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Folivory and bill morphology in the Tooth-billed Bowerbird, Scenopoeetes dentirostris, (Passeriformes: Ptilonorhynchidae): food for thought PDF

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Preview Folivory and bill morphology in the Tooth-billed Bowerbird, Scenopoeetes dentirostris, (Passeriformes: Ptilonorhynchidae): food for thought

FOLIVORY AND BILL MORPHOLOGY IN THE TOOTH-BILLED BOWERBIRD, SCENOPOEETESDENT1ROSTRIS PASSER1FORMES: PTILONORHYNCHIDAE): < FOOD FOR THOUGHT CLIFFORD B. FRITH AND DAWN W. FRITH Frith. C.B. & Frith, D.W. 1999 06 30: Folivory and bill morphology in the Tooth-billed Bowerbird, Scenopoeetes dentirostris, (Passeriformes: Ptilonorhynchidae): food for thought.MemoirsoftheQueenslandMuseum43(2):589-596.Brisbane.ISSN0079-8835. The Tooth-billed Bowerbird, Scenopoeetesdentirostris, is a facultative, arboreal, folivore. Forasubstantial proportionofwinterdiettheytearandmasticatepiecesofleaves,succulent budsandvinestems,butinsummertheyaremostlyfrugivorous.Specialisednotches,cusps, or'teeth1 ontheirlowermandiblecuttingedgesfitintoreciprocal indentations inthe upper mandiblewhenthebillisclosed,tomoreefficientlycrushandmasticatevegetablematter.As a resultofthisdiet, birdscommonly voidcompactfaecal 'pellets' consistingpredominantly to exclusively offinely-masticated foliage. Folivory by this passerine in the resource-rich habitatoftropical uplandrainforestissurprisingandmaybeinpartduetothepresenceinits habitatofthreeclosely related bowerbird, andmany other frugivorous, species. Studies ofTooth-bill diet, nutrition, and associated morphology and physiology are required. O Folivory, billmorphology, bird 'teeth', mastication offoliage. Tooth-billedBowerbird, Scenopoeetes dentirostris. CliffordB. Frith&Dawn W. Frith, HonoraryResearchFellowsoftheQueenslandMuseum, 'Prionodura\ PO Box 581. Malanda4885,Australia; 17March 1999. The Tooth-billed Bowerbird, Scenopoeetes (1985a). Geoffrey Moore (unpubl. data) dentirostris (subsequently Tooth-bill), examinedtheroleofmalesasplantseeddispersal represents a monotypic genus ofthe bowerbird agents. Court seasonality, morphology, family, Ptilonorhynchidae, whose 19 species are dispersal, constancy and ownership are detailed endemic to Australia and Papua New Guinea. It in Frith & Frith (1994) and home range in adult occurs only in upland rainforests between males in Frith etal. (1994). 60105°-4124'0S01m45a°b1o8v'eE)m,eanenasreCaoloevketlo,wfnr,omsMouttAhwmaorsd The Tooth-bill is unique among bowerbirds in t(o Mt Elliot (19°30'S 146°57'E), just south of having a conspicuous irregular notch or 'tooth' Townsville,NQueensland,tropicalNEAustralia on the cutting edges ofthe upper mandible and (Nix & Switzer, 1991). Tooth-bills, like other several, more regular, cusps and notches on the polygynous bowerbirds, demonstrate male tip and cutting edges of the lower mandible promiscuity and female-only nesting duties. respectively. These 'teeth' were long considered They are, however, atypical in being sexually adaptations used solely toobtain leaves forcourt monomorphic, short and stout-billed, and in decoration, by biting, snippingorsawingattheir court-clearing males that form exploded leks petioles (Marshall, 1951;Gilliard, 1969; Chaffer Frith & Frith, 1985a, 1993, 1994, 1995). 1984). In support ofthis interpretation Marshall ( (1954) and Chaffer (1984) noted that the means Male Tooth-bills clear leaf litter to form a by which Tooth-bills obtained leaves for the display area on the forest floorabout the base of court was laborious and arduous; birds havingto at least one tree trunk and collect fresh large tearand sawatleafpetioles,particularly thoseof A leaves to lay them paler side uppermost on this larger ones such as the gingers (Alpinia spp.). court. Courting starts with singing and court fully-developed 'toothed' bill adorns birds of maintenance from late August to September and both sexes and all post-juvenile ages, while only continues toJanuary orearly February (see Frith oldermales(probably>2-3 yearsold,pers. obs.) & Frith, 1993, 1994). decorate courts with leaves. Jackson (1909, 1910), Marshall (1951, 1954) By far the most commonly used leaves for and Warham 1962)made preliminarystudiesof court decoration at Paluma, near Townsville, N ( males and courts, and limited knowledge of Queensland were those of the small tree nesting biology is summarised by Frith & Frith Polyscias australkma (see Frith & Frith, 1994), 590 MEMOIRS OF THE QUEENSLAND MUSEUM but this is not necessarily the case elsewhere average 64% of daylight upon such favoured (pers. obs.)- Leaves ofP. australianaare quickly perchesduringtheirpeakdisplayseason(Frith& and and easily removed from the plant by male Frith, 1994, 1995) faecal samples were large. Tooth-bills. It is possible that differing leaf Because Tooth-bills swallow whole the vast attachment strengths of plants accounts for the majority offruitstheyeat (largerfigs, Ficus spp, observed differences in Tooth-bill effort in leaf excepted) seeds are intact, and no regurgitation removal. occurs, these samples represent an accurate Recent observations have demonstrated that indication of fruit diet. In addition to work on Tooth-bills are partly folivorous and that the males at courts, the feeding ecology of the externally-toothedbill isanadaptationtothisdiet species was examined by recording all observed & & bowerbird foraging during l,360hrs of (Lavery Grimes, 1974; Frith Frith, 1979and standardised transect and quadrat observation unpubl. data). Tooth-bills certainly usethe 'tooth- like8 structures ofthe mandible edge to cut, tear, and an additional 187h of random observation and manipulate leaves and leafpieces (Lavery & through Tooth-bill habitat. These observations Grimes, 974). However,betweentheseexternal resulted in 533 records of Tooth-bills feeding serrations1 lie a more sophisticated and complex upon plants. set ofstructures, alluded to by Marshall (1954: Subsequent to the report that Tooth-bills eat 154)whose function equates more closely to that foliage by tearing leaves, buds and vine stems of 'teeth'. This contribution provides an initial and manipulating and masticating them prior to & & description ofthese structures ofbill and palate ingestion (Lavery Grimes, 1974; Frith Frith and illustrates graphically how they function to 1979), we closely examined the bill of several finelymasticate foliage priorto ingestion. Wedo living and preserved Tooth-bills for physical not review comprehensively the morphology, adaptations to such folivory. ecology, nutrition or physiology associated with this unusual passerinediet. Ouraim inpresenting RESULTS thisreviewofourinitialfindingsis,asthesubtitle implies, to stimulate the interest of appropriate Tooth-bill folivory typicallyinvolvedaquietly specialistsintheseaspectsofTooth-billbiology. perched solitary bird biting or tearing offpieces offresh leafor vine stem growth. Once a larger METHODS piece ofleafwas removed from the plant it was rapidly, skillfully and repeatedly 'folded' in the We studied male Tooth-billed Bovverbird mandible tips into a compact wad. This was then sociobiology and ecology from 1978 to 1990 in masticated or 'chewed' between the mandible rainforest near Panama (19°00'S 146°IO'E), N tips before being ingested; green fluid resulting Queensland at an elevation of -875m ASL. fromthemasticationoftenvisiblyaccumulatedat Subsequent qualitative work was carried out on thetipofthemandibles(Frith & Frith, 1979)and the Alherton Tableland (I7D25'S 145°42,E - presumably with some ingested. 680m ASL). Intensiveannual fieldworkbegan as The majority of Tooth-bill excreta accumu- soonas males started singingand/orclearingand latedbeneath favouredcourtperchesconsistedof decoratingcourts (Septemberorearly Octoberat an amorphous mass (with some, more recently Paluma); and annual fieldwork ceased when produced, discrete faecal 'pellets1) offruit peri- singingandcourtusagedeclined(duringJanuary carp and seeds, the quantity of this increasing or early February). Court attendance, displays during seasonal peak court attendance (Frith & and vocalisations were monitored intensively Frith, 1995). Some 5 to 10% ofmonthly excreta from 7 November to 8 December 1979 and samples consisted of faecal 'pellets' pre- October 1980 to 14 February 1981 (see Frith &1 dominantly or exclusively composed of Frith, 1993, 1994, 1995; Frith et al., 1994). To finely-masticated vegetablematter(see Figs 1 & learn what male Tooth-bills ate during their 2A). The smaller samples ofsuch faecal matter court-attendance season we erected ~50cm forOct-Dec,comparedwith Sept, 1979aredueto piecesofblacknylonfinemesh-10cm abovethe lower court attendance levels by males due to forest floor beneath low (<1.5m) court perches unseasonally dry conditions (Frith & Frith, favouredby males. Excretavoidedbybirds from 1994). It must be noted that the percentages in theseperchesaccumulatedonthenylonandwere Fig. for leaf matter are minimal because we 1 collectedweeklyforsubsequentanalysis(Frith& scored each entire pellet of same as one 'leaf Frith, 1994 & unpubl. data). As males spent on record whereas the remaining mass of fruit FEEDING IN THE TOOTH-BILLED BOWERBIRD 591 DISCUSSION FOLIVORY. Habitual folivory is a rare trait among birds. However, the New Zealand k avifauna is exceptional in this regard, having L evolved in the absence of competion from browsing mammals (I. Flux, pers. comm.). A A'Q7S8ONDJFMAMJ JASMoOntNhDsJFMAMJ JASONDJ,WF nfoltiagbhlteletsesr,resntroicaltuarnndala,rboKraekalapfoo,livoSrteriisgotphse habroptilus, an extraordinary parrot endemic to FIG. 1. Percentage of total weekly excreta samples, New Zealand temperate forests which browses collected beneath court perches favoured by court-attending male Tooth-billed Bowerbirds, plants by masticating leaves and fronds, often in consisting offaecal pellets primarily ofmasticated situ on some plants (Merton, 1985). Elsewhere leafmatter(solidbars)andthepercentageofsampled folivory is common typically among the non- trees that were bearing fruit (open bars) over three passerine groups of: waterfowl, which feed upon courtship seasons (see text). aquatic vegetation or graze upon terrestrial grasses and herbage; some terrestrial game bird remains were scored by constituent fruits (as groups including the palearctic Black Grouse, indicated by seed numbers). While these data Tetrao tetrix, and Western Capercaillie, Tetrao were only obtainable during the months that urogallus (Phasianidae), (Dorst, 1974); some malesattendedcourtstheydosuggestanincrease rails; and several other species (Dorst, 1974: 70; in folivory when fewer fruits were available in Morton, 1978; Carboneras, 1992; Taylor, 1996). the habitat (see Fig. 1. text below, and Frith & True folivory is also well known in the extra- Frith, 1995, 1998). ordinary, neotropical, Hoatzin {Opisthocomus hoazin, an aberrant cuckoo) that lives inriverine While details ofdirect observations ofTooth- gallery forest subject to flooding (Dominguez- bill foragingwillbepresentedelsewhere,wenote Bello et al., 1994; Thomas, 1996) thatof533 recordsoffeedinguponplantmaterial Folivory is particularly rare among arboreal observed, 79% were upon fruits and 21% (n = passerines. It is known, however, as typical 111) upon otherplantmaterialas follows: leaves foraging in the three neotropical plantcutters (n = 90), flowers (8), succulent stems (7) and (Phytotoma spp., Cotingidae: Kuchler, 1936; buds (6). We stress that we considerthis 21% of Ames, 1971; Lanyon & Lanyon, 1989; Sibley & annual diet as folivory to be a gross under- Ahlquist, 1990) of open woodland and scrub estimate, because Tooth-bills eating foliage (Ridgely & Tudor, 1994) and in three species of (particularly during winter when they become saltator (Saltator spp., Emberizidae) ofsecond- silent,secretiveandinactiveintheforestcanopy) ary growth, gardens, plantations and forest ed^e are extremely cryptic while birds taking fruit are (Jenkins, 1969; Stiles & Skutch, 1989). The much more conspicuous because fruiting plants Kokako (Cailaeas cinerea. Callaeidae) ofNew attract numerous bowerbirds and other frugiv- Zealand temperate forests is conspicuously orous birds (pers. obs.). folivorous and will eat yellowing, dehiscent, or even brown and dead, leaves of some plants During winter, Tooth-bills become so elusive (Hay, 1985; I. Flax,pers. comm.; pers. obs.). Itis that some observers believed they left their also known in the Common Bullfinch, Pyrrhula upland rainforest breeding habitat (e.g. Green, pyrrhula(Fringillidae), and several otherspecies 1910). As a percentage of directly-observed (Dorst, 1974) which eat buds more than leaves, Tooth-bill foraging events, folivory increased butisotherwiseonlyoccasionallyobservedasan during periods of least fruit availability within irregular and small dietary component in few othbesehravbeidtatfo(lFiivgo.ry1)w.aTshe>2p0er%cebnuttagaet toifmdeisremctalyy bpaoswseerrbiinredssp:ecFireisth(i.e&. sFormiteh,bir1d9s7o9f;paDroandaisgeheavn,d & reach 25-40% (Fig. 3) which, for winter months 1981, 1996; Frith Beehler, 1998). It is at least,weconsideran underestimate(asabove). doubtless more widespread than is indicated by The gizzard ofa male Tooth-bill that died on 14 present knowledge. June 1989 contained 7.8g of finely-masticated It has been noted that Hoatzin selectively eat leafmash(seeFig. 2b);theentiregutbeingfullof 'young leaves, tendershoots andbuds,which are finely-textured green leafy slime. higher in water content, as well as being both 592 MEMOIRS of THE QUEENSLAND MUSEUM t £= 40 'i il i I-llILH M-mLh;; cm FIG. T Number (left axis) ofobservations ofTooth- I billedBowerbird feedingsnearPalnma,Queensland. upon fruit(openbars)and foliage(solidbars),andthe U iin I iiiialiUmh !"!• -'I percentage (right axis) records of foliage eating representedoftotal feedingeventsduringeachmonth (line CUrVe With solid squares). Data foi August i97S-Februar\ 98 inclusive are combined. I I probably limits folivory in passerines, this diet being far more common in larger birds and especially those with fewer predators. That this rare avian diet and associated bill adaptation1 occurin theTooth-bill begstheobviousquestion: why so in this passerine It is possible that lower fruit resource availability in Winter has resulted PIG. 2. A, fresh Tooth-hilled tiowerhird faecal pellet in the need for obligate frugivores to perform consisting predominantly of finely-masticated leaf folivory as an adaptation to winter survival, but (m[rabitogtthethr)-bwoiifltlFheidnleoBlroyn-wmseacrasWlteircdiantgdeiidczazltaeeraddfImBla,etfttf)ererasnh(dlryuiltdesircswosniettcethnetd S1u9p9p8o,rttiig.ng2cda).taAnareadleeqwua(tFeigasnIs&we3r;wFirliltdho&ubFtrlietshs. and 5mm markings}. Both near I'akuna.Queensland.I require considerable research and lime. It lias June 1989. been noted that the extraction of energy from leaves requires a relatively long food retention easier to digest and more nutriJJCMS1 (Thomas, time and that large quantities must be ingested I996). This Statement applies equally to the ant! stored; circumstances which present major Tooth-bill m our experience. The Hoatzin is disadvantages for flying animals (Morse. 1975; remarkable, however, in that Us crop and lower Morton, 1978; Sibly, 1981). An alternative Oesophagus are its main digestive organs. strategy is for rapid throughput ofplant material sIilmoiutl/airnswafyermteontthveeggeuttatifoenrmmenttahteiofnoreoig~utcamttlea Twoiotthh-mbiinlilmarlemadiignesstmioanrk(eSdilblyy,in1a9c8t1i)v.e Tahned (tIoS9t9rt3ah;helTdheiotgmeaaslst,i,on1L999o8[$9');,suDPcohhynsiiamonultoiugneiuzcs-aulBacalidlaaopntdaettipoarlne.s-, Tawphhpueasnrenftothlleiyvolfrloyiwesqueliinttetelregpoedstusiricibnlgdyetdhmoeamniwdinnsatteeorsi"miotesnatdtihiesnt,g. (abundant) leaves might outweigh the costs of sumably low carbohydrate/energy diet, such as seeking (sparse! winter fruits, As predator dn (ifonly seasonally) elongated gut Isee Sibly, pressure may be important in explaining why 1981), might be expected. These have not, folivory is rare in birds (Morton, 1978), par- however, been looked Forin Tooth-bills, or in the ticularly in passerines, the highl) cryptic several other bovverbird species which also ea1 plumage and folivorous foragingofbothsexesoi We foliage to a lesser extent. did not investigate the Tooth-bill are noteworthy. the relative nutritional values of plant foliage- eaten by Tooth-bills, and this remains a Held lor Satin Bowerbirds, Piiionorhynchus Violacepa, future study. form flocksin ihewintertoearlyspringandthen, typically, cattencstriai herbs and grasses in both Foliage represents a dietary component low in rainforest and woodland (Donaghey, 1981; readily available carbolivdrate/enerev content Vellenga & Vellenga, 1985. pets. obs.). These (Sun et aL IW7; Powlesland et nl., 1997). The plants may represent a seasonally significant energetic disadvantage of small body si/e proportion oftheir diet (c. 50-80% according to FEEDING IN THE TOOTH-BILLED BOWERBIRD 593 FIG. 4. A, bill and fore skull of a Tooth-billed Bowerbird [seethesameprofile in Fig. 5]). B, inside oftheupper(above)andlower(below)mandibletips with the cusps (on the latter) and reciprocal indentations or pits (on the former) indicated with black lines. Donaghey, 1981). Satin Bowerbirds appear to have played some role in the evolution of its 'chew' leafmatter in the mandible tips prior to folivorythroughinterspecificcompetition(Lack, & ingesting it. Male Satin Bowerbirds (and other 1971; Lavery Grimes, 1974), particularly avenue bower building species) also masticate during strong competitive pressure exerted by foliagetoproduce 'paint' whichtheyapplytothe leanseasons. Intheuplandwettropicalrainforest inner surface of bower walls (Marshall, 1954; habitat ofthe Tooth-bill, the winter months are Gilliard, 1969; Donaghey, 1996; pers. obs.). It resource-poor with respect to both arthropods shouldbenoted,however,thatSatinBowerbirds, (Frith&Frith, 1985b;Frith,D.&Frith,C, 1990), including those populations (P. v. minor) which female Tooth-bills feed to their offspring sympatric with Tooth-bills do so in habitats asasmallproportionoftheirdiet,andfruits(Frith adjacent to, but outside, the rainforsts within &Frith, 1994).Suchascenariomight,inaddition which Tooth-bills perform their winter folivory to a lackofpredators,have in part influencedthe (Frith & Frith, unpubl. data). evolution ofpartial folivory in the NewZealand Kokako as this (now endangered) passerine Donaghey (1981, 1996) found that Satin sharedmuchofitshabitatwithtwo,predominatly Bowerbirds living in subtropical woodland ate insectivorous, closely related members of the more leaves during winter to early spring, than same family (the Saddleback, Philesturnus those living in adjacent rainforest, suggesting carunculatus and the, now extinct, Huia, that the latter area was richer in other foods. As Heteralocha acutitostris). The folivorous, and tropicalrainforests are rich indiverse avian food now endangered, flightless Kakapo similarly resources it is surprising to find substantial sharedhabitatwith uptofourotherNewZealand folivory in the Tooth-bill. The Tooth-bill is endemic parrot species. sympatricwiththree,predominantly frugivorous bowerbirds (Spotted Catbird, Ailiiroedus BILL MORPHOLOGY. With respect to fruits, melanotis, Satin Bowerbird and Golden Tooth-bills are 'gulpers' (Levey, 1990) in that Bowerbird, Prionodura newtoniana) and a they swallow fruits whole with their seed(s) number ofother, obligate, frugivores. This may intact,donottypicallyusetheir"teeth' toremove 594 MEMOIRS OF THE QUEENSLAND MUSEUM indigestable fibre as do many trugivores The most important point concerning the Tooth-bilPs use of lower mandibular 'teeth' is that their five functional lips, or cusps, fit perfectly inlo reciprocal indentations, or pits, in the under surface of the distal premaxilla (see Figs 4, 5). These specialised structures form efficient grinding 'teeth' for Tooth-bills by creating pressure points for foliage mastication (Fig. 6). Notwithstanding their folivory, there is nocomparablesophisticationofbill moq^hology in Satin Bowerbirds. Various bill modifications to deal with FIbGll.le5d.BAowseirmbpilridfibeidllsicnhpermoaftiliecsdhioawgirnagmhoofw:ithie'coioitshp- (vJeoghentsagbalred,mat1t%eSr)araendknsoomwen oitnhetrhegrwoautpesrf(oswele atthetipoftfae lowermandible(lowera)andthoseon above). We were able to briefly examine a its cutting edges (lower b & c) fit into the reciprocal freshly-thawed kokako specimen while in New indenlations (dotted lines) in [he upper mandible Zealand in May 1998 and Foundstructures on the (upper a,h &c) when the mandibles are closed to central palate ofthe upper premaxilla that may masticate foliage. See also Fig. 4. function in mastication of vegetable matter. However, this possibly novel adaptation awaits fleshoflarge-seeded fruits, anddonot regurgiate confirmation m additional specimens, and an seeds. The more easily digested nutrients, of proteins and soluble carbohydrates, in plant understanding of its function, and formal foliage cells are protected by cellulose walls description (1. Flux. pers. comm.). which vertebrates lack theenzymes todigest, and It is noteworthy that theconsiderableliterature the cell walls must therefore be mechanically on the Uoal/in and its fohvorous diet does not broken up (Sibly. 1981). Details of direct appear to allude to any kind of mastication of observation of Feeding Tooth-bills combined vegetationor to morphological adaptationsofthe & with knowledge gained by examination of inner mandibles fordoing so (Thomas. 194o several preserved and living individuals suggest references therein). However, the cutting edges to us that: a) the cutting edges o\ the reciprocal mandibular notches (Fig 4a) are used to bileortearandthen manipulate and fold leaf pieces into a compact wad prior to masti- cation, and thai b) the lower mandible "teeth*, used in a .• 'chewing' action, enhance digestibility of foliage by crushing and grinding, Thus the Lteeth' servetobreak upthe cell walls of the foliage. The nature of voided faecaI 'pellets' of masticated leaf matter (Fig. 2a) suggest that Tooth-bills might not digest plant Fibre asdocs the Hoat?in. , but merely break down plant cells and so release their digcslahle content; but this FIG HfraPalroiolohf-htihlelebdaiUowreirbi iProdhtsccotutrit&aa;,u/atrcrouarJtrmdaecloeraaftfioonu.ndNoftreeshtlhyatlIahied requires experimental study. i ;c' marks left by (he bird's bill clearh the pressure points Certainly male Tooth-hills at Where tlie five lower mandih meet the reciprocal indenlations their courts do not regurgitate (indicated) in the upper mandible (see Figs 4 5). FEEDING IN THE TOOTH-BILLED BOWERBIRD 595 ofthe mandibles ofthe three neotropical plant- DOMINGUEZ-BELLO, M.G., LOVERA, M., cuttersareconspicuoulsyserrated,presumablyto SUAREZ, P. & MICHELANGELI, F. 1993. enhance their cutting (and masticating?) funct- Microbial inhabitants in the crop ofthe Hoatzin ion. While many ofthepan-tropical (Australasia (Opisthocomiis hoazin): The only foregut ferrnenter avian. Physiological Zoology 66: excluded) non-passerine barbels (Piciformes, 374-383. Cnaopticthoendidaoer) s'htooowthaeddi'vermsaintydiobflceonsepdigceuso,usnloy DOMnRMUGIUZ,EZM-.CB.E,LGLAOR,GIM.AG,.,A.MI&CHREOLDARNIGGEULEIZ,,FE.., evidenceto suggestthesemightbeused in foliv- 1994. Ecology of the folivorous Hoatzin orous feeding appears to exist notwithstanding {Opisthocomushoazin)ontheVenezualanplains. long-termintensivecollectingandobservationof Auk 11 1:643-651. African and Asian species. A recent review of DONAGHEY, R.H. 1981. The ecology and evolution diets ofall African species makes no mention of ofbowerbird mating systems. Unpublished PhD foliagefoundinbirdsorseentobeeatenbythem Thesis, Department of Zoology, Monash (Short&Home, 1988). TheGreatBarbet,Mega- University, Melbourne. laima virens, has alongbutvisiblyunnotched or 1996. Bowerbirds. In Strahan, R. (ed.) Finches, 'toothed' bill but has, however, been noted to b(oAwnegrubsi&rdsRob&ersottshoenr:pSaysdsneeryi)n.es of Australia. avidly eat flower petals by Lthe whole flower beingfirstrevolvedandcrushedinthemandibles DORS&T,J. 1974.Thelifeofbirds.Vol. I. (Weidenfeld Nicolson: London). (anAdHc&omRpipalcetye,d1i9n7t0o).boTlhuesessaomfecaruutmhoprlsednopteetatlhsat1 FRITHp,araCd\iBs.e:&PaBraEdEisHaLeiEdRae,.(BO.xMf.or1d99U8n.ivTerhseitbyirPdrsesso:f the Green Barbet, M. zeylanica, eats flower Oxford). petals. FRITH, C.B. & FRITH, D.W. 1979. Leaf eating by We suggest that the mandibles and palate of birds of paradise and bowerbirds. Sunbird 10: specimens of all folivorous birds, and any sus- 21-23. pected ofbeing so, be examined forthe possible 1985a. Parental care and investment in the Tooth- presence of structures for the mastication of billed Bowerbird, Scenopoeetes dentirostris (Ptilonorhynchidae). Australian Bird Watcher foliageasthismightproveinstructive. Therecan 11: 103-113. be no doubt that studies of Tooth-bill diet, nutrition, and associated morphology and 1985b. Seasonality of insect abundance in an Australian upland tropical rainforest. Australian physiology will prove rewarding in the broad Journal ofEcology 10: 237-248. context ofavian folivory. 1993. Courtship display of the Tooth-billed Bowerbird Scenopoeetes dentirostris', its ACKNOWLEDGEMENTS behavioural and systematic significance. Emu 93: 129-136. Wearemostgratefulto AlanTennysonand Ian 1994.Courtsandseasonalactivitiesatthem bymale Flux of Wellington, New Zealand, for the Tooth-billed Bowerbirds Scenopoeetes eopxpaomritnueniatyspteocidmiescnusinstKheokflaeksho. eWceolpoagryticaunldarltyo 199dQ5eun.eteiCnroossultarrntidss(MiPtuteisleconuoonmrsht3ya7nn:cch1yi2,d1a-ed1)i4.s5pM.eermsoiionr,somfatlhee thank Ian Flux, Eugene Morton, Peter Woodall survival and court ownership in the male and an anonymous referee for kindly comment- Tooth-billed Bowerbird, Scenopoc* te ingconstructivelyonadraftofthiscontribution. dentirostris(Ptilonorhynchidae),Emu95:84-98. 1998. Nesting biology of the Golden Bowerbird LITERATURE CITED Prionodura newtoniana endemic to Australian upland tropical rainforest. Emu 98: 245-268. ALI, S. & RIPLEY, S.D. 1970. Handbookofthe birds FRITH,D.W.&FRITH,C.B. 1990.Seasonalityoflitter of India and Pakistan. Volume 4. (Oxford invertebrate populations in an Australian upland University Press: Bombay). tropical rain forest. Biotropica22: 181-190. AMES, P.L. 1971. The morphology ofthe syrinx in FRITH, C.B., FRITH, D.W. & MOORE, G.J, 1994. passerinebirds. Bulletinofthe Peabody Museum Home range and extra-court activity in the male ofNatural History 37: 1-194. Tooth-billed Bowerbird Scenopoeetes CARBONERAS, C. J992. Family Anatidae. In del dentirostris (Ptilonorhynchidae). Memoirs ofthe Hoya,J., Elliot. A. & Sargatal,J. (eds) Handbook Queensland Museum 37: 147-154. ofthe birdsoftheworld. Vol- 1. (Lynx Edicions: G1LL1ARD, E.T. 1969. Birds ofparadise and bower & Barcelona). birds. (Weidenfeld Nicolson: London). CHAFFER, N. 1984. In quest ofbowerbirds. (Rigby: GREEN, B. 1910. Tooth-billed Bower-bird. Emu 9: Adelaide). 247. . 596 MEMOIRS OF THE QUEENSLAND MUSEUM HAY, J.R. 1985. Kokako Callaeas cinerea. In arborealfolivores.(SmithsonianInstitutionPress: Robertson, C.J.R (ed.) 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