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The Function of the Salt Gland in the Brown Pelican

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The Function of the Salt Gland in the Brown Pelican 282 LVol.r 75 THE FUNCTION OF THE SALT GLAND IN THE BROWN PELICAN BY KNUT SCHMIDT-NIELSEN AND RAGNAR I•'ANGE It has long been a matter of speculationhow oceanicbirds cover their needs for water. Some marine birds remain at sea for weeks or months,hundreds of miles from land and any possiblesources of fresh water. Sea water is known to be toxic to man and most other mammals, the reasonbeing its high salt content. Someauthors have statedthat marine birds do drink sea water (Murphy, 1936: 337), while others have maintainedthat they can subsistwholly on water obtainedfrom the food (Smith, 1953:163). In order to profit from the ingestionof sea water it is necessaryfor an animal to excrete salts in a concentrationat least as high as that in the water ingested. The eliminationof the salt would otherwise require an additional amount of water which would be taken from the bodytissues. Therefore, if the organismcannot excrete a highlycon- centratedsalt solution,the drinking of sea water only will lead to a progressivedehydration or a harmful accumulationof salt. The bird kidneyis ableto excretesalts in a concentrationonly about one-halfof that found in seawater. Hence, if the bird kidney should excrete the salts from a given amount of sea water, it would be neces- sary to producetwice as much urine as the amount of water ingested. Thus, the kidneyis not ableto keepa marinebird in a favorablewater balance if it drinks sea water. However, it was recentlydiscovered that in marine birds a major part of the ingestedsalt is excretedextrarenally. The nasalglands, or salt glands,are able to producea highly concentratedsalt solution, makingit possibleto toleratedrinking of sea water (Schmidt-Nielsen ½t al., 1957, 1958). Cormorantsas well as a number of other marine birds have been found to secretesalt in high concentrationsfrom the salt gland, and there is little doubt that this is the generalavenue for salt excretion in all marine birds. This function is well correlated with the size of the salt gland, which is large in marine birds, as contrasted with terrestrialbirds, which have a very smallnasal gland. Our findings on the functionof the salt glandin the Brown Pelicanare here reported. MATERIALS AND METYIODS The experimentalanimals were commonBrown Pelicans(Pelecanus occidentaliscarolinensis). They were caught on the Gulf Coast of Florida immediatelybefore being broughtto the laboratoryfor the physiologicalstudies. Altogether eight birds were used, four with •J•l•] S½}•M•)x-N•zLSZ•^N•)F^NaE, Salt Gland inBrown Pelican 283 mature plumage (average weight 3.36 kg.), and four with juvenal plumage(average weight 2.59 kg.). Most of the birds were unwilling to eat in captivity,and force feedingresulted in vomiting. The experi- mental work was therefore done on fasting animals. The purposeof the investigationwas to establishwhether the salt gland plays the samerole in salt excretionin the pelicanas it doesin other marinebirds. Stimulationof the gland was accomplishedin two different ways, either by imposinga heavy salt load by infusion of hypertonicsodium chloride solution, or by injection of a solutionof mecholyl,a syntheticdrug with an effectsimilar to that of parasympa- thetic nerve stimulation. Although these stimuli do not correspond preciselyto the normal situationthe bird meetsin nature, the salt load is an exaggeratedrepresentation of the physiologicaleffects of ingestion of sea water, and the mecholylinjection simulatesthe action of the secretorynerves that normallycontrol the gland. All injectionswere made intravenouslyin the foot of unanesthetized birds. We have found in other speciesof marine birds that anesthesia blocksthe normal responseof the gland to a salt load. Samplesof the secretionfrom the salt gland were collectedby meansof thin poly- ethylenetubings introduced one or two mm into the narrow external nares. Occasionalsamples were taken of urine and of lacrymal fluid for comparativepurposes. The sodiumand potassiumcontent of the sampleswas determined by meansof a flamephotometer, and chlorideby a modificationof the Volhardtitration method (Rehberg, 1926). RESPONSETO A SALT LOAD A salt load was imposedby injectionof variousamounts of a 10• sodironchloride solution in four pelicans (2 adult and 2 juveniles). Within 1 to 5 minutesafter the injection,drops of a clear, water-like liquid appearedat the externalnares. The liquid ran downalong the grooveson the upper side of the beak until it reachedthe tip of the beak,where it drippedoff. The headshaking which was characteristic in the behavior of cormorantsduring secretionfrom the salt gland (Schmidt-Nidsen,½taf., 1958) was not observed in pelicans.The secre- tion continued for some one to two hours. In a typicalsalt load experimentwith a pelican(2.54 kg. body weight) 28 ml of a 10• NaC1 solutionwere injectedintravenously. Within one minute of the beginningof injectionthe nasal secretion had started.During an initlaJperiod of 7 minutesthe rate of secretion increasedrapidly. When it had reacheda high level it continuedat a rather constantrate for 110 minutesand then declinedabruptly and 284 SCHMIDT-NIELSENANDFANGE, Salt Gland in BrownPelican tVol[ Auk75 ceasedaltogether during the next 15 minutes. Except for the terminal observationperiod the flow remainedbetween 0.26 and 0.31 ml/minute (seetable 1). TABLE 1 VOLUME AND COMPOSITION OF NASAL SECRETION IN A PELICAN SUBJECTEl)TO SALT LOAI) Time, Vol. o] secr. ml per Conc.mEq/liter min. Min. ml. min. Na Cl K O-7 7 -- -- 65O -- 11 7-17 10 2.885 0.29 637 656 10 17-27 10 2.686 0.27 700 695 12 27-37 10 2.997 0.30 764 850 15 37-57 20 6.155 0.31 736 740 16 57-77 20 5.879 0.29 721 730 14 77-97 20 5.209 0.26 704 708 14 97-117 20 5.119 0.26 696 704 13 117-132 15 2.815 0.19 676 694 14 Total: 33.745 Aver.: 0.27 698 722 13 The total amount of liquid secretedfrom the salt gland in this experimentwas 33.75 ml. In the same period four sampleswith a total volume of about 22 ml of cloacalcontents were passed(most of this was only slightlycontaminated with fecal material). The amount of liquid producedby the salt gland therefore exceededthe amount producedby the kidney. However, the important differencein the roles of these two organs appearswhen the salt concentrationsare compared. While the average salt concentrationin the nasal secretionwas over 700 mEq/liter (ab. 4 g NaC1per 100 ml), the averageurine concentra- tionswere about250 mEq/liter (ab. 1.5 g NaCI per 100 ml) (see table 2). With the smallervolume of urine and its much lower salt concen- TABLE 2 VOLUME AND COMPOSITIONoF URINI• SAMPLES DISCIIAR(;E1) DURIN(; TIlE EXPERI]';IENTDESCRIBED IN TABLE 1 Urine vol. Conc.mEq/1 ml Na Cl K 6.7 222 251 18 7.1 207 205 7 5.9 261 316 38 1.9 156 269 52 21.6 212 260 29 July1958/-] SCHMIDT-NIELSENANDFANGE, Salt Gland in BrownPelican 285 trations, it appearsthat the amount of salt eliminatedby the kidney is about one fifth of the total, while about four-fifths of the salt was excretedfrom the salt gland in the observationperiod of slightlymore than two hours (see table 3). In this connectionit is desirableto emphasizethat the salt load imposedin this experiment was in the form of a salt solution about three times as concentrated as sea water. Such loads would not occur in nature. The total volumeof nasalsecretion (33.75 ml) exceededthe injected volume of salt solution (28 ml). Its concentrationof salt (ab. 700 mN), althoughnot as high as in the injectedsolution (1710 mN) was well abovethat of seawater (ab. 550 mN). In other words, the salt glandhas the capacityto excretethe saltscontained in ingested sea water. TABLE 3 THE AMOUNTS OF SALT EXCRETEDIN A PELICAN DURING TWO HOURS AFTER INJECTIONOF A SALT LOADOF 28 ML OF 10% NACL SOLUTION N aC l Nasal Renal Total injected excretion excretion excretion Volume, ml 28 34 22 56 Total NaC1, mEq 47.9 23.9 5.3 29.2 Total NaC1, gram 2.8 1.4 0.3 1.7 RESPONSETO OTHER STIMULATION Previous work on cormorants has shown that the secretion from the salt gland is stimulatednot only by a load with sodiumchloride, but also by a generalosmotic load in the absenceof increasedsalt concen- trations(Schmidt-Nielsen et al., 1958). This was shownby the injection of hypertonicsolutions of sucrose,which stimulateda secretionsimilar to that observed after a salt load. Studieson gulls,which will be describedin anotherpublication, have shown that the innerration of the salt gland is of parasympathetic nature,and that secretionfrom the gland can be stimulatedby mecholyl (methacholinechloride), a drug that mimicsparasympathetic stimula- tion and causessecretion from a numberof glands. It was thereforeof interestto comparethe stimulationby mecholylin the pelicanwith its effect on gulls. Mecholyl was injdcted intravenouslyin amountsof from 0.1 mg to 0.17 mg per kg body weight. Secretionfrom the salt glandsas well as secretionof tear fluid startedimmediately and con- tinuedfor periodsup to ten minutes.The rate of secretionfrom the salt glands was rather low, the highestrate observedunder mecholyl 286 SCHMIDT-NIELSENANDFANCE, Salt Gland in BrownPelican LVol.I' Auk stimulationwas 0.17 ml/minute for a five minuteperiod. I-Ienee,some samplesobtained were too small for completeanalysis, but sodium determinationscould be madeon five samples.These ranged from $90 to 750 m]•q Na/liter (aver. 652 m]•q/1). In other words, the con- centrationwas similar to that obtainedby a salt load (see table 1). Potassiumwas from 10-18 m]•q/1, and chloride from 632 to 708 mEq/1. The mecholylstimulation also providedan opportunityto obtain samplesof lacrymalfluid. In the three samplesobtained the sodium concentrationswere 52, 83 and 93 mEq/liter, respectively.This is lower than the sodiumconcentration of the plasma,which is about 150 to 160 mEq/liter, and it clearly showsthat the glandsthat produce the lacrymal fluid have no role similar to that of the salt gland in the excretion of salt.
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