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SHARPE,R. B. 1909.A hand-listof the generaand spe- Rhodopechys,Carpodacus, Pinicola, Loxia, Uragus, ciesof birds, vol. 5. Taylorand Francis,London. Urocynchramus,and Propyrrhula.American Mu- SIBLEY,C. G., AND B. L. MONROE,Jr. 1990. Distribu- seum Novitates 1786:1-37. tion and taxonomyof birds of the world. Yale VAURIE, C. 1959. The birds of the Palearctic fauna. University Press,New Haven, Connecticut. Passeriformes.H. E & G. Witherby,London. SUSHKIN,P. P. 1927.On the anatomyand classifica- WOLTERS,H. E. 1979. Die Vogelarten der Erde, vol. 4. tion of the weaver-birds. Bulletin of the Ameri- Paul Parey,Hamburg and Berlin, Germany. can Museum of Natural History 57:1-32. Zu$I, R. L. 1978.The interorbitalsepturn in cardue- SWOFFORD,D. L. 1998.PAUP*. Phylogenetic analysis us- line finches. Bulletin of the British Ornitholo- ing parsimony(*and other methods), version 4.0. gists' Club 98:5-10. Sinauer Associates,Sunderland, Massachusetts. VAURIE, C. 1956. Systematic notes on Palearctic Received26 October1998, accepted 23 November1999. birds,no. 20. Fringillidae:The generaLeucosticte, AssociateEditor: A. ]. Baker

The Auk 117(3):791-794, 2000

Anatomical and Nutritional Adaptations of the Speckled Mousebird (Colius striatus)

COLLEENt. DOWNS,• J. OLAF WIRMINGHAUS,2 AND MICHAEL J. LAWES Schoolof Botanyand Zoology, University of Natal,Private Bag X01, Scottsville3209, SouthAfrica

Folivoryis a rare phenomenonin birds that has creasingbody mass, small folivores have proportion- evolvedindependently in severallineages. It hasbeen ally higher metabolicrequirements relative to their reportedin ratites(Withers 1983, Herd and Dawson gut capacitythan do large folivores(Demment and 1984), anatids(Buchsbaum et al. 1986, Dawson et al. VanSoest1985). Consequently,small avian folivores 1989),ptarmigan (Gasaway et al. 1975),the Kakapo have greaterproblems of energy acquisitionthan (Strigopshabroptilus; Oliver 1955, Powleslandet al. theirlarger avian counterparts and thus are expected 1992),and somespecies of Saltator(Bosque et al. 1999). to be rare. The Hoatzin (Opisthocomushoazin) is uniqueamong Mousebirds,order Coliiformes,comprise six spe- birdsin beingthe only documentedforegut fermenter ciesthat are endemicto sub-SaharanAfrica (Maclean andthe only obligate avian folivore (Grajal et al. 1989). 1993).Despite the paucityof species,mousebirds are Althoughfolivory is commonin mammals(Chivers remarkablysuccessful and haveradiated into many and Langer1994), the evolutionof folivoryin birdsis habitatsin Africa, occurringfrom harsh desert to constrainedby bodymass and the highmass-specific moist savanna. The folivorous habits of these birds energyrequirements of endothermyand flight, despite were first observedin the SpeckledMousebird (Col- the apparentunlimited supply of freshfoliage in na- ius striatus;Rowan 1967), althoughpeculiarities of ture.Klasing (1998) defines an avianfolivore as one that their thermoregulatoryability were noticedprior to concentrateson leaves;however, the categories from an this (McAtee 1947). Body temperaturesof mouse- obligatefolivore to a facultativefolivore are poorlyde- birds are correlatedwith ambienttemperature fluc- fined. tuations,which is a putativereason for their noctur- Folivoryis associatedwith reducedfood quality nal huddling behavior(Rowan 1967). Average body (Chiversand Langer 1994). Digestioncosts for fer- mass of each speciesis about 50 g, making mouse- mentingfolivores are high owing to gut specializa- birds amongthe smallestof folivorousbirds. Con- tions (i.e. a fermentation chamber) and associated sequently,we investigatedtheir gastrointestinal tract bacterial micro flora for the breakdown of cellulose and digestivephysiology and suggesthow adapta- and release of volatile fatty acids (VFA; VanSoest tionsin thesetraits permit the combinationof small 1983).Energy from a folivorousdiet is releasedslow- size and folivory in birds. To determinethe extentof ly, requiringa behavioraland physiologicallifestyle morphologicaland physiologicaladaptations, we that minimizesenergy expenditure. Because energy madeoutgroup comparisons with the Purple-crested requirementsper unit body massincrease with de- Turaco(Tauraco porphyreolophus ), which is a largefor- est frugivore,and with the Hoatzin. Methods.--Wecollected 13 Speckled Mousebirds E-mail: [email protected] from Creighton(30ø02'S, 29ø46'E) and Pietermaritz- Deceased. burg (29ø36'S,30ø24'E), South Africa, in May 1994 792 ShortCommunications [Auk, Vol. 117

TABLE1. Body and gut dimensionsof Coliusstriatus, C. colius,Urocolius indicus, and Tauracoporphyreolophus. Valuesare œ+__ SE, with n in parentheses.

Urocolius Tauracoporphyreolo- Parameter Coliusstriatus C. colius indicus phus Body mass(g) 50.7 ---2.27 (13) 38.8 _+0.4 (15) 50 (1) 318.1 _+41.49 (4) Esophaguslength (mm) 44.1 ___1.30 (13) 44.6 + 0.7 (27) 30 (1) 64.2 _+3.59 (4) Proventriculuslength (mm) 21.3 ---0.99 (12) 17.2 _+0.7 (27) 26 (1) 26.2 + 2.21 (4) Ventriculuslength (mm) 21.9 ---0.86 (13) 12.2 + 0.5 (27) 14 (1) 31.6 + 2.60 (4) Ventriculusbreadth (mm) 15.7 ---0.67 (12) 14.1 _+0.5 (27) 19 (1) 20.8 _+3.78 (4) Small intestine-cloacal(mm) 225.8 --- 7.54 (11) 169.0 _+4.7 (27) 260 (1) 401.0 _+38.15 (4) Total GIT length (mm) 312.4 + 8.59 (11) 244.0 _+4.7 (27) 330 (1) 522.9 _+38.36 (4) GIT:HB indexa 46.86 (11) 54.39 (1) 66.59 (4) GIT:mass indexb 61.42 (11) 70.65 (1) 59.09 (4) Lengthof smallintestine to cloaca/cuberoot of head-bodylength (mm). Lengthof smallintestine to cloaca/cuberoot of body mass(g). and dissectedthe fresh specimens.Body measure- were pigmentedblack. The ventriculusin situwas a ments and gastrointestinaltract (GIT) dimensions prominentorgan, lying to the lower left sideof the were made with vernier calipersand a steel ruler abdomenwith the anterior dorsal portion slightly (+0.5 mm). Under a dissectingmicroscope, we de- behindthe posteriorend of a liver lobeand the pos- terminedthe proportionof leaf material,fruit, and terior dorsalportion lying directlyagainst the dorsal seedin the ventriculusof eachspecimen. Sections of bodywall. Thebody wall wasnonmuscular here and the GIT of C. striatuswere fixed in 5% bufferedglu- the skin pigmentedblack, with featherson the ex- taraldehydeat 4øCas initial preparationfor scanning terior surface.The GIT length:bodylength index of electronmicroscopy. The remainingsections of the SpeckledMousebirds was lower than that of the Pur- GIT were fixed in Bouin's solution from which his- ple-crestedTuraco, whereas the GIT length:body tologicalsections were prepared;these were stained massindex was higher (Table1). with eosinhaematoxylin to showthe histologicalar- Both the Speckled Mousebird and the Purple- rangementof the gastricepithelia. Immediately after crestedTuraco showed a typical gastricplan with dissection,the gut contentsin the ventriculiof eight mucosa,submucosa, and muscularis.In theSpeckled C. striatuswere identified to food categoryas noted Mousebird,the musculaturewas less extensively de- aboveand then placedin clearscrew-top vials, fro- velopedand showedno elastictissue compared with zen, and analyzedfor VFAs using gas chromatog- the Purple-crestedTuraco. The main differencebe- raphyby the Animal Nutrition and Animal Produc- tweenthe two specieswas the extensivesurface area tion Institute, Irene, South Africa. Gut contents of the in the ventriculusof the SpeckledMousebird owing remainingindividuals were spreadon a glassslide to the extensive convolutions, whereas few convo- and viewed using a dissectingmicroscope and per- lutionswere presentin the Purple-crestedTuraco. centagesof food categoriespresent estimated. Scanningelectron microscopy revealed the ven- We dissectedone Red-faced Mousebird (Urocolius in- triculus to be coveredby speciosemicrobial flora. dicus)and four Purple-crestedTuracos obtained from The microbial flora included sphericaland ovoid the Durban Natural Science Museum to obtain GIT di- bacteriaarranged in long chainsor pairs (possibly mensions. Furthermore, 27 White-backed Mousebirds Planococcusor Rumenococcus;Sneath et al. 1986) and (Coliuscolius) collected in Prieska(29ø39'S, 22ø46'E) and othersthat were rod-shaped.Further research is re- PrinceAlbert (33ø14'S, 22ø02'E) by A. McKechniewere quired to isolate,culture, and classifythe microor- dissectedfor GIT dimensions.Gross morphology of the ganismsin the foregutof mousebirds. GIT of all specimenswas examinedusing a dissecting We recordedthe presenceand concentrationof microscope. VFAs in the proventriculusand ventriculuscontents Results.--Thestructure of the GIT of the Speckled of SpeckledMousebirds: i.e. aceticacid, propionic Mousebirdconsisted of an esophagusleading into a acid,iso-butyric acid, n-butyric acid, iso-valeric acid, well-developedproventriculus that was composed of and n-valericacid (Table2). Small peaksindicating a muscularwall with a grosssmooth inner surface other VFAs were also seen. exceptfor a gracilereticulate pattern; no cropwas ev- The gut contentsof SpeckledMousebirds varied ident. The proventriculusled to the ventriculus, widely in the amountof leaf materialpresent (0 to which was simple,unilobular and thin-walled.The 100%).A high proportionof fruit was eatenwhen inner wall of the ventriculuswas a mat of adpressed leaf intakewas low. The meanproportions (n = 10) papillae.The surfacearea of the ventriculusof the of dietary categoriesin the ventriculuswere 43.2 +__ Speckled Mousebird is large becauseof extensive SE of 10.5% leaves, 54.3 + 10.4% fruit, and 2.5 + 2.5% convolutions.It also has some areas (>50%) that seeds.We observedSpeckled Mousebirds feeding on July2000] ShortCommunications 793

TABLE2. Volatilefatty acid concentrations (mmol/g 104)in the ventriculusof eightspecimens of Coliusstriatus.

Acetic Iso-butyric n-Butyric Iso-valeric n-Valeric acid Propionicacid acid acid acid acid 9.50 156.96 -- 36.90 -- -- 180.90 49.81 10.61 81.44 -- -- 115.46 23.29 67.27 45.71 18.70 -- -- 17.78 27.35 27.35 -- 26.20 7.62 21.32 6.69 30.94 ------8.40 8.18 52.30 ------4.46 9.10 44.30 ------4.42 7.07 52.13 -- --

the leavesof various introducedplant species,in- otherfood sources are scarce.Frugivores with fixed cluding cultivatedvegetables. In addition, we saw home rangesrespond to periods of low fruit avail- SpeckledMousebirds feeding on the leavesof native abilityby increasingthe proportion of non-fruitsand plant species, including Erythrina lysistemon,al- aseasonalfruit typesin the diet (Leightonand Leigh- thoughfruit was available. ton 1983).A disadvantageof microbialfermentation Discussion.--Unlikethe Hoatzin (Grajal et al. is the increasein transit time of food in the gut 1989),GIT grossmorphology of the SpeckledMou- (Chivers and Langer 1994). Mousebirdsappear to sebirdcomprised an esophagusleading into a well- haveovercome this by switchingdiets if higher-qual- developedproventriculus with no clearlydeveloped ity food is available.Gastrointestinal tract data for crop. The much larger Hoatzin has a gut capacity Red-faced Mousebirds and White-backed Mouse- equivalent to 9% of total adult body mass (680 g) birds have been included for comparison(Table 1) with a large double-chamberedcrop and a multi- becausethese species also are reportedto feed irreg- chamberedlower esophagus(together constituting ularly on leaves.Further researchis neededto test 77% of total gut capacity;Grajal 1995b)that allows for the presenceof bacteriaand VFAs in the GITs of for high intake of food. thesespecies. All foliage-fermentingvertebrates rely to variable Hoatzinsare very inactive comparedwith other degreeson microbessuch as bacteria and protozoans bird species(Grajal and Strahl 1991). All Mousebirds to produce nutrients from cellulose(VanSoest 1983). exhibit heterothermia(Bartholomew and Trost 1970, Many avian herbivorescan switchbetween a "fiber- Prinzinger 1988),and clusteringbehavior is an effec- skimming"strategy and a higher-efficiencyfermen- tive energy saver(Prinzinger 1988,Brown and Foster tationstrategy (Klasing 1998). The Hoatzinhas a di- 1992)at night. Clusteringduring the daytimemay be verse microbial flora, including anaerobicbacteria a restingbehavior for theseleaf-eating birds (Yama- and ciliateprotozoans that appearto play an impor- gishi and Kabango1986). These factors can balance tant role in nutrition (Dominguez-Belloet al. 1993). the tradeoff between a diet of low nutritional value The Hoatzin is the only known bird with a high de- and the high energy demandsof flight and endo- greeof fermentationin the crop,producing high lev- thermy(Morton 1978). els of VFAs (Grajal et al. 1989, Grajal 1995a). Al- Why, then, have mousebirdsnot evolveda larger thoughnot an obligatefolivore, the SpeckledMou- body size to overcomethermal constraints? A tempo- sebirdalso has VFAsin its foregut,which probably rally dynamicfruit-eating habit (when food is avail- areproduced by the variouslyshaped bacteria found able)may be a responseand meansof obtainingextra there. Although levels of VFAs that we found in energy.Folivory allows mousebirds to usea low-qual- SpeckledMousebirds are similarto thosein Hoatzins ity but freelyavailable diet but requiresspecializations (Grajalet al. 1989),much of the variationin VFA lev- of the GIT. Becauseenergy from leavesis not readily els betweenindividuals probably resultsfrom dif- available,this small-sizedfolivore reduces energy de- ferencesin the amountof leaf materialingested. Fur- mands with an energy minimization/conservation ther researchis requiredto determinethe actualfer- strategy.Mousebirds have labile thermoregulation mentationsubstrate and passagerates. (Bartholomewand Trost1970, Prinzinger 1988) and re- Unlike the Hoatzin, whose diet is 80% leaves(Gra- duceenergy costs of flightthrough gliding (pers. obs.). jal et al. 1989),the proportionof leavesin the diet of In addition,the abundanceof foodrequires less flying the SpeckledMousebird varied. However, Speckled time and fewer sear&es for meals. This increases the Mousebirdsin the laboratory can maintain body amountof time availablefor baskingand socializing. mass when feeding only on leaves (C. Downs un- SpeckledMousebirds per& vertically,projecting their publ. data). Consideringthe seasonalphenology of legs to facilitatesun baskingand exposingthe belly fruiting and the irregularity of fruit shortages, (andthe gut) to the sun(pers. ohs.). Mousebirds occur mousebirdsshould feed extensivelyon leaveswhen in groups,huddling to conserveenergy and to avoid 794 ShortCommunications [Auk,Vol. 117 the risks of roostingalone. Other small-to-medium- GRAJAL, A. 1995b. Structure and function of the di- sized birds are considered facultative folivores because gestivetract of the Hoatzin (Opisthocomushoa- theyinclude leaves in the diet seasonally(A1-Dabbagh zin): A folivorousbird with foregut fermenta- et al. 1987,pers. obs.). Mousebirds adjust to seasonal tion. Auk 112:20-28. fluctuationsin food abundanceby havinga broaddi- GRAJAL,A., AND S. D. STRAHL. 1991. A bird with the etarytolerance and a propensityfor folivory. guts to eat leaves.Natural History 100:(8):48-54. Acknowledgments.--Wethank J. Collier of the Ani- GRAJAL, A., S. D. STRAHL, R. PARRA, M. G. DOMIN- mal Nutrition and Animal Products Institute, Irene, GUEZ,AND A. NEHER.1989. Foregut fermenta- tion in the Hoatzin, a Neotropicalleaf-eating for the VFA analyses;J. 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