living birds is a satisfactory
include gulls, terns, auks, penguins, alba- confirmation of their marine life.
trosses, petrels, cormorants, pelicans, gannets,
herons and ducks, represent all the major Marine Reptiles
orders of mariine birds; it seems logical, there- Only a few reptiles live in the sea; they
fore, to conclude that the salt-secreting gland represent 4 orders: turtles, snakes, lizards
is present in all marine birds. and crocodiles. The great sea turtles eat fish
It is interesting that the gland not only or seaweed, and go on land only to lay their
is large in marine birds, but that, to some eggs on sandy beaches. They are known to
extent, its size varies with the exposure to salt shed tears as the eggs are deposited, evidently
loads. Long before the function of the gland a sign of osmoregulation, rather than pain.6
was known, Schildmacher3 found that ducks The sea snakes (Hydrophidae) of the Indian
brought up with access to a 3 per cent salt Ocean are truly marine; the more primitive
solution instead of fresh water developed an lay their eggs on land, but the most special-
enlarged gland. However, after a careful dis- ized bear living young and remain at sea
cussion of the apparently causal connection throughout life. They are reputed to be the
between the size of the gland and salt water, most poisonous of snakes, and their osmoreg-
Schildmacher repeated the mistake of the old ulation has never been studied. A single liz-
interpretation, stating that the only possible ard, the Galapagos lizard (Amblyrhyiichus
explanation is that the gland protects the cristatus) is marine; it lives on the beaches
nasal mucosa against irritation. of the Galapagos Islands where it eats sea-
The change in the size of the gland with weeds and occasionally blows a spray of drop-
the degree of exposure to salt was observed lets out through its nostrils, reminiscent of a
earlier by the Heinroths, who found that eider puff of smoke from a fiery dragon. This harm-
ducks which were reared in fresh water in the less creature is easily handled in the labora-
Berlin Zoo had smaller gland impressions on tory, and it proves to have an osmoregulatory
their skulls than individuals of the same spe- nasal gland that produces the salty fluid
cies collected in the wild.4 However, the rela- which is ejected from the nose. The marine
tive ease with which the gland hypertrophies crocodile (Crocodylus porosus) has been
with use and atrophies with disuse should not found far out at sea, but normally it lives in
be taken to mean that terrestrial birds can estuarine swamps. A single specimen which I
develop a functional salt gland from their had in the laboratory did not respond to os-
nasal gland. This does not seem to be the case; motic loads, and crocodile tears must still be
only those birds that have an evolutionary classed as one of the mysteries of biology.
history of adaptation to a marine habitat seem Terminology
to have evolved a gland of significant size, and The presence, but not the function, of the
seem to be capable of secreting hypertonic salt-secreting gland has been known for cen-
solutions. turies7 and received considerable attention
With the apparently universal existence of early in the last century.'-10 It has been called
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the nasal gland (glandula nasalis), although 10 times as high as the total cloacal excretion.
it is not always found in what one would call In other words, in this particular experiment,
the nose. In most marine birds it is located the extrarenal excretion of salt was 10 times
on top of the head, above the orbit of the eye, as important as the renal excretion. In spite
and has therefore also been called the supra- of the salt load, the concentration of sodium
orbital gland, or glandula nasalis supraorbi- in the urine was low and tended to decrease
talis. In the marine turtles the salt-secreting further during the experiment, although the
gland is seemingly of a different embryologic kidney has the capacity to excrete concentra-
origin. It is located in the posterior part of tions of sodium up to about 300 mEq./L. This
the orbit of the eye, and its duct opens in the drop in the concentration of sodium in the
posterior corner of the eyelids. This gland in urine after a salt load has frequently been
the turtle should, therefore, probably be re- observed in gulls, but in other species of birds
garded as a modified lacrimal gland. It is about which we have similarly complete rec-
interesting that the gland of the turtle, in ords of the effects of a salt load, the concen-
spite of its different origin, has the same his- trations of sodium in the urine have tended
tologic structure as the gland of the bird. to rise toward the concentration ceiling (about
Since these glands, which anatomically are 300 mEq./L.).
not homologous, have the same function, the Composition of the Nasal Secretion
need arises for a convenient terminology. We The fluid secreted fromi the salt gland is
have therefore decided to call them salt-se-
very simeple. Except for epithelial cells and
creting glands, or simply salt glands; this other debris in samples collected immediately
designation, then, denotes any gland in the after the start of secretion, the almost neutral,
head region of marine birds and reptiles
watery liquid is clear and colorless. The dom-
which, irrespective of anatomic origin, has aii
osmoregulatory function and secretes highly inating solutes are sodium and chloride in
hypertonic sodium chloride solutions. approximately equivalent amnounts (table 3).
There is a relatively small amount of potas-
Response to a Salt Load sium, some bicarbonate, and almost nothing
The effect of a considerable salt load in a else. Magnesium and sulfate, which are pres-
black-backed gull (Larus marin ts) is shown ent in sea water in rather high concentrations,
in table 1. In this case the bird, which weighed are virtually absent from the nasal fluid. The
1,420 Gm., was given almost one-tenth of amount of organic material, including urea,
its body weight of sea water by stomach tube. is very small. Phenol red, which apparently
After about 3 hours the total volume of the is excreted by all kidnevs, is not secreted by
exereta equaled the infused aimount, and all the nasal gland and does not appear in the
the ingested salt had been eliminated. In fluid.
other words, a gull handles quite easily a salt
load which could not possibly be tolerated by Concentration of the Fluid
man. The activity of the salt gland is an all-or-
Some details of the relative importance of none phenomenon. If there is an osmotic load,
the kidney and the salt gland are given in the gland secretes; in the absence of an os-
table 2. The total amount of fluid excreted niotic load, the gland is at complete rest. In
from the salt gland was 56 ml., while in the this intermittency, the gland differs from the
same 3-hour period 75 ml. was eliminated kidney which produces urine continuously.
from the cloaca, most of this latter being The concentration of salt in the nasal secre-
urine. The concentration of sodium was uni- tion is always very high, and remains fairly
formly high in the nasal fluid, while it was constant for each species (table 4). There
low in the cloacal fluid. Thus, the total amount seems to be a clear connection between the
of salt eliminated by the salt gland was about coneentrating ability of the salt gland and
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Table 1 Table 3
The Total Excretion of Water and Salt in a Black- Typical Composition of the Fluid from the Salt-
Backed Gull After a Load of Sea Water by Stom- Secreting Gland of Herring Gulls
ach Tube
Na+ 718 mEq./L. Cl- 720 mEq./L.
Body weight 1,420 Gm. K+ 24 mEq./L. HCO3- 13 mEq./L.*
Sea water ingested 134 ml. Ca++ + MIg++ 2.0 mEq./L. S04-- 0.68 mEq./L.
Exereta, total volume in 3 hrs. 131 ml.
Sodium ingested 54 mEq. *Dr. Maren has kindly permitted me to quote aver-
Sodium excreted in 3 hrs. 48 mEq. age figures obtained in his laboratory. For nasal
secretion these are: HC03-=9.1 mEq./L., pH=7.03;
and for plasma: HCO3-=21.7 mEq./L., pH-17.48.
Table 2
Nasal and Cloacal Excretion by a, Black-Backed
Gull During the 175 Minutes Following the Inges- Table 4
tion of Sea Water (see Table 1) Usual Concentration of Sodium in the Nasal Secre-
tion of Different Species of Birds*
Nasal excretion Cloacal excretion
Concentration of
Sodium Sodium Sodium Sodium Species sodium, mEq./L.
Time, Vol., conc., amount Vol., conc., amount,
min. ml. mN mEq. ml. mN mEq. Cormorant, double-crested 500-600
15 2.2 798 1.7 3.8 38 .28 Duck, mallard (550)
Skimmer, black 550-700
40 10.9 756 8.2 14.6 71 1.04
Eider duck, common (625)
70 14.2 780 11.1 25.0 80 2.00 Pelican, brown 600-750
100 16.1 776 12.5 12.5 61 .76 Gull, herring 600-800
130 6.8 799 5.4 6.2 33 .21 Gull, black-backed 700-900
160 4.1 800 3.3 7.3 10 .07 Penguin, Humboldt 's 725-850
175 2.0 780 1.5 3.8 12 .05 Guillemot 750-850
Albatross, blackfooted 800-900
Total 56.3 43.7 75.2 4.41 Petrel, Leach 's 900-1,100
*Some samples fall outside these limits, which rep-
the feeding habits of the bird. For example, resent only the usual range. Numbers in paren-
in the cormorant, which eats fish that is rela- theses represent species in which samples have been
tively low in salt content, the concentration too few to establish a normal range.
in the secretion from the gland is about 500
to 550 mEq./L. and rarely exceeds 600 bird we have examnined, up to 1,100 or 1,200
mEq./L. In the herring gull, which consumes mEq./L.
more invertebrate food, and consequently No other gland in higher vertebrates, ex-
more salt, the concentration is usually between cept the mammalian kidney, can produce
600 and 800 mEq./L.; the great black-backed fluids which are concentrated to this degree.
gull which is more marine in its habits, has The concentration limit for electrolytes in
concentrations between 700 and 900 mEq./L. the kidney of man is about 400 mEq./L., in
The petrel is a bird with pronounced oceanic the rat 600 mEq./L., in the kangaroo rat,
habits. It spends most of its life at sea and 1,500 mEq./L., and in the champion concen-
comes to land only to breed. It lives on plank- trator, the North African rodent Psammomys,
tonic organisms, mostly crustaceans, which it 1,900 mEq./L. Thus, the salt gland compares
picks off the surface of the ocean as it flies by. favorably to the kidney in its concentrating
The planktonic organisms, being inverte- ability. In other respects the salt gland is
brates, have the same osmotic concentration quite different from the kidney; it secretes
as sea water and therefore impose a consid. only sodium chloride, it always produces a
erable salt load. It is no surprise, therefore, liquid which is highly hypertonic to the blood,
that in the petrel the salt concentration of and it works as an all-or-none system, becom-
the nasal fluid is higher than in any other ing active only after an osmotic load.
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Table 5
A Comparison Between the Rate of Secretion from the Salt Gland of the Gull and the
Volume of Urine During Water Diuresis in Man
Salt gland, herring gull 0.5 ml./mimi.
Flow per Kg. body weight: Kidney, water diuresis, man 0.24 ml./min,
Kidney, GFR, man 1.8 ml./min.
Salt gland, herring gull 0.6 ml./mini.
Flow per Gm. gland: Kidney, water diuresis, man 0.03 ml./min.
Kidney, GFR, man 0.2 ml./min.
Volume of Flow 0.3n ml. per Gm. of kidney per minute. In
Although the concentration of the nasal other words, despite the considerable osmotic
secretion is relatively constant, its volume is work necessary to produce the concentrated
not. The rate of flow can change from zero fluid, the salt gland can secrete at a rate
to a maximum which varies with the species which is as high as, or higher than, the glo-
and, to some extent, between individuals merular filtration rate in the mammalian
within the species. After a salt load is given kidney.
to a bird, the rate of flow rapidly increases,
Structure of the Gland
and remains rather high for a period that
depends on the degree of the load. It then What is the structure of this unusual gland
tapers off and diminishes as the salt is elim-
which produces fluid as fast as the kidney
inated (table 2). However, the rate can re- filters the plasma? Figure 1 shows the loca-
main at near-maximal levels for hours. That tion of the gland in the gull. On top of the
this rate is quite high becomes clear when skull there are 2 crescent-shaped, flat glands,
the flow from the gland in the gull is com- which are located in shallow depressions in
pared wth the flow of urine during water di- the bone. Actually, each gland consists of 2
uresis in man. In table 5 flows are calculated parts which are so similar in structure and
are so closely joined that they can be consid-
per kilogram of body weight. It may be seen
that although the osmotic concentration of ered as one funetional unit, i.e., as one gland.'1
the nasal secretion is high, the production of
Two ducts run from each side down to the
nose where they open at the vestibular concha.
nasal fluid is more thall twice the maximum
water diuresis in man.
From the anterior nasal cavity the secretion
flows out through the nares and drips off from
Size of the Gland and Flow Rate the tip of the beak. A few marine birds have
What is the size of a gland which has this closed and nonfunctional external nares;
amazingly high excretory capacity? Its size is characteristically these birds, e.g., gannets
not very impressive compared to the kidney; and cormorants, are good divers and enter the
in the gull, which has a relatively large salt water after a fast dive from some height. The
gland, it is about 0.1 per cent of the body closed nares probably are a protection against
weight, while the kidney of mammals ap- the penetration of water at the time of impact
proaches about I per cent of the body weight. with the surface. In these birds the nasal se-
Thus, if we relate the volume of secretion to cretion flows through the internal nares along
the weight of the gland rather than to body the roof of the mouth, forward to the tip of
weight, the capacity of the salt gland becomes the beak.
even more striking. The gland of the gull can The glands consist of longitudinal lobes,
produce about 0.5 ml. of fluid per Gm. of which in cross section show tubular glands
gland per minute. The glomerular filtration radiating from a central canal (fig. 2). Except
rate in man is about 0.2 ml. per Gm. of kidney for the most distal portion where the cells are
per minute and in the rat, I believe, about somewhat smaller but of the same general
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Figure 1
The skull of the herring gull shows the location of the salt-secreting glands as 2 shallow,
crescent-shaped depressions in the bone above the orbit of the eye. (Drawing by M.
Cerame-Vivas.)
type (fig. 3), the branehing, tubular glands tubular cells as reconstructed by Rhodin, the
have a rather uniform structure throughout transport process might indeed take place inl
their length. The tubules are closed in the dis- the intereellular spaces of interdigitating
tal end, and there is no structure reminiseent cells, rather than across the cell body. These
of the glomerulus of the kidney. The struc- studies are being continued by Dr. Doyle and
ture is characteristic of a tubular gland, which will be published elsewhere.
indicates that the secreted fluid is elaborated Blood Supply to the Gland
only by simple glandular secretion, and that'
The gland receives its main arterial blood
there is no ultrafiltration of fluid comparable
to that in the kidney. This conclusion is sup-
supply from the arteria ophthalmica interna.
ported by the fact that inulin does not appear In the gull, several blood vessels penetrate the
in the secretion. bony wall of the orbit and enter the gland
A retrograde injection of india ink into the from below. This makes the blood vessels diffi-
gland through its duct shows that the ink cult to reach, and attempts at perfusion of
penetrates all the way into the cells, giving the gland are likely to lmeet with immense
the appearance of intracellular canialiculi. technical difficulties.
which probably have a secretory function. The circulation in the lobes of the gland
Electron micrographs made by Dr. W. L. can be visualized most easily in preparations
Doyle at the University of Chicago, as well as which have been prepared by the injection
by other investigators, show that there are of the vascular system with india ink.1' It is
deep infoldings both in the apical and the found that the main arteries to the gland
basal parts of the secreting cell, which has branch into interlobular arteries, which send
some similarity to the tubular cell of the smaller branches into the single lobes. These
nephron. It must be assumed that the deep arteries continue toward the central canal,
infoldings are intimately related to the fune- where they split up into capillaries which
tion of the cells, and it could be suggested run parallel to the tubular glanids toward the
that the elaboration and transport of fluid periphery of the lobe. A section cut perpen-
does not necessarily take place as a tranls- dicular to the tubular glands (fig. 4) shows
tubular process. If the infoldings prove to be that the capillaries are interspersed between
similar to the interdigitations of the renal the glands, much as in the papilla of the kid-
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Figure 2 Figure 3A
The salt glatndi of the quttI-11cosists of longitudinal It crossss tion tMc loOr of the eodlt-setreting glaln
lobes afbout .1 mm. i"n (liha teter; each lobe has a shows th.e u tItot coito l 1(te rodiol arrattyc
central canaltl uwtih the broiuching secretorY tubtules tucut of the sectvtottj tub olc. I the lo right
arranged rahially aroantd it. (Irauwing by 31. han oro r on tt ?obalott tin and at otIs rq
Ce)o(iint-Vivas.) ( itt le.
nley wihcir thle vasa reet a are interspersed be
tween the limibs of Ilfele's loop. A diagram.
of the eireiflation (fig. 5) shlows howv the bloo(d
flovs parallel to, blut iii the opposite tireetiot)
fr omii, the flow in dlie tulbular glancd.
Is There a Countercurrent System
in the Salt Gland?
Tileo arrangement jlust deseslibed cani, ot
colilse,be recog'n1ized as
aI countercurrent flow,
and n-to r-enial physiotlogist is unawvare of the
inuportance of the counttereurreiit multijtiier
systel iii the elal)oration of a concentrated
urinle in tlhe kidney. Iloowever, iii the ease of Figure 3B
the salt gland,I thel cottitercurreiit flow cannlot In higher mnigfnicjhtion the pelhertol ettds of
thle scc 1 torj1 tol (tlc op)ycotr (Os clou)Cd tn-b)Cs wllith-
be used to explain thie elaboration of a eoi- oalt a ji. titiuriitq to hlt( 1loturlo oppottlus o f
centrated fluid. A countercurrenlt mlultiplier the litlitct. 101 t'eve,
t thl petiphetar por)a?t of tAte
sy steni consists of a tuIbD whliehli lhas beeni tabule hos stiallr clls otid aitt 0ppe(t'r(ttte w,7hich
tu-rned back on-t it:sel f to formi a loop) but (IilrettS I to ttt tltt to t (C)tcft? tot potts.
in the salt glancd we have 2 unconnected tubes
ruinnigo in opposite direct ions. This is tvpical of a1 secretion which is isotonic, with plasma,
for a type of couiniter-currenit exchiange s-stemii awln tlhe highi (coneentra,Ctions wviichi are ac-
wvhieh is iiartieularly well suited for obtaining tuallly pI oduee(d rinol esult fu1'n a counter-
the same concentration in the oitg(oing(, fluidil ein re-it mul-lltiplier sy stein.
hovm onle tube as in the iiieoming fluIid i; the It is truel( that tI-le direction of the blood
other (fig. 6). Il other wvords, the systenm in flow may be opposite lo what wve have as-
the salt glaind seems ideal for the elaboration sumed for there is alwvays soniic doubt abolut
Circulation, Voluime XX!, May 1960
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Figure 4
-As maY 1)e seenz in this coss ,scctiton, te secretinyg tubnuls are interspersed withh lapillarns,
'Much 1ib4' the arrangyenent in the J)apiltl of the kidlney. C(olpallwre wvith the dlia grammotic,
cross scc tion to the right in figure 5).
the, initerpretation of histologic sectioins. But [ orin llbe faci.l nerve,7 well as ly symplla-
as,
iwere thte reverse of wx-hat
even if the 1)00(I1o flow thletfi fibers. Apparently nominyelinated fibers
we have sugg(,este(, with the flow in the same fromlw thle gainglion penetrate the bone to reachl
directioll as the fluid inl the gklanid, the ar- the glaud. Electrie stimnulatioii of the oplithlil-
rangemeut woil(d still nlot be a muiltiplier imuie nerve cauises nio secretioni, but if the small.
system. AVe mullst therefore conch(lude thiat, braneh froim the facial nerxve is stimnulated, a
altlhough there is a countercurrent flow, the fluid of the usuial compositiol, rich itn sodium
countercurrent multiplier prineijle cann-ot be chloride is secreted. As far as we can establish,
used to exl)lain the functioni of thils partieular the br-anch of the facial nerve conthinues back
glanid anid its ability to elabor:(ate high-ly coil- towai(I the ininer ear; it is reminiscent of, antd
centrate(I soluitionis. eould be homologrous to, the clhorda tynupani
Nervous Control xlhieh stimlIIates sdlivax y seeretion in1 niamn-
The nerve supj)ly to the salt g1land( is ratlher mals.
eom)lex anld not easilv workced out because Thc secretory nerve apparently is parasyin-
the nierves iii the head of tlhe l)ird have a pathetic in natur1e2.0 Stimiiulatioin of the cervi-
comiplex course witli frequenit ranastomoses. cal symnpatlhetic chain causes nio seeretioni and
The gland is inniiervated from a g,anglion in in.jeetiori of epinephlinie blocks secretion from
the orbit, t-he gancglion ethraoidale. This gan- fthe gland. Accttleholine, if injected in a prox-
glionl is supplied by a relatively lalrge branch imal artery, causes the gyland:I to secrete; if
of the ophtlhalie ni erve, and a smnaller onie injected in the genieral eireulationl it will, of
Circulation, Volume XXI, May 1960
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Figure 5
The arrangement of the blood vessels and capillaries in the lobes of the salt gland
indicates that the capillary blood flow is countercurrent to the flow of secreted fluid in
the secretory tubule. (Drawing by M. Cerame-Vivas.)
course, be hydrolyzed before it reaches the osmoreceptor is used, rather than salt recep-
gland. The parasympathomimetic substance tor, because the gland responds not only to
methacholine (Mecholyl) also causes the salt loads, but to osi-otic loads in general. If
gland to secrete. a hypertonic solution of a nonelectrolyte such
Effect of Anesthesia as sucrose is infused, the gland begins to se-
crete a fluid of the usual composition, with a
One difficulty in the study of the function
high concentration of sodium chloride. This
of the salt gland is that the secretion is
indicates that the secretion occurs in response
blocked by anesthesia. Secretion can always
be induced in the nonanesthetized bird by an to an osmotic load, rather than to the concen-
osmotic load, for examnple by the injection of tration of sodium or chloride in the plasma.
hypertonic sodium chloride. Within a few Carbonic Anhydrase in the Salt Gland
minutes, somnetimes within 1 minute of an in- It has frequently been proposed that car-
jected load, secretion will begin. However, bonic anhydrase plays an important role in
since anesthesia immediately blocks secretion, ionic transport nmechanisms. Since the salt
many further experiments, in particular those gland is an organ which apparently has no
involving surgical procedures, cannot be car- other funetion than the transportation of
ried out. sodium chloride, it seems well suited to a
Osmoreceptor Reflex study of the possible role of this enzyme in
The effects of anesthesia, of nerve stimula- the mechanism of transport. Many schemes
tion, and of osmotic load, indicate a sequence which have been suggested to accounit for
of control as suggested in figure 7. The term ionic transport involve bicarbonate and car-
Circulation, Volume XXI, May 1960
Downloaded from http://circ.ahajournals.org/ by guest on March 19, 2015100I
1000 L I MI
100°
QO
-
THE SALT-SECRETING GLAND OF MARINE BIRDS
COUNTER CURRENT FLOW
PARALLEL FLOW
Figure 6
Top. Thermal models indicate how the heat flow in a countercurrent exchange system
0Q
AO0°
50g LIMIT
50' LIMIT
leads to equal temperature in the affluent from one tube and the effluent from the other.
Bottom. A parallel flow leads to equal temperature in the effluent from both tubes. These
models assume equal volumes of flow in the 2 tubes. If the flows differ the limits change
accordingly, but in no case can a passtve exchange system increase the temperature in
the effluent from one tube to a level above that in the other.
bonic anhydrase in an ion exchange system.
With Dr. T. H. Maren, in 1958, we found that
the salt gland is rich in carbonic anhydrase.
Of considerable interest is the observation
that the carbonic anhydrase inhibitor, acet-
azoleamide (Diamox), when injected into a
bird whose gland is actively secreting, blocks
965
LIMIT
that the inhibition of the secreting cells is a
matter of relative concentrations, and that, if
the stimulus is strong enough, the gland starts
secreting in spite of the presence of the inhibi-
tor. Further work on this point has been done
by Dr. James Larimer, a former student of
mine, in Dr. AMaren's laboratory.
the secretion almost instantaneously.12 This
The Role of Acetylcholine in Secretion
result indicates that carbonic anhydrase is
essential to secretion, but it does not prove It is possible that the parasympathetic na-
that the block is in the ionic pump of the se- ture of the gland affords a clue to the mecha-
creting cells. A possible explanation is that nism of ion transport. The secretion occurs in
the block could be somewhere else in the path- response to the release of acetylcholine from
way indicated in figure 7. To examine this the stimulating nerve. This pattern is reminis-
possibility experiments were done to deter- cent of other systems in which acetylcholine
mine if the gland retains its ability to secrete has an important influence on the movement
in the presence of the enzyme inhibitor. This of sodium, such as in the depolarization of the
has actually been found to be the case: direct muscle fiber and of the nerve fiber. Recently,
stimulation of the gland with methacholine the Hokins of the University of Wisconsin
gives a secretion of the usual composition, have demonstrated that slices of the salt gland
showing that the ionic pump can work in the in vitro, when incubated with acetyleholine,
presence of a carbonic anhydrase inhibitor. show a greatly increased turnover of phos-
Another possible interpretation, however, is phatidic acid, as evidenced by radiophos-
Circulation, Volume XXI, May 1960
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CNS GANGLION SECRETORY
OSMORECEPTOR ETHMOIDALE TUBULE
KO -( *4 b, NA CL
\ ~~~/ S ECRETION
A\ACETYL I-,'
OSMOTIC CHOLINE
STIMULAT ION
Figure 7
Suggested sequence of events in the osmotic stimulation of secretion from the avian
salt gland.
phorus tracer experiments.13 The Hokins sug- the question. At this time I can only say that
gest that phosphatidic acid is an integral part if there is any organ in which an ionic pump
of the sodium pump in the gland, and that it and its metabolic ramifications can be studied
may be the actual ionic transport agenlt itself. in its pure form, the salt gland of marine
In a recenit series of papers'4-16 Scothorne birds almost seems to be designed for this pur-
has described histologic and histochemical pose.
studies of the nasal gland of ducks and References
pigeons. The gland of the domestic duck, like 1. SCHMIDT-NIELSEN, K., JORGENSEN, C. B., AND
that of the mallard, its wild ancestor, does OSAKI, H.: Extrarenal salt excretion in birds.
secrete salt, but the gland of the pigeon does Am. J. Physiol. 193: 101, 1958.
not. In the gland of the duck there is a mod- 2. TECHNAU, G.: Die Nasendrfise der V6gel. J.
Ornithol. 84: 511, 1936.
erate amount of alkaline phosphatase, and a
3. SCHILDMACHER, H.: Ueber den Einfluss des Salz-
high content of suceinic dehydrogenase. Not wassers auf die Entwicklung der Nasendriisen.
all glands have a high conitent of succinic de- J. Ornithol. 80: 293, 1932.
hydrogeniase; it seems probable that the pres- 4. HEINROTHv, O., AND HEINROTH, M.: Die V6gel
eniee of this enzyme in the salt gland nmay be Mitteleuropas in allen Lebens- uid Entwick-
closely related to the energy which is re- lunigsstufen photographisch aufgenommen und
in ihrem Seelenleben bei der Aufzucht vom Ei
quired to perform an exceptionally high level ab beobachtet. 3 vols. Berlin, H. Bermilhler,
of osmotic work. 1926-1928.
Obviously, much work remains to be done 5. MARPLES, B. J.: Structure and development of
on this unique gland, which apparently has nasal glands of birds. Proc. Zool. Soc. London.
11o other function than that of transporting 1932, p. 829.
sodium chloride and therefore seems to be 6. SCHMIDT-NIELSEN, K., AND FANGE, R.: Salt
glands in marine reptiles. Nature 182: 783,
eminently suited for studies of processes in- 1958.
volved in ionic transport. I believe that it is 7. COMELIN, C.: Collegium privatum Amsteloda-
too early to say whether the transport is due mense. Amsterdam, 1667. Quoted by TechnauiY
to a sodium pump or to a chloride pump. My 8. JACOBSON, L. L.: Sur une glande conglomeree ap-
personal guess is that it may be a chloride partena ate a la cavite nasale. Bull. Soc.
pump, but I have no real support for this no- Philom. Paris 3: 267, 1813.
9. NITZSCH, C. L.: Ueber die Nasendriise der V6gel.
tion except that the proportion of sodium to Deutscli. Arch. Physiol. 6: 234, 1820.
potassium in the secreted fluid may indicate 10. JOBERT, C.: Recherches anatomiques sur les
that the cation follows passively. In either glandes nasales des oiseaux. Ann. Sci. Nat.,
case, I expect that future work will answer ser. 5, 11: 349, 1869.
Circulation, Volume XXI, May 1960
Downloaded from http://circ.ahajournals.org/ by guest on March 19, 2015THE SALT-SECRETING GLAND OF MARINE BIRDS 967
11. FANGE, R., SCHMIDT-NIELSEN, K., AND OSAKI, histological and histochemical study of the in-
H.: Salt gland of the herring gull. Biol. Bull. active gland in the domestic duck. J. Anat.
115: 162, 1958. 93: 246, 1959.
12. -, -, AND ROBINSON, M.: Control of secretion 15. -: On the response of the duck and the pigeon
from the avian salt gland. Am. J. Physiol. to intravenous hypertonic saline solutions.
195: 321, 1958. Quart. J. Exper. Physiol. 44: 200, 1959.
13. HOKIN, L. E., AND HOKIN, M. R.: Evidence for 16. -: Histochemical study of suceinic dehydro-
phosphatidic acid as the sodium carrier. Na- genase in the nasal (salt-secreting) gland of
ture 184: 1068, 1959. the Aylesbury duck. Quart. J. Exper. Physiol.
14. SCOTHORNE, R. J.: The nlasal glands of birds: A 44: 329, 1959.
Water as a Substrate for Life
Water, of its very nature, as it occurs automatically in the process of cosmic evolution,
is fit, with a fitness no less marvelous and varied than that fitness of the organism whieh
has been won by the process of adaptation in the course of organic evolution.
If doubts remain, let a search be made for any other substance which, however slightly,
can claim to rival water as the milieu of simple organisms, as the milieu interieur of all
living things, or in any other of the countless physiological functions which it performs
either automatically or as a result of adaptation.-L. J. Henderson. The Fitness of the
Environment. Boston, Beacon Press, 1958, pp. 131-132.
Circulation, Volume XXI, May 1960
Downloaded from http://circ.ahajournals.org/ by guest on March 19, 2015The Salt-Secreting Gland of Marine Birds
KNUT SCHMIDT-NIELSEN
Circulation. 1960;21:955-967
doi: 10.1161/01.CIR.21.5.955
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