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The Salt-Secreting Gland of Marine BirdsBy KNUT SCHMIDT-NIELSEN, PH.D.

Marine birds possess salt-secreting nasal glands which produce hypertonic solutions ofsodium 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 urineconcentration 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. Thestructure and blood supply to the gland indicate a countercurrent flow, but at the momentit is not possible to explain the high concentrations of the secreted fluid as the resultof a countercurrent multiplier system. The gland is under parasympathetic nerve control;its secretory function is blocked by anesthesia and certain drugs, including carbonicanhydrase inhibitors.

The Comparative ViewpointTHE SUBJECT which I am going to deal

with can, I think, be referred to as com-parative physiology. Renal physiologists havemore sophistication in comparative physiologythan most other physiologists. They are usedto discussing animals such as alligators andfrogs and the very interesting and uniqueaglomerular fish, which has a kidney but noglomeruli. Names such as Marshall, Smith,Forster and others testify to the value of acomparative approach in relnal physiology.

This leads me to say, without hesitation,something which might have seemed startlinga few years ago, but, I am sure, will not bevery surprising to most of this audience; thatis, that the kidney is not always the mostimportant organ of excretion, and, in fact,that the mammals constitute the only class ofvertebrates in which the kidney is always themajor organ of osmoregulation.To explain this statement, it is helpful to

review briefly the physiologic conditions forlife in the sea and in fresh water. Earlier inthis symposium Dr. Fishman quoted fromThales of Miletus that "YWater is best," buthe made the comment that salt is also good.To be specific, this is a matter of concentra-tion. As you know, the ocean contains over 3

From the Department of Zoology, Duke University,Durham, N. C.

Supported by National Institutes of Health GrantH-2228 and Office of Naval Research Contract NONR-1181 (08).

Circulation, Volume XXI, May 1960

per cent salt, and the body fluids of all ver-tebrates contain around 1 per cent.* Thisposes serious physiologic problems of osmoticloss of water, as well as influx of salt fromthe more concentrated medium. In fresh wa-ter, the problems are reversed. Since the watercontains very little salt, the fresh-water ver-tebrates face a steady influx of water and aloss of salt to the dilute surrounding medium.

Dr. Wald suggested yesterday evening thatthe vertebrates have evolved in fresh water.That may or may not be so. At this time Idon't think we know, but it is convenient tostart our discussion with fresh-water verte-brates. In fresh-water fish and Amphibia, thekidney is important because it eliminates, asa very dilute urine, the water which entersthe body due to osmotic inflow. However, onecould say that their major organ of osmoticregulation is not the kidney, for the fresh-water fish makes up for the loss of saltsthrough active uptake of ions in the gill, andthe amphibian has a similar mechanism inthe skin. In fact, the frog skin has become aclassical object of study because it is so emi-nently suited for experimental work on ionictransport mechanisms, and has permitted the

*The most primitive vertebrates, the cyclostomes,are exceptions; they are in osmotic equilibrium withand have salt concentrations similar to sea water.The elasmobranchs are in osmotic equilibrium withsea water, but a major part of the solutes in theirbody fluids is urea and trimethylamine oxide, andthe salt concentration of their body fluids is similarto that of other vertebrates.

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development of Ussing's ingenious method ofmeasuring the ion flux by means of the short-circuit current.

Salt-water fish have an osmotic loss of wa-ter to the concentrated surrounding mediumand compensate by drinking sea water. Theexcess salt is eliminated by the pump in thegill, which, compared to the fresh-water fish,has been turned around. Again, we have acase in which the kidney is not the majororgan of osmoregulation. No amphibian hasbeen reliably reported to live in salt water,and it seems that the amphibians as a groupare unable to solve the physiologic problemsof adaptation to life in salt water.

Other vertebrates, reptiles, birds and mam-mals are, of course, mostly terrestrial. Inthese the kidney is the major organ of excre-tion, and, as such, a very efficient organ. Themammals, in particular, have evolved a kid-ney with a high concentrating ability, which,as Marshall pointed out, undoubtedly is re-lated to the presence of the loop of Henle.More recently, the role of the loop structurehas become clear with the understanding ofhow it functions as a countercurrent multi-plier system.Some mammals, birds and reptiles have

evolved a secondary adaptation to a marinehabitat. Seals and whales can handle theproblem of life in salt water because theirkidney can produce a highly concentratedurine. Elimination of the salts from sea wa-ter is well within the capacity of the mamma-lian kidney. Desert rodents, such as kangaroorats and jerboas, which have to conserve wa-ter, have kidneys that can excrete urine morethan twice as concentrated as sea water. Thereason that sea water is toxic to man is pri-marily that his kidney is not very efficient incomparison to other mammalian kidneys.The kidneys of birds and reptiles have a

concentrating ability which is considerablyless than that of the mammalian kidney, ap-parently because they contain no typical loopsof Henle. Birds, which can excrete a urinewhich is about twice as concentrated as theplasma, have some looped nephrons, but these

are not as highly developed as in mammals.Reptiles have no loops in their kidneys, thereis no countercurrent multiplier system, andtheir urine cannot be concentrated above theplasma concentration. As a consequence, ma-rine birds and reptiles cannot rely on thekidney for osmoregulation, and they appearto have a choice between avoiding the drink-ing of sea water and acquiring some meansfor salt excretion more efficient than theirkidneys.

Marine BirdsMany birds and a few reptiles have adapted

to marine life. Some birds come to land onlyto breed, and spend most of the year on theocean; others, such as the penguins, have be-come excellent swimmers and have lost thepower of flight. The emperor penguin is saidnever to come on land, not even to breed, butthis statement is merely a play on words, forthe emperor penguin hatches its eggs standingon the antaretic ice during the cold polarwinter. Many marine birds eat fish, whichcontain much water; this circumstance re-duces their problem of salt excretion. In fact,on a diet of fresh fish, cormorants have plentyof water to spare and do not need to drinkat all.' But other birds eat inivertebrateswhich are in osmotic equilibrium with seawater; gulls eat mussels, sea urchins andcrabs, eider ducks filter small organisms outof the water, some penguins eat large quanti-ties of krill, and so on. How do these birds,with their inefficient kidney, eliminate thesalt that is present in their food and in thewater they may drink? The aniswer is thatthey possess an accessory organ, a gland inthe head, which produces a concentrated saltsolution that drips off from the tip of thebeak.

This salt-seereting gland is highly devel-oped in all marine birds, as opposed to ter-restrial birds. The gland has long been knownto anatomists as the nasal gland; it is presentin all birds, but in terrestrial species it isvery small.2 The size of the gland in marinebirds is 10 to 100 times as large, a strikingdifferenee that was noticed long ago. The


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THE SALT-SECRETING GLAND OF MARINE BIRDS

usual interpretation has been that the fune-tion of the gland should be to rinse away theirritating and harmful effects of sea waterthat might penetrate into the nasal cavity.However, in all the marine birds that we haveexamined, the gland secretes a solution of so-dium chloride which is more concentratedthan sea water, and the exclusive function ofthe gland seems to be that of osmoregulation.The species which we have examined, whichinclude gulls, terns, auks, penguins, alba-trosses, petrels, cormorants, pelicans, gannets,herons and ducks, represent all the majororders of mariine birds; it seems logical, there-fore, to conclude that the salt-secreting glandis present in all marine birds.

It is interesting that the gland not onlyis large in marine birds, but that, to someextent, its size varies with the exposure to saltloads. Long before the function of the glandwas known, Schildmacher3 found that ducksbrought up with access to a 3 per cent saltsolution instead of fresh water developed anenlarged gland. However, after a careful dis-cussion of the apparently causal connectionbetween the size of the gland and salt water,Schildmacher repeated the mistake of the oldinterpretation, stating that the only possibleexplanation is that the gland protects thenasal mucosa against irritation.The change in the size of the gland with

the degree of exposure to salt was observedearlier by the Heinroths, who found that eiderducks which were reared in fresh water in theBerlin Zoo had smaller gland impressions ontheir skulls than individuals of the same spe-cies collected in the wild.4 However, the rela-tive ease with which the gland hypertrophieswith use and atrophies with disuse should notbe taken to mean that terrestrial birds candevelop a functional salt gland from theirnasal gland. This does not seem to be the case;only those birds that have an evolutionaryhistory of adaptation to a marine habitat seemto have evolved a gland of significant size, andseem to be capable of secreting hypertonicsolutions.With the apparently universal existence of


the salt gland in living marine birds, its pres-ence in fossil forms can safely be taken as anindication of a marine habitat. Some fossilbirds, such as Ichthyornis and Hesperornisfrom the Cretaceous period, have clear im-pressions on the skull where a large glandhas been located.5 These birds were fish eat-ers, and supposedly marine, and the presenceof the large gland in the same location as thesalt gland of living birds is a satisfactoryconfirmation of their marine life.

Marine ReptilesOnly a few reptiles live in the sea; they

represent 4 orders: turtles, snakes, lizardsand crocodiles. The great sea turtles eat fishor seaweed, and go on land only to lay theireggs on sandy beaches. They are known toshed tears as the eggs are deposited, evidentlya sign of osmoregulation, rather than pain.6The sea snakes (Hydrophidae) of the IndianOcean are truly marine; the more primitivelay their eggs on land, but the most special-ized bear living young and remain at seathroughout life. They are reputed to be themost poisonous of snakes, and their osmoreg-ulation has never been studied. A single liz-ard, the Galapagos lizard (Amblyrhyiichuscristatus) is marine; it lives on the beachesof the Galapagos Islands where it eats sea-weeds and occasionally blows a spray of drop-lets out through its nostrils, reminiscent of apuff of smoke from a fiery dragon. This harm-less creature is easily handled in the labora-tory, and it proves to have an osmoregulatorynasal gland that produces the salty fluidwhich is ejected from the nose. The marinecrocodile (Crocodylus porosus) has beenfound far out at sea, but normally it lives inestuarine swamps. A single specimen which Ihad in the laboratory did not respond to os-motic loads, and crocodile tears must still beclassed as one of the mysteries of biology.

TerminologyThe presence, but not the function, of the

salt-secreting gland has been known for cen-turies7 and received considerable attentionearly in the last century.'-10 It has been called

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the nasal gland (glandula nasalis), althoughit is not always found in what one would callthe nose. In most marine birds it is locatedon top of the head, above the orbit of the eye,and has therefore also been called the supra-orbital gland, or glandula nasalis supraorbi-talis. In the marine turtles the salt-secretinggland is seemingly of a different embryologicorigin. It is located in the posterior part ofthe orbit of the eye, and its duct opens in theposterior corner of the eyelids. This gland inthe turtle should, therefore, probably be re-garded as a modified lacrimal gland. It isinteresting that the gland of the turtle, inspite of its different origin, has the same his-tologic structure as the gland of the bird.

Since these glands, which anatomically arenot homologous, have the same function, theneed arises for a convenient terminology. Wehave therefore decided to call them salt-se-creting glands, or simply salt glands; thisdesignation, then, denotes any gland in thehead region of marine birds and reptileswhich, irrespective of anatomic origin, has aiiosmoregulatory function and secretes highlyhypertonic sodium chloride solutions.

Response to a Salt LoadThe effect of a considerable salt load in a

black-backed gull (Larus marin ts) is shownin table 1. In this case the bird, which weighed1,420 Gm., was given almost one-tenth ofits body weight of sea water by stomach tube.After about 3 hours the total volume of theexereta equaled the infused aimount, and allthe ingested salt had been eliminated. Inother words, a gull handles quite easily a saltload which could not possibly be tolerated byman.Some details of the relative importance of

the kidney and the salt gland are given intable 2. The total amount of fluid excretedfrom the salt gland was 56 ml., while in thesame 3-hour period 75 ml. was eliminatedfrom the cloaca, most of this latter beingurine. The concentration of sodium was uni-formly high in the nasal fluid, while it waslow in the cloacal fluid. Thus, the total amountof salt eliminated by the salt gland was about

10 times as high as the total cloacal excretion.In other words, in this particular experiment,the extrarenal excretion of salt was 10 timesas important as the renal excretion. In spiteof the salt load, the concentration of sodiumin the urine was low and tended to decreasefurther during the experiment, although thekidney has the capacity to excrete concentra-tions of sodium up to about 300 mEq./L. Thisdrop in the concentration of sodium in theurine after a salt load has frequently beenobserved in gulls, but in other species of birdsabout which we have similarly complete rec-ords of the effects of a salt load, the concen-trations of sodium in the urine have tendedto rise toward the concentration ceiling (about300 mEq./L.).

Composition of the Nasal SecretionThe fluid secreted fromi the salt gland is

very simeple. Except for epithelial cells andother debris in samples collected immediatelyafter the start of secretion, the almost neutral,watery liquid is clear and colorless. The dom-inating solutes are sodium and chloride inapproximately equivalent amnounts (table 3).There is a relatively small amount of potas-sium, some bicarbonate, and almost nothingelse. Magnesium and sulfate, which are pres-ent in sea water in rather high concentrations,are virtually absent from the nasal fluid. Theamount of organic material, including urea,is very small. Phenol red, which apparentlyis excreted by all kidnevs, is not secreted bythe nasal gland and does not appear in thefluid.

Concentration of the FluidThe activity of the salt gland is an all-or-

none phenomenon. If there is an osmotic load,the gland secretes; in the absence of an os-niotic load, the gland is at complete rest. Inthis intermittency, the gland differs from thekidney which produces urine continuously.The concentration of salt in the nasal secre-tion is always very high, and remains fairlyconstant for each species (table 4). Thereseems to be a clear connection between theconeentrating ability of the salt gland and

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Table 1The Total Excretion of Water and Salt in a Black-Backed Gull After a Load of Sea Water by Stom-ach Tube

Body weightSea water ingestedExereta, total volume in 3 hrs.Sodium ingestedSodium excreted in 3 hrs.

1,420 Gm.134 ml.131 ml.54 mEq.48 mEq.

Table 2Nasal and Cloacal Excretion by a, Black-BackedGull During the 175 Minutes Following the Inges-tion of Sea Water (see Table 1)

Nasal excretion Cloacal excretion

Sodium Sodium Sodium SodiumTime, Vol., conc., amount Vol., conc., amount,min. ml. mN mEq. ml. mN mEq.

15 2.2 798 1.7 3.8 38 .28

40 10.9 756 8.2 14.6 71 1.04

70 14.2 780 11.1 25.0 80 2.00100 16.1 776 12.5 12.5 61 .76

130 6.8 799 5.4 6.2 33 .21160 4.1 800 3.3 7.3 10 .07175 2.0 780 1.5 3.8 12 .05

Total 56.3 43.7 75.2 4.41

Table 3Typical Composition of the Fluid from the Salt-Secreting Gland of Herring Gulls

Na+ 718 mEq./L.K+ 24 mEq./L.Ca++ + MIg++ 2.0 mEq./L.

Cl- 720 mEq./L.HCO3- 13 mEq./L.*S04-- 0.68 mEq./L.

*Dr. Maren has kindly permitted me to quote aver-

age figures obtained in his laboratory. For nasalsecretion these are: HC03-=9.1 mEq./L., pH=7.03;and for plasma: HCO3-=21.7 mEq./L., pH-17.48.

Table 4Usual Concentration of Sodium in the Nasal Secre-tion of Different Species of Birds*

Species

Cormorant, double-crestedDuck, mallardSkimmer, blackEider duck, common

Pelican, brownGull, herringGull, black-backedPenguin, Humboldt 'sGuillemotAlbatross, blackfootedPetrel, Leach 's

Concentration ofsodium, mEq./L.

500-600(550)

550-700(625)

600-750600-800700-900725-850750-850800-900900-1,100

the feeding habits of the bird. For example,in the cormorant, which eats fish that is rela-tively low in salt content, the concentrationin the secretion from the gland is about 500to 550 mEq./L. and rarely exceeds 600mEq./L. In the herring gull, which consumes

more invertebrate food, and consequentlymore salt, the concentration is usually between600 and 800 mEq./L.; the great black-backedgull which is more marine in its habits, hasconcentrations between 700 and 900 mEq./L.The petrel is a bird with pronounced oceanichabits. It spends most of its life at sea andcomes to land only to breed. It lives on plank-tonic organisms, mostly crustaceans, which itpicks off the surface of the ocean as it flies by.The planktonic organisms, being inverte-brates, have the same osmotic concentrationas sea water and therefore impose a consid.erable salt load. It is no surprise, therefore,that in the petrel the salt concentration ofthe nasal fluid is higher than in any other


*Some samples fall outside these limits, which rep-resent only the usual range. Numbers in paren-theses represent species in which samples have beentoo few to establish a normal range.

bird we have examnined, up to 1,100 or 1,200mEq./L.No other gland in higher vertebrates, ex-

cept the mammalian kidney, can producefluids which are concentrated to this degree.The concentration limit for electrolytes inthe kidney of man is about 400 mEq./L., inthe rat 600 mEq./L., in the kangaroo rat,1,500 mEq./L., and in the champion concen-trator, the North African rodent Psammomys,1,900 mEq./L. Thus, the salt gland comparesfavorably to the kidney in its concentratingability. In other respects the salt gland isquite different from the kidney; it secretesonly sodium chloride, it always produces aliquid which is highly hypertonic to the blood,and it works as an all-or-none system, becom-ing active only after an osmotic load.

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Table 5A Comparison Between the Rate of Secretion from the Salt Gland of the Gull and theVolume of Urine During Water Diuresis in Man

Flow per Kg. body weight:

Flow per Gm. gland:

Salt gland, herring gullKidney, water diuresis, manKidney, GFR, man

Salt gland, herring gullKidney, water diuresis, manKidney, GFR, man

Volume of FlowAlthough the concentration of the nasal

secretion is relatively constant, its volume isnot. The rate of flow can change from zero

to a maximum which varies with the speciesand, to some extent, between individualswithin the species. After a salt load is givento a bird, the rate of flow rapidly increases,and remains rather high for a period thatdepends on the degree of the load. It thentapers off and diminishes as the salt is elim-inated (table 2). However, the rate can re-

main at near-maximal levels for hours. Thatthis rate is quite high becomes clear whenthe flow from the gland in the gull is com-

pared wth the flow of urine during water di-uresis in man. In table 5 flows are calculatedper kilogram of body weight. It may be seen

that although the osmotic concentration ofthe nasal secretion is high, the production ofnasal fluid is more thall twice the maximumwater diuresis in man.

Size of the Gland and Flow RateWhat is the size of a gland which has this

amazingly high excretory capacity? Its size isnot very impressive compared to the kidney;in the gull, which has a relatively large saltgland, it is about 0.1 per cent of the bodyweight, while the kidney of mammals ap-

proaches about I per cent of the body weight.Thus, if we relate the volume of secretion tothe weight of the gland rather than to bodyweight, the capacity of the salt gland becomeseven more striking. The gland of the gull can

produce about 0.5 ml. of fluid per Gm. ofgland per minute. The glomerular filtrationrate in man is about 0.2 ml. per Gm. of kidneyper minute and in the rat, I believe, about

0.3nml. per Gm. of kidney per minute. Inother words, despite the considerable osmoticwork necessary to produce the concentratedfluid, the salt gland can secrete at a ratewhich is as high as, or higher than, the glo-merular filtration rate in the mammaliankidney.

Structure of the GlandWhat is the structure of this unusual gland

which produces fluid as fast as the kidneyfilters the plasma? Figure 1 shows the loca-tion of the gland in the gull. On top of theskull there are 2 crescent-shaped, flat glands,which are located in shallow depressions inthe bone. Actually, each gland consists of 2parts which are so similar in structure andare so closely joined that they can be consid-ered as one funetional unit, i.e., as one gland.'1Two ducts run from each side down to thenose where they open at the vestibular concha.From the anterior nasal cavity the secretionflows out through the nares and drips off fromthe tip of the beak. A few marine birds haveclosed and nonfunctional external nares;characteristically these birds, e.g., gannetsand cormorants, are good divers and enter thewater after a fast dive from some height. Theclosed nares probably are a protection againstthe penetration of water at the time of impactwith the surface. In these birds the nasal se-

cretion flows through the internal nares alongthe roof of the mouth, forward to the tip ofthe beak.The glands consist of longitudinal lobes,

which in cross section show tubular glandsradiating from a central canal (fig. 2). Exceptfor the most distal portion where the cells are

somewhat smaller but of the same general


0.5 ml./mimi.0.24 ml./min,1.8 ml./min.0.6 ml./mini.0.03 ml./min.0.2 ml./min.

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Figure 1The 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 glandshave a rather uniform structure throughouttheir length. The tubules are closed in the dis-tal end, and there is no structure reminiseentof the glomerulus of the kidney. The struc-ture is characteristic of a tubular gland, whichindicates that the secreted fluid is elaboratedonly by simple glandular secretion, and that'there is no ultrafiltration of fluid comparableto that in the kidney. This conclusion is sup-ported by the fact that inulin does not appearin the secretion.A retrograde injection of india ink into the

gland through its duct shows that the inkpenetrates all the way into the cells, givingthe appearance of intracellular canialiculi.which probably have a secretory function.Electron micrographs made by Dr. W. L.Doyle at the University of Chicago, as well asby other investigators, show that there aredeep infoldings both in the apical and thebasal parts of the secreting cell, which hassome similarity to the tubular cell of thenephron. It must be assumed that the deepinfoldings are intimately related to the fune-tion of the cells, and it could be suggestedthat the elaboration and transport of fluiddoes not necessarily take place as a tranls-tubular process. If the infoldings prove to besimilar to the interdigitations of the renalCirculation, Volume XXI, May 1960

tubular cells as reconstructed by Rhodin, thetransport process might indeed take place inlthe intereellular spaces of interdigitatingcells, rather than across the cell body. Thesestudies are being continued by Dr. Doyle andwill be published elsewhere.

Blood Supply to the GlandThe gland receives its main arterial blood

supply from the arteria ophthalmica interna.In the gull, several blood vessels penetrate thebony wall of the orbit and enter the glandfrom below. This makes the blood vessels diffi-cult to reach, and attempts at perfusion ofthe gland are likely to lmeet with immensetechnical difficulties.The circulation in the lobes of the gland

can be visualized most easily in preparationswhich have been prepared by the injectionof the vascular system with india ink.1' It isfound that the main arteries to the glandbranch into interlobular arteries, which sendsmaller branches into the single lobes. Thesearteries continue toward the central canal,where they split up into capillaries whichrun parallel to the tubular glanids toward theperiphery of the lobe. A section cut perpen-dicular to the tubular glands (fig. 4) showsthat the capillaries are interspersed betweenthe glands, much as in the papilla of the kid-

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Figure 2 Figure 3AThe salt glatndi of the quttI-11cosists of longitudinal It crossss tion tMc loOr of the eodlt-setreting glalnlobes afbout .1 mm. i"n (liha teter; each lobe has a shows th.e u tItot coito l 1(te rodiol arrattyccentral canaltl uwtih the broiuching secretorY tubtules tucut of the sectvtottj tub olc. I the lo rightarranged rahially aroantd it. (Irauwing by 31. han oro r on tt ?obalott tin and at otIs rqCe)o(iint-Vivas.) ( itt le.

nley wihcir thle vasa reet a are interspersed between the limibs of Ilfele's loop. A diagram.of the eireiflation (fig. 5) shlows howv the bloo(dflovs parallel to, blut iii the opposite tireetiot)fr omii, the flow in dlie tulbular glancd.

Is There a Countercurrent Systemin the Salt Gland?

Tileo arrangement jlust deseslibed cani, otcolilse,be recog'n1ized asaI countercurrent flow,and n-to r-enial physiotlogist is unawvare of theinuportance of the counttereurreiit multijtiiersystel iii the elal)oration of a concentratedurinle in tlhe kidney. Iloowever, iii the ease ofthe salt gland,I thel cottitercurreiit flow cannlotbe used to explain thie elaboration of a eoi-centrated fluid. A countercurrenlt mlultipliersysteni consists of a tuIbD whliehli lhas beenitu-rned back on-t it:sel f to formi a loop) butin the salt glancd we have 2 unconnected tubesruinnigo in opposite direct ions. This is tvpicalfor a type of couiniter-currenit exchiange s-stemiiwvhieh is iiartieularly well suited for obtainingthe same concentration in the oitg(oing(, fluidilhovm onle tube as in the iiieoming fluIid i; theother (fig. 6). Il other wvords, the systenm inthe salt glaind seems ideal for the elaboration

Figure 3BIn higher mnigfnicjhtion the pelhertol ettds ofthle scc 1 torj1 tol (tlc op)ycotr (Os clou)Cd tn-b)Cs wllith-oalt a ji. titiuriitq to hlt( 1loturlo oppottlus ofthe litlitct. 101 tt'eve, thl petiphetar por)a?t of tAtetabule hos stiallr clls otid aitt 0ppe(t'r(ttte w,7hich(IilrettS I to ttt tltt to t (C)tcft? tot potts.

of a1 secretion which is isotonic, with plasma,awln tlhe highi (coneentra,Ctions wviichi are ac-tuallly pI oduee(d rinolesult fu1'n a counter-einre-it mul-lltiplier systein.

It is truel( that tI-le direction of the bloodflow may be opposite lo what wve have as-sumed for there is alwvays soniic doubt abolut

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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. Buteven if the 1)00(I1o flowiwere thte reverse of wx-hatwe have sugg(,este(, with the flow in the samedirectioll as the fluid inl the gklanid, the ar-rangemeut woil(d still nlot be a muiltipliersystem. AVe mullst therefore conch(lude thiat,altlhough there is a countercurrent flow, thecountercurrent multiplier prineijle cann-ot beused to exl)lain the functioni of thils partieularglanid anid its ability to elabor:(ate high-ly coil-centrate(I soluitionis.

Nervous ControlThe nerve supj)ly to the salt g1land( is ratlher

eom)lex anld not easilv workced out becausethe nierves iii the head of tlhe l)ird have acomiplex course witli frequenit ranastomoses.The gland is inniiervated from a g,anglion inthe orbit, t-he gancglion ethraoidale. This gan-glionl is supplied by a relatively lalrge branchof the ophtlhalieni erve, and a smnaller onieCirculation, Volume XXI, May 1960

[ orin llbe faci.l nerve,7 as, well as ly symplla-thletfi fibers. Apparently nominyelinated fibersfromlw thle gainglion penetrate the bone to reachlthe glaud. Electrie stimnulatioii of the oplithlil-imuie nerve cauises nio secretioni, but if the small.braneh froim the facial nerxve is stimnulated, a

fluid of the usuial compositiol, rich itn sodiumchloride is secreted. As far as we can establish,the br-anch of the facial nerve conthinues backtowai(I the ininer ear; it is reminiscent of, antdeould be homologrous to, the clhorda tynupanixlhieh stimlIIates sdlivax y seeretion in1 niamn-mals.Thc secretory nerve apparently is parasyin-

pathetic in natur1e2.0 Stimiiulatioin of the cervi-cal symnpatlhetic chain causes nio seeretioni andin.jeetiori of epinephlinie blocks secretion fromfthe gland. Accttleholine, if injected in a prox-imal artery, causes the gyland:I to secrete; ifinjected in the genieral eireulationl it will, of

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SCHMIDT-NIELSEN

Figure 5The arrangement of the blood vessels and capillaries in the lobes of the salt glandindicates that the capillary blood flow is countercurrent to the flow of secreted fluid inthe secretory tubule. (Drawing by M. Cerame-Vivas.)

course, be hydrolyzed before it reaches thegland. The parasympathomimetic substancemethacholine (Mecholyl) also causes thegland to secrete.

Effect of AnesthesiaOne difficulty in the study of the function

of the salt gland is that the secretion isblocked by anesthesia. Secretion can alwaysbe induced in the nonanesthetized bird by anosmotic load, for examnple by the injection ofhypertonic sodium chloride. Within a fewminutes, somnetimes within 1 minute of an in-jected load, secretion will begin. However,since anesthesia immediately blocks secretion,many further experiments, in particular thoseinvolving surgical procedures, cannot be car-ried out.

Osmoreceptor ReflexThe effects of anesthesia, of nerve stimula-

tion, and of osmotic load, indicate a sequenceof control as suggested in figure 7. The term

osmoreceptor is used, rather than salt recep-tor, because the gland responds not only tosalt loads, but to osi-otic loads in general. Ifa hypertonic solution of a nonelectrolyte suchas sucrose is infused, the gland begins to se-crete a fluid of the usual composition, with ahigh concentration of sodium chloride. Thisindicates that the secretion occurs in responseto an osmotic load, rather than to the concen-tration of sodium or chloride in the plasma.

Carbonic Anhydrase in the Salt GlandIt has frequently been proposed that car-

bonic anhydrase plays an important role inionic transport nmechanisms. Since the saltgland is an organ which apparently has noother funetion than the transportation ofsodium chloride, it seems well suited to astudy of the possible role of this enzyme inthe mechanism of transport. Many schemeswhich have been suggested to accounit forionic transport involve bicarbonate and car-


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100I

1000 L I MI

COUNTER CURRENT FLOW 0Q LIMIT

AO0°

PARALLEL FLOW 50g LIMIT

50' LIMITFigure 6

Top. Thermal models indicate how the heat flow in a countercurrent exchange systemleads 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. Thesemodels assume equal volumes of flow in the 2 tubes. If the flows differ the limits changeaccordingly, but in no case can a passtve exchange system increase the temperature inthe 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 thatthe 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, blocksthe secretion almost instantaneously.12 Thisresult indicates that carbonic anhydrase isessential to secretion, but it does not prove

that the block is in the ionic pump of the se-

creting cells. A possible explanation is thatthe block could be somewhere else in the path-way indicated in figure 7. To examine thispossibility experiments were done to deter-mine if the gland retains its ability to secretein the presence of the enzyme inhibitor. Thishas actually been found to be the case: directstimulation of the gland with methacholinegives a secretion of the usual composition,showing that the ionic pump can work in thepresence of a carbonic anhydrase inhibitor.Another possible interpretation, however, is


that the inhibition of the secreting cells is amatter of relative concentrations, and that, ifthe stimulus is strong enough, the gland startssecreting in spite of the presence of the inhibi-tor. Further work on this point has been doneby Dr. James Larimer, a former student ofmine, in Dr. AMaren's laboratory.

The Role of Acetylcholine in SecretionIt is possible that the parasympathetic na-

ture of the gland affords a clue to the mecha-nism of ion transport. The secretion occurs inresponse to the release of acetylcholine fromthe stimulating nerve. This pattern is reminis-cent of other systems in which acetylcholinehas an important influence on the movementof sodium, such as in the depolarization of themuscle fiber and of the nerve fiber. Recently,the Hokins of the University of Wisconsinhave demonstrated that slices of the salt glandin vitro, when incubated with acetyleholine,show a greatly increased turnover of phos-phatidic acid, as evidenced by radiophos-

100°

QO

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SCHMIDT-NIELSEN

CNSOSMORECEPTOR

GANGLIONETHMOIDALE

SECRETORYTUBULE

KO -(

OSMOTICSTIMULAT ION

*4\ ~~~/

A\ACETYL I-,'CHOLINE

Figure 7Suggested sequence of events in the osmoticsalt gland.

phorus tracer experiments.13 The Hokins sug-gest that phosphatidic acid is an integral partof the sodium pump in the gland, and that itmay be the actual ionic transport agenlt itself.

In a recenit series of papers'4-16 Scothornehas described histologic and histochemicalstudies of the nasal gland of ducks andpigeons. The gland of the domestic duck, likethat of the mallard, its wild ancestor, doessecrete salt, but the gland of the pigeon doesnot. In the gland of the duck there is a mod-erate amount of alkaline phosphatase, and ahigh content of suceinic dehydrogenase. Notall glands have a high conitent of succinic de-hydrogeniase; it seems probable that the pres-eniee of this enzyme in the salt gland nmay beclosely related to the energy which is re-quired to perform an exceptionally high levelof osmotic work.

Obviously, much work remains to be doneon this unique gland, which apparently has11o other function than that of transportingsodium chloride and therefore seems to beeminently suited for studies of processes in-volved in ionic transport. I believe that it istoo early to say whether the transport is dueto a sodium pump or to a chloride pump. Mypersonal guess is that it may be a chloridepump, but I have no real support for this no-tion except that the proportion of sodium topotassium in the secreted fluid may indicatethat the cation follows passively. In eithercase, I expect that future work will answer

stimulation of secretion from the avian

the question. At this time I can only say thatif there is any organ in which an ionic pumpand its metabolic ramifications can be studiedin its pure form, the salt gland of marinebirds almost seems to be designed for this pur-pose.

References1. SCHMIDT-NIELSEN, K., JORGENSEN, C. B., AND

OSAKI, H.: Extrarenal salt excretion in birds.Am. J. Physiol. 193: 101, 1958.

2. TECHNAU, G.: Die Nasendrfise der V6gel. J.Ornithol. 84: 511, 1936.

3. SCHILDMACHER, H.: Ueber den Einfluss des Salz-wassers auf die Entwicklung der Nasendriisen.J. Ornithol. 80: 293, 1932.

4. HEINROTHv, O., AND HEINROTH, M.: Die V6gelMitteleuropas in allen Lebens- uid Entwick-lunigsstufen photographisch aufgenommen undin ihrem Seelenleben bei der Aufzucht vom Eiab beobachtet. 3 vols. Berlin, H. Bermilhler,1926-1928.

5. MARPLES, B. J.: Structure and development ofnasal glands of birds. Proc. Zool. Soc. London.1932, p. 829.

6. SCHMIDT-NIELSEN, K., AND FANGE, R.: Saltglands in marine reptiles. Nature 182: 783,1958.

7. COMELIN, C.: Collegium privatum Amsteloda-mense. Amsterdam, 1667. Quoted by TechnauiY

8. JACOBSON, L. L.: Sur une glande conglomeree ap-partena ate a la cavite nasale. Bull. Soc.Philom. Paris 3: 267, 1813.

9. NITZSCH, C. L.: Ueber die Nasendriise der V6gel.Deutscli. Arch. Physiol. 6: 234, 1820.

10. JOBERT, C.: Recherches anatomiques sur lesglandes nasales des oiseaux. Ann. Sci. Nat.,ser. 5, 11: 349, 1869.


b, NA CLS ECRETION

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11. FANGE, R., SCHMIDT-NIELSEN, K., AND OSAKI,H.: Salt gland of the herring gull. Biol. Bull.115: 162, 1958.

12. -, -, AND ROBINSON, M.: Control of secretionfrom the avian salt gland. Am. J. Physiol.195: 321, 1958.

13. HOKIN, L. E., AND HOKIN, M. R.: Evidence forphosphatidic acid as the sodium carrier. Na-ture 184: 1068, 1959.

14. SCOTHORNE, R. J.: The nlasal glands of birds: A

histological and histochemical study of the in-active gland in the domestic duck. J. Anat.93: 246, 1959.

15. -: On the response of the duck and the pigeonto intravenous hypertonic saline solutions.Quart. J. Exper. Physiol. 44: 200, 1959.

16. -: Histochemical study of suceinic dehydro-genase in the nasal (salt-secreting) gland ofthe Aylesbury duck. Quart. J. Exper. Physiol.44: 329, 1959.

Water as a Substrate for LifeWater, 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 whiehhas 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 allliving things, or in any other of the countless physiological functions which it performseither automatically or as a result of adaptation.-L. J. Henderson. The Fitness of theEnvironment. Boston, Beacon Press, 1958, pp. 131-132.


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KNUT SCHMIDT-NIELSENThe Salt-Secreting Gland of Marine Birds

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