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Relative Passage Rates of Lipid and Aqueous Digesta in the Formation of Stomach Oils

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Relative Passage Rates of Lipid and Aqueous Digesta in the Formation of Stomach Oils RELATIVE PASSAGE RATES OF LIPID AND AQUEOUS DIGESTA IN THE FORMATION OF STOMACH OILS DANIEL D. ROBY,• KAREN L. BRINK,2 AND ALLEN R. PLACE3 •CooperativeWildlife Research Laboratory and Department of Zoology, SouthernIllinois University, Carbondale, Illinois 62901 USA, 2P.O. Box 571, Carbondale,Illinois 62903 USA, and 3Centerof MarineBiotechnology, University of Maryland,Baltimore, Maryland 21202 USA ABSTRACT.--Weused tritium-labeled glycerol triether as a nonabsorbablelipid-phase mark- er and carbon-14labeled polyethylene glycol as a nonabsorbableaqueous-phase marker to examine gastrointestinaltransit of a homogenized fish meal fed to 4-week-old chicks of AntarcticGiant-Petrels (Macronectes giganteus) and GentooPenguins (Pygoscelis papua). Both aqueous-phaseand lipid-phase markers passedthrough the gastrointestinaltract without being metabolized.Label recoveries from the two specieswere statisticallyindistinguishable. Mean retention time was significantlylonger for lipid-phasecomponents than for aqueous- phasecomponents in both species.In the petrel, mean retention time for lipid-phaseand for aqueous-phasewas significantlylonger than in the penguin. Interspecificdifferences in retention were largely the result of differing ratesof gastricemptying. Both markersemptied rapidly from the proventriculusand gizzard of the penguins,while in giant-petrelsthe lipid- phase was retained for extended periods in the stomach.Differential transit of lipid and aqueousphases coupled with the lower rate of gastricemptying in giant-petrelchicks provides a physiologicalbasis for accumulationof dietary lipids in the proventriculus. The large, distensibleproventriculus and the ventral positionof the pyloric valve relative to the gizzard and proventriculusare morphologicaltraits which enhance the formation and retention of stomachoils. Received31 May 1988,accepted 19 December1988. OFall avian internal organs,the range of mor- (Matthews 1949, Duke et al. 1989). In other birds phologicalvariation in the stomachis the great- the much smaller proventriculus is cranial to est. This reflectsboth widely differing dietary the gizzard. habits and the importance of the stomach in With the exception of diving petrels (Pele- processingsolid food items (Ziswiler and Far- canoididae), all members of the Procellariifor- ner 1972). The avian stomach consists of two messtore lipids ("stomachoils") in the enlarged chamberswhich are externallydistinguishable proventriculus. The origin of stomachoils was in most species(McLelland 1979). The glan- previously thought to be secretory(Matthews dular proventriculus is continuous with the 1949, Lewis 1966), but evidence is now com- esophagusand secretesgastric juice. The giz- pelling for a dietary origin (Cheah and Hansen zard or ventriculusis caudalto the proventric- 1970, Warham et al. 1976, Clarke and Prince 1976, ulusand functions as the siteof gastricproteoly- Imber 1976). The function of stomach oils has sisand, in manyspecies, of mechanicaldigestion been viewed primarily as an energy and water (Duke 1986b). reserve and secondarily as a defense against In procellariiforms (petrels, fulmars, shear- predators (Warham 1977, Jacob1982). Previous waters,and albatrosses),the mostpelagic avian work (Roby et al. 1986a,Place and Roby 1986, order,the division betweenthe proventriculus Duke et al. 1989) indicated that petrels retain and gizzard is readily apparent. Forbes(1882) lipids in the proventriculus longer than sea- describeda distensibleproventriculus that con- birds without stomachoils. This suggeststhat, sistedof a largesac with a fundus,a smallgiz- for seabirdsthat store stomachoils, gastroin- zard twisted so that the pylorus facesback in- testinal passagerates for lipid digestaare con- steadof forward,and an ascendingloop of the siderablylower than thosefor aqueousdigesta. duodenumbefore the descendingand ascend- However, there are no publishedreports of rel- ing limbs.The proventriculusmay be so large ative passagerates of lipid and aqueousdigesta when distended with food that it extends cau- in birds;hence, there is no basisfor comparison dally in the bodycavity well beyondthe gizzard with those speciesthat store stomachoils. 303 The Auk 106: 303-313. April 1989 304 RoB¾,BRINK, AND PLACE [Auk,Vol. 106 Nonabsorbablemarkers are widely used to ratesand gut morphologyin penguinsand pe- monitor movementof a specificphase along the trels, we hoped to elucidate mechanismsre- gastrointestinaltract. They are also used to es- sponsible for stomach oil formation in the lat- timate nutrient absorptionfrom or secretioninto ter. a marker specifiedphase. It is important that the marker have properties similar to compo- MATERIALS AND METHODS nents of the phaseunder study (Wiggins and Radiolabelsand fiuors.--We used [•4C]-polyethylene Dawson 1961; Carlson and Bayley 1972a, b). glycol(molecular weight 4000,15 mCi/g) from Amer- Polyethylene glycol (MW 4000) is a widely ac- sham (Arlington Heights, Illinois) without further cepted aqueous-phasemarker (Wingate et al. purification.Fluors were ACS II (Amersham,Arling- 1972)and glyceroltriether, a neutrallipid-phase ton Heights, Illinois) and BiosafeII (ResearchProd- marker, is used extensively in studies with ucts International,Mount Prospect,Illinois). Dupli- mammals(Morgan and Hofmann 1970;Carlson cate sampleswere counted on a BeckmanLS 3801 and Bayley 1972a,b; Meyer et al. 1986),but has scintillationcounter. A correction("quench") curve not been used with birds. The triethers will wasderived to determinecounting efficiency for dif- mark only the neutral lipid phase;polar lipids, ferentextracts and tissuetypes using Compton edge suchas phospholipids and fatty acids,partition ("H number") calibration (BeckmannInstruments). into the aqueousor miceliar phase.These com- Countingefficiency for •4Cin thesamples varied from 88.0-75.4%and that for 3H from 22.0-6.0%.Counting pounds are nonabsorbable, nontoxic, nonde- times (2-10 min) were chosen to ensure at least 95% gradableby digestiveor bacterialenzymes, and counting accuracy.The coefficient of variation for do not influence the normal absorptionof di- replicatesamples averaged 3.0% (SD = 1.3) for tritium etary aqueousnutrients or fat. and 1.9% (SD = 0.9) for carbon-14. All radioactivities In mammals, passagerate of lipids through are expressedin disintegrationsper min (DPM). the pyloric valve and into the small intestine is Tracer synthesis.--BachemBioscience Inc. (Phila- nearly half that for aqueouscomponents (Jian delphia, Pennsylvania)synthesized the glycerol et al. 1982,Meyer et al. 1986).If a meal is ho- triether[1-(9 cis-octadecenyl)2,3 didodecylglycerol mogenized prior to ingestion, however, both triether]as described by Morganand Hofmann (1970). lipids and aqueous components empty the The tritiatedglycerol triether (3H-GTE) was prepared by reductionwith platinum as a catalyst(New En- stomachtogether (Cortot et al. 1979). gland Nuclear, Boston, Massachusetts).Purified 3H- Using lipid-phase and aqueous-phasemark- GTE(> 98%radiopurity) was obtained by chromatog- ers, we examined gastrointestinal transit in raphy on a silicic acid column eluted with hexane/ chicks of the Antarctic Giant-Petrel (Macro- diethyl ether 85:15 (v/v). Solvent was removed with nectesgiganteus) and Gentoo Penguin (Pygoscelis nitrogen evaporationand the purified 3H-GTE dis- papua).These speciesrepresent the two major solvedin absoluteethanol to a specificactivity of 1 orders of seabirds in the Southern Ocean. The mCi/ml. young of both speciesare fed at the nest by Studyarea and subjects.--Feeding (including excreta their parents until full grown. Giant-petrels collection)trials were conductedduring Januaryand February,1986, at Ardley Island (62ø13'S,58ø55'W), a usually locate their nestsnear penguin breed- ca. 18-ha island off King George Island, South Shet- ing coloniesand feed their young a diet of (in land Islands,where ca. 9,000 pairs of GentooPen- decreasingorder of importance)penguins, krill guinsand 15pairs of AntarcticGiant-Petrels nest (Roby (Euphausiasuperba), seals, squid, and small sea- et al. 1986b).Six nestlingsof eachspecies were re- birds (Hunter 1983, 1985). The chicks of both moved from nests and held in enclosures for 12-20 giant-petrelsand Gentoo Penguinsare usually h beforeingesting the labeledmeal. Subjects were ca. fed 1-2 meals daily. The diet of Gentoo Pen- 4 weeks old, judging from wing-length and body- guins consistsprimarily of krill and, to a lesser mass measurements (Hunter 1984, Volkman et al. extent,fish (Croxalland Prince1980). Nestling 1980).All weredeveloped sufficiently to thermoregu- giant-petrelsstore stomach oils at an early age late at ambienttemperatures (ca. 0-5øC)indepen- dently of their parents.Body mass of subjectsused in and are adept at regurgitatingoil on potential feedingtrials ranged from 0.98-2.2kg and averaged predators.Penguins do not storestomach oils. 1.5 kg. Averagemass of subjectsdid not differ sig- We measured relative transit times of the two nificantly between the two species(t = 0.344, P > phasesin penguins to ascertainthe extent of 0.05, Table 1). differential passagerates in an avian species Priorto feedingthe radiolabeled meal, we pumped which lacksstomach oils. By comparingpassage the stomachsof giant-petrelchicks to remove any April 1989] StomachOils and GI Transit 305 TABLE1. Morphological measurementsof the gas- Scornbetjaponicus peruvianus) was used to prepare the trointestinal tracts of Gentoo Penguin (n = 6) and labeled meal. Composition of the canned fish was Antarctic Giant-Petrel chicks
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