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Structure and Function of the Digestive Tract of the Hoatzin (Opisthocomus Hoazin): a Folivorous Bird with Foregut Fermentation

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Structure and Function of the Digestive Tract of the Hoatzin (Opisthocomus Hoazin): a Folivorous Bird with Foregut Fermentation The Auk 112(1):20-28, 1995 STRUCTURE AND FUNCTION OF THE DIGESTIVE TRACT OF THE HOATZIN (OPISTHOCOMUS HOAZIN): A FOLIVOROUS BIRD WITH FOREGUT FERMENTATION ALEJANDRO GRAJAL• Departmentof Zoology,University of Florida,Gainesville, Florida 32611, USA A•TI•CT.--The Hoatzin (Opisthocomushoazin) is a uniqueobligate folivorous bird with a well-developedforegut fermentation system. Its relativegut capacityis equivalentto 9% of the adult body mass(ca. 680 g). The large crop and lower esophagusrepresent 77% of the total gut capacity.The crop is folded into two interconnectedchambers, and the lower esophagusis a multichamberedorgan. Both are unusuallymuscular with constrictionsbe- tween chambers.The interior lining of the crop and esophagushas longitudinal ridges coveredby cornifiedepithelium. The cropand esophagusare the main fermentationorgans, with pH and volatile-fatty-acidslevels equivalent to thosefound in mammalswith foregut fermentation.The proventriculumand gizzardare muchreduced in capacity.A combination of abrasionand microbialaction effectively reduces particle size along the gut. A trial with markersmade out of thin (0.6-ram)plastic film demonstratedthat large particles(10 mm2) are retainedlonger than medium (4-ram2) or small (l-ram2) particlesat the anterior fermen- tation sites.The extremegut adaptationsin the Hoatzin are more similarto thoseof small mammalswith foregutfermentation than to any known bird. This suggeststhat a similarset of evolutionaryconstraints may affectthe evolution of foregut fermentationin vertebrates. Received8 June1992, accepted 25 November1992. TIlE HO^TZlN(Opisthocomus hoazin) is a Neo- those of mammalian foregut fermenters.The tropical folivorous bird that inhabits oxbow crop and esophagusare situated in front of a lakes, flooded forests,and lowland swampsof greatly reduced sternal carina, and leave little the Guianas, Orinoco, and Amazon basins. Up area for flight musclesto attach (Fig. 1). As a to 87% of its diet consistsof leaves(Grajal et al. result, hoatzinsare not powerful fliers,prefer- 1989).Obligate folivory is unusualin birds be- ring to hop from branchto branch(Strah11988). causeleaves are bulky, have low nutritional val- The peculiaritiesof Hoatzin anatomywere the ue, and may contain noxiouschemicals. These subjectof many early descriptivestudies at- propertiesare in direct conflictwith the flying tempting to establishthe evolutionary affinities ability and energy demands typical of most between Hoatzins and other birds (L'Hermen- birds. Much of the organic matter of plant tis- ier 1837, Perrin 1877, Goeldi 1886, Parker 1891, suesis structuralcarbohydrate in cell walls, of Pycraft 1895, Huxley 1868, Verheyden 1956). which celluloseis one of the main components The presenceof functionalwing clawsin Hoat- and alsois the mostcommon organic compound zin chicks, the reduced sternal carina, and the in nature. Becauseno vertebrate producesthe poor flying abilities of the Hoatzin were re- enzymes necessaryto digest cellulose, many garded as the primitive characteristicsof a herbivoreshave enlarged chambers in their gut, "missinglink" betweenthe firstfossil birds such where anaerobicmicrobes secrete enzymes that asArchaeopteryx and modern birds (Parker 1891). digest cellulose. Present systematicstudies place the Hoatzin The Hoatzin is the only bird known to pos- within the Cuculiformes(Sibley and Ahlquist sessa fully-functionalforegut fermentation sys- 1973, 1990, de Queiroz and Good 1988, Sibley tem (Grajal et al. 1989). The voluminous crop et al. 1988). Some early authors attempted to and posterior esophagushave become func- relatethe largegut capacityto a folivorousdiet tional fermentation chambers, analogous to in the Hoatzin (L'Hermenier 1837, Gadow 1891, B/•ker1929). In fact, Goeldi (1886) and Young • Presentaddress: Wildlife ConservationSociety, (1888) describedthe smell of the gut contents 185th Street and Southern Blvd., Bronx, New York as resemblingthat of fresh cow manure.How- 10460, USA. ever, none of theseauthors suggested that fore- 20 January1995] HoatzinDigestive Tract 21 Fig. 1. Schematicrepresentation of anterior gut of adult Hoatzin seen from left, showing (A) crop, (B) posterioresophagus, (C) proventriculus,and (D) gizzard. Anterior sternumis much reducedto make room for large fermentationchambers, resulting in drasticreduction in areaavailable for flight-muscleattachment to (E) sternal carina;(F) "resting" pad at end of sternum used while perching with full crop. gut fermentationwas the primary function of (66ø20'W, 6ø8'N), and Pifiero (68ø4'W, 8ø82'N). The the large gut capacityof Hoatzins. total body massof each bird was recordedimmedi- I describethe grossanatomy and function of ately usinga portablespring scale (+ 1 g), after which the gastrointestinaltract of the Hoatzin, and the gastrointestinaltract was removedand weighed. then comparethe Hoatzin'sgastrointestinal tract The gut was divided with string knotsand then cut into anterior esophagus,crop, posterioresophagus, to other herbivorous birds and foregut-fer- proventriculus, gizzard, small intestine, caeca, and menting mammals.I measuredthe gut capacity large intestine.The wet massof the contentsof each of Hoatzins and explored relevant functions, sectionwas determinedby subtractionof the massof such as particle dynamics,and nutritional and each sectionwith and without its contents.The pH physicalcharacteristics of gut contents.If fore- of the contentsfrom each segmentwas measuredin gut fermentationis nutritionally importantfor situwith a portable pH-meter, usually within 20 rain Hoatzins, one would expectgut capacityto be of the bird'sdeath. Samples from eachsegment were similar or exceed that of mammalian foregut fixed with concentrated sulfuric acid and frozen in fermenters. Also, the Hoatzin's digestive tract dry ice for later measurementof the concentrationof volatilefatty acids.Other freshsamples were weighed might be expectedto reduce particle size and and dried at 100øC until their mass remained constant show selective particle retention to optimize for determinationof percentagedry matter.Samples the nutritional use of plant cell wall. Under- of the contentsfrom somesegments were fixed in standingthe anatomyand function of the Hoat- buffered formalin for particle-sizeanalysis, and the zin digestivetract can provide insightsinto the remaining contentswere frozen and later dried at evolutionary limits of foregut fermentation in 60øC until their mass remained constant for nutri- vertebratesand birds in particular. tional analysis.Tissue samples from the gut were fixed in 10%buffered formalin for histologicalanalysis. MATERIALS AND METHODS Gut contents were analyzed for dry matter, cell wall, nitrogen, ash, volatile fatty acids,and particle Hoatzins were shot at the following sitesin the size. Cell wall and ash content were determined fol- Llanosof Venezuela:Masaguaral (67ø35'W, 8ø34'N), lowing the neutral-detergentfiber (NDF) method of Guf•rico River (67ø28'W, 8ø33'N), Suapure River Goering and Van Soest(1970). Nitrogen content was 22 ALEJANDROGRAJAL [Auk,Vol. 112 determinedby the Kjeldahl method (Van Soest1982). were found amongcapture sites or timesof cap- The concentrationof volatile fatty acids was deter- ture (Mann-Whitney U-test). mined using gaschromatography (Wilkie et al. 1986). Digestive-tractmorphology.--The mouth re- Mean particle size in somegut sectionswas measured gion and other regions of the gut have been using a computerizedparticle-analysis video system partially describedby early authors(Mitchell and a video cameramounted on a microscope.This systemallowed a statisticalanalysis of particle size 1896, 1901,Banzhaf 1929,B6ker 1929).The gen- frequency.Small sample sizes at the intestineor caeca eral structure of the bill looks more galliform did not allow an accuratemeasurement of particle than cuckoolike,which may explain the clas- size, so the contentsof all hindgut siteswere pooled. siftcation of the Hoatzin as a member of the Particle retention at variousportions of the gut was Galliformes for many years(Huxley 1868, Ban- measuredin a singlecaptive adult Hoatzin. The bird zhaf 1929).The bill has sharp edgesthat prob- was acclimated to a maintenance diet for more than ably help in cutting leaves. The lanceolate 60 days(Grajal et al. 1989).The maintenancediet con- tongue has sharp posteriorlydirected papillae sistedof romainelettuce, soybean protein powder, at its base that resemble backward-pointing ground alfalfa pellets and fresh young shootsof En- spines,and probably assistin swallowing large terolobiumcyclocarpum, Pithecellobium saman, Guazuma ulmifoliaand Phthirusacf. orinocensis.The Hoatzinwas piecesof leaves.A pair of largesublingual man- force-feda gel capsulecontaining plastic markers made dibular salivary glands (glandulamandlgularis out of brightly-colored commercial flagging tape externasensu McLelland 1979) are evident. Al- (0.6mmthickness). The inert plasticmarkers were cut though I did not measurethe compositionof in three sizes (10, 4, and 1 mm 2) and administered in the saliva from these glands,it was quite thick a singlepulse dose (Warner 1981).The specificgravity and sticky.Other salivaryglands in the corner of this material is almost one (1.01), so it resembles of the mouth (glandulaanguli oris) and in the the specificgravity of wet food particlesin the fer- cheeks are relatively smaller (F. Michelangeli mentationchambers (Warner 1981). The captiveHoat- pers.comm.). Although the salivaryglands are zin was housed in an individual custom-made met- not large, the
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