Pellet Formation in a Great Horned Owl: a Roentgenographic Study

PELLET FORMATION IN A GREAT HORNED OWL: A ROENTGENOGRAPHIC STUDY

ROBERTJ. GRIMM AND WALTER M. WHITEHOUSE

IN the literatureon owls,there has been much interest in the formation in the uppergastro-intestinal tract of pelletswhich contain indigestible materialand whichare subsequentlyregurgitated. This featureof gastro- intestinalfunction has interestedbird physiologists,and analysisof the pelletshas been used to monitorfeeding habits (Errington et al., 1940). Althoughpellet formationis not limited to the order Strigiformes,most informationconcerning this aspectof avianphysiology comes from work on owls. Studieshave centered on suchproblems as factorsaffecting the meal-pelletinterval (Chitty, 1938),pellet analysis, physico-chemical prop- ertiesof digestivejuices, and anatomicaldistinctions between pellet forming and non-pelletforming birds (Guerin, 1928). It is possiblefrom indirect evidenceto make a reasonableestimate of the sequenceof eventsinvolved in the 10 hourprocess of the formation of a pellet from the indigestibleportion of an animal. A review of the availableliterature, however, fails to revealan accurateaccount of events in vivoas seenby radiographicmethods. The opportunityfor sucha study was afforded when a full-grown Great Horned Owl (Bubo virginianus) was receivedfor study.

METttODS The owl, which appearedto be in splendidcondition, was securely tetheredto a woodenplatform by meansof leather jesses.Following a period of two days with this restriction,the bird was blindfolded,carried to an animal radiologylaboratory in The Universityof Michigan Medical Center, and left to becomeaccustomed to its surroundingsin semi-dark- ness. During this periodof acclimatization,the X-ray tube, casette,and casette holder mounted on a ring stand were moved about the bird to simulateexperimental procedure. This experiencewas repeatedtwice, each time with the owl spendingfour to six hoursin the laboratory. On the secondoccasion, a rodentwas offered,and waspromptly killed by the owl, but not eaten. After four days of food deprivation,the owl was returnedto the laboratoryfor experimentation. X-rays were made in a lateral projectionwith the film casettepressed againstthe wing surface(this did not disturbthe owl) on the side op- positeto the X-ray tube. The X-ray tube was placedapproximately 60 cm (two feet) from the owl. Exposureswere made at 50 KV with 100 milliamperesfor 0.1 second.

301 The Auk, 80: 301-306. July, 1963 302 GR•z•z ANDWHITEHOUSE, Pellet Formationin Owls LI' Vol.Auk 80

Also a recently shot Great Horned Owl was received for autopsy. Figure 1A is an X-ray of this bird in the lateral positionwith a tube in the esophagus.The tip of the tube lies in the regionof the proventriculus. An introducedradio-contrast material (Hypaque) outlined the size and contour of the lumen of the ventriculus (as shown by arrows). This pro- cedureestablished the positionof the gastro-intestinaltract in relation to other anatomicallandmarks. An autopsywas performed;the findingswill be consideredbriefly later. O]•SE•V^T•ONS Figure lB is an X-ray of the bird prior to feeding. Residualfood (the area of density in the lower part of the ventriculus) is not unusual in owls forced to go for long periodswithout food (Chitty, 1938). The owl was fed sevenlaboratory mice, which were consumedwithin seven minutes. Figure 1C, taken one hour after feeding, showsan expanded ventriculus. Small bones can be seen (as a dense reticular pattern) scatteredwithin the ventriculus. Figures 1D and 1E, taken two and three hours after feeding,show a reductionin the volume of the ventriculus, and give somesuggestion of condensationof the small bones. In Figure iF, taken five hours post-prandial,arrows delineate the outline of the forming pellet. Figure 1G, taken eight hours after feeding, demonstrates continuedcondensation of materials,the pellet sizeand configurationbeing essentiallyfixed by 10 hours (Figure 1H). Films taken up to 16 hours (when the pellet was expelled)fail to showa significantchange in its size. The pellet remainedin the superiorarea of the ventriculus (approximately its positionin Figure 1H) until regurgitation. The recoveredpellet meas- ured 4.5 cm in length and 2.5 cm in diameter; Figure 1I is an X-ray of the pellet. Regurgitationof the pellet was not observed. The secondexperiment, performed after a period of food deprivation, was carried out by injecting two mice intraperitoneally with 2.5 ml of radio-contrastmaterial. The mice were promptly taken by the owl. Spillageof this material into the small intestineseemed a simple way of determininghow quickly disruptionand digestionoccur. Figure 2B shows radio-contrastmaterial in the ventriculus of the owl, five minutes after the mice were swallowed. It is apparent from the irregular pattern of distribution,that contrastmaterial has remainedin the abdominalcavity of the mice. By 10 minutes (Figure 2C) however,not only has contrast material diffused evenly throughout the ventriculus, but it also appears in the proximal portion of the small intestine (arrows).

GE•]•AZ. COnSiDErATiONS The observationthat the owl carried the pellet approximatelysix hours after it appearedto be completed,and the presenceof indigestiblematerial July1963 ] GRIMMA•'• WmTEHOX•SE, PelletFormation in Owls 303

A B

D E F

10 t

Figure 1. X-rays of Great Horned Owls. A. Autopsy specimen,intubated, showing contour of ventrienlus filled with radio-contrast material. B-I show in vivo studies (all times refer to hours after feeding). B. Hungry owl before feeding. X-ray suggests the presence of residual food material in the ventriculus. C. Appearance of the ventriculus one hour after swallowing seven mice. D. Two hours. E. Three hours. F. Five hours. Arrows delineate forming pellet. G. Eight hours. Further condensa- tion of pellet material is seen. H. Ten hours. Pellet is essentially complete (no further reduction in size was seen in later films). I. Pellet• recoveredsixteen hours after feeding. 304 Gsm•AND WHITEHOUSE, PelletFormation inOwls [ Vol.Auk so

B C

Figure 2. A. The bird used in the study. B. X-ray taken $ minutes after ingestion of two mice injected with radio-contrast material (material still in the abdominal cavities of the mice). C. After 10 minutes (contrast material fills the proximal portion of the owl's small intestine). within the ventriculusbetween feedings, tend to supportChitty's observa- tions (1938) that the meal-pellet intervals increaseduring periods of food shortage. Autopsy,confined mainly to the gastro-intestinaltract, confirmedReed and Reed'sobservations (1928) that in the Great Horned Owl the pyloric oufiet is very small (1.5 mm) and arisesfrom the superiorsurface of the ventriculus. As Reed and Reed pointed out, this anatomicalarrangement appears to be an effective barrier against the passageof bulky food particles. The grossand microscopicanatomy of the proventriculusand ventriculus proved interesting. The ventricular wall, composedof an inner circular and outer longitudinal musclelayer, was 2 to 4 mm in thickness,and there was no evidenceof hypertrophyin the areas of the sphinctersbe- tween the proventriculusand ventriculus,or the ventriculusand duedenum. The ventriculus was securely bound to the abdominal wall by dense fibrous connectivetissue. The spacious,thin-walled esophagusand the superiorportion of the proventriculuswere lightly anchoredto the thoracic cageby thin sheetsof connectivetissue. Proventricularglandular pits were prominent, and the cellular elementsof these exocrineunits were eosino- philic, suggestinga seroussecretory character. Basophilic,mucus-produc- ing cells lined the fine viiius-like structuresof the ventriculus. It is perhapsworthy of note that there is no apparentanatomical modi- fication of the gastro-intestinaltract significantlyrelated to pellet formation (seeGuerin, 1928). Somewhatsimilar pellets are formedby a variety of predatory birds that consumeparts or all of vertebrateanimals, for July1963 ] GRnvr•A•O WmTr•OVSE, Pellet Formation in Owls 305 exampleby hawks,owls, gulls, cormorants,crows and ravens,and probably others. Gallinaceousbirds, which do not form pellets, have stomachs grosslysimilar to the short, thick-walled stomachof crows. The presence, on the other hand, of a relatively thin-walledventriculus in the Great Horned Owl (as in most hawks and owls; Farner, 1960: 428), lined with viiius-like structures,supports the view that this organ functionsin these, as in other birds, primarily in mixing. One curiousaspect of digestionin Great Horned Owls is that during pellet formation in adult birds the stomachpH approximatesneutrality or is slightly alkaline (Guerin, 1928; Wilson and Niosi, 1961). In young birds (three monthsof age), F. H. Wilson (pers.comm., 1962) notedthat stomachpH during feeding, sampledby means of a gastric tube, was acidic (pH 4). In older birds, the pH becameneutral, a condition,as he noted, that excludespepsin as the active proteolyticenzyme. Wilson and Niosi (1961) concludedthat the essentiallyneutral character of the ventriculusduring active digestionis due to reflux into the ventriculusof alkaline secretionsof the small intestineand pancreas. In summarizing,the processof pellet formation in owls seemsto occur as follows:an owl retainsits animal meal within the ventriculusby closure of the sphincterbetween the ventriculusand proventriculus;the pyloric opening,which is small and arisessuperiorly, probably remainsopen during most of the digestiveprocess. In this actively contractingand re- laxing pouch collect enzymaticsecretions arising from the glands of the proventriculus,small intestine,and pancreas. Although the generalenzy- matic action in digestionis little known, there is evidencethat in young owls the gastric pH is distinctly acidic, becomingmore neutral in older birds. As digestionproceeds, the nutrient effluent is pumped into the small intestine by ventricular contractions. Indigestible solids, e.g., bone, fur, teeth, nails, and chitinousmaterials, collect in the inferior portion of the ventriculus,and are gradually forcedinto a tight pellet form. The length of time between feedingand regurgitationof a pellet is subject to both internal and externalfactors (Chitty, 1938). In the hungry Great Horned Owl in our laboratory, pellet formation was essentiallycomplete eight hours after feeding. Before regurgitation,an event Guerin (1928) held to be voluntary, the pellet lies in the superiorportion of the ventriculusimmediately below the sphincter. At expulsion,the sphincter is relaxed, and ventricular con- traction, with accessorycontractions of the abdominal wall and proventriculus,force the pellet upward in a seriesof stepsuntil it is finally discharged;the processin the Great Horned Owl takes approximately four minutes. 306 GRi•r•r ^m>WHrrEHo•rsE, Pellet Formation in Owls /I' Vol.Auk 80

ACKNOWLEDGMENTS The authors wish to thank Mr. Melvin Block, curator of birds at the Toledo Zoo, for the use of a Great Horned Owl, and Charles Collins for making the necessary arrangements.We are indebtedto Jack Wirth for his help with the experiments.Our specialthanks to Dr. Edward Willy, who photographedand printedthe originalX-ray films, and to Dr. Harrison B. Tordoff for critical review of the manuscript.

LITERATURE CITED CmTT¾,D. 1938. Pellet formationin Short-earedOwls, Aslo fiammeus.Proc. Zool. Soc. London, 108 (Series A): 267-287. ERRINGTON,P. L., F. HAMERSTROM,and F. N. HAMERSTROM,JR. 1940. The Great Horned Owl and its prey in north-centralUnited States. Agric. Expt. Sta., Iowa State CollegeAgric. and Mech. Arts, Bull. no. 277. Pp. 759-850. FARNER,D.S. 1960. Digestionand the digestivesystem. In The biologyand com- parativephysiology of birds. Vol. I. A. J. Marshall(ed.). New York, Academic Press. GVERI•, G. 1928. La vie des chauttes.Regime et croissancede l'effreys commune. Paris, P. Lechevalier. R•o, C. I., and B. P. REly. 1928. Mechanismof pellet formation in the Great Horned Owl Bubo virglnianus. Science,68: 359-360. W•so•, F. H., and P. N. NIoSI. 1961. Someobservations on gastricdigestion in the horned owl. Amer. Zool., 1-- 399 (abstract). Departmentof Physiologyand Biophysics,University of Washington, Seattle,Washington, and Department of Radiology,University of Michi- gan Medical Center,Ann Arbor, Michigan.