A FEEDING ADAPTATION OF THE JAW ARTICULATION IN NEW WORLD JAYS (CORVIDAE) RICHARD L. ZUSI NationalMuseum of Natural History,Smithsonian Institution, Washington, D.C. 20560 USA ABSTRACT.--Thejaw articulationof mostendemic New World jays(Corvidae) has a condyle of the quadrateand an opposingcotyla of the lower jaw not found in other birds. They also have well-developed meatic articular facets of the quadrate and cranium. The tip of the rhamphothecaof the lower mandible is chisel shaped.These and other featuresconstitute a functionalunit, the buttresscomplex, that bracesthe partiallyopened lower jaw and enhances its use as a chisel. The buttresscomplex stabilizes the lower jaw by anchoringthe jaw on the quadrateand reducing torque on the quadrateduring pounding. A hypothesisof pounding with the lower mandible was confirmed by field observationsof Aphelocomacoerulescens coerulescens,which stabsacorns with the lower mandible and then tears off the shell using both mandibles.This may be an unusually effective method of peeling acorns,and it differs from the techniquesused by Garrulusand Pica.The origin of the complexmay not be associated with acorn eating. A slight modification of the jaw articulation in Cyanolycaprobably rep- resentsthe evolutionary precursorof the buttresscomplex. The distribution of the complex in the Corvidae suggeststhat Cyanolycais the sistergroup of other endemic New World jays. Gymnorhinusis related to the New World jays, not to Nucifraga.An exampleof convergent evolution is provided by Hemignathuswilsoni (Drepanidinae). Received 15 August1986, accepted 22 April 1987. MANY members of the Corvidae pound hard found only in certain New World jays and are food items with the tip of the bill while holding clearly associatedin somespecies with a special the food against a firm substrate with one or technique for opening nuts, especiallyacorns. both feet. Most birds that pound with their bills Within the Corvidae, however, the occurrence on a hard substrate(e.g. woodpeckers)use both of this charactercomplex does not correlatewell mandiblesor primarily the upper for the trans- with the occurrenceof acorn eating; it appears mission of force (Spring 1965). Becauseof its to representan evolutionary novelty of broader unstablesuspension from the cranium, the low- ecologicalsignificance within the family. er jaw alone appearsnot to be an effective im- plement for strong pounding. For this reason MATERIALS AND METHODS my curiosity was aroused by an unusual con- figuration in the lower jaw and quadrate of a I examinedskulls of 76 speciesfrom all genera of the Corvidaeexcept Temnurus and Zavattariornis.The New World jay that implied use of only the jaw articulationsof 2 additional specieswere ob- lower mandible in pounding. I studied modi- servedin skin specimensby softeningand reflecting ficationsof the lower jaw and its articulation as a flap of skin. I alsoexamined 13 speciesfrom 4 fam- a functionally integrated charactercomplex. The ilies allied to the Corvidae. To determine the action variation and taxonomic distribution of this of the jaw articulationand its ligaments,I manipu- apomorphouscomplex have somephylogenetic lated a freshly killed BlueJay (Cyanocitta cristata) and implications within the Corvidae (sensuBlake American Crow (Corvusbrachyrhynchos). Information and Vaurie 1962). aboutontogenetic stages of the featuresunder study Although acornsand other nuts are impor- was obtainedby clearingand staining(Taylor 1967) tant food items for many speciesof Corvidae, two nestlings of the Florida Scrub Jay (Aphelocoma coerulescenscoerulescens) and by dissectionof a hatch- the only well-defined modificationof the bill ling FishCrow (Corvusossifragus). Jaw muscles of an for cracking nuts is the rhamphothecalbulge adult EurasianJay (Garrulus glandarius) and one adult in the lower jaw of the nutcrackers(Nucifraga; Blue Jaywere dissected.I drew the original illustra- references in Turcek and Kelso 1968). Most tions in pencil, using a dissectingmicroscope and corvidshave stout bills capableof a variety of drawing tube for all anatomicalfigures; final figures manipulations.The modificationsI describeare were inked by an illustrator.Field observations,pho- 665 The Auk 104: 665-680. October 1987 666 RICHARDL. ZUSI [Auk, Vol. 104 palate of different speciescould be compared.The system was assumedto remain in static equilibrium. Mag- upperjaw nitudes and directions of some force vectors were set arbitrarily; magnitudesand directionsof all others were determined graphically by assumingthat the sum of all torques equaled zero and that the sum of all force componentson the x- and y-axesof each bone equaled zero. Slight discrepanciesfrom zero resultedfrom errorsin graphing.Gravity was ignored I / quadrate becauseits effecton the systemin a living bird would / t•,m;aniccavity be highly variable.All numericalvalues for vectors cranium represent indices that are proportional to vector lengths.These indices are usefulfor comparison,but units of force or torque are unspecified. I use the term "jaw" when referring to the entire lower jaw or only to its articulation. "Upper mandi- ble" and "lower mandible" refer to the rostral por- tions of the jaws coveredby rhamphotheca."Bill" refers to both mandibles. Anatomical terminology generallyfollows Baumel et al. (1979),but 5 new terms are proposed:cotyla prootica (prootic cotyla) and cotyla squamosa(squamosal cotyla) of the cranium for the articular depressions that receive the prootic and squamosalcondyles of the quadrate;processus meaticus (meatic process)for the processof the quadrate that articulateswith the suprameaticprocess of the squa- mosal;condylus rostralis (rostral condyle) of the quad- rate and cotylarostraIis (rostral cotyla) for new struc- tures of the quadratomandibulararticulation. Foruniformity throughout the family Corvidaeand conveniencein referring to groups of speciesby a generic name, I use the scientificnomenclature of Blake and Vaurie (1962); for Drepanidinae I follow Greenway(1968). Common names are from the A.O.U. Fig. 1. Osteologyof the jaw articulationin corvids. Check-list (A.O.U. 1983) and Goodwin (1986). (a) Skull of GarruIusglandarius, lateral view. Box in- cludesmajor features discussed in thispaper. (b) Low- er jaw and quadrateof Picanuttalli. (c) Aphelocoma RESULTS coerulescens.Note buttressin Aphelocoma. MORPHOLOGY Osteology.--Thispaper is concernedwith the suspensionsystem of the lower jaw, including tographs,and motion pictures(8 ram, 36 frames/s)of the feeding behavior of the Florida ScrubJay were the jaw, quadrate,and cranium (Fig. la, b). Al- obtained at the Archbold BiologicalStation in Lake though the upper jaw and palate are linked to Placid, Florida, during 10-18 September 1983, and the suspensionsystem, they are peripheral to brief observationsof a captive American Crow were this discussion.In certain jays the suspension made in Maryland. system,hereafter called the jaw articulation,dif- An analysisof hypotheticalforces on the jaw artic- fers from that of other corvids by the presence ulation during mandibular pounding was undertaken of a prominent buttresson the lower jaw (Fig. [seeBock (1966, 1968) for similar analysespertinent lc). to birds].The analysisis not intended to reflectactual In most corvids [illustrated by the Yellow- forcesin the living bird becausethe musclesacting billed Magpie (Picanuttalli) in Fig. 2] the quad- on the systemare unknown, the exactdirection and magnitudeof eachforce are unknown,and the planes rate articulateswith the lower jaw by a rounded of rotation of the lower jaw and quadrateare neither medial condyle and an elongate, obliquely constantnor preciselyknown. Nevertheless,the anal- transversesurface formed by the confluenceof ysisproduced a setof hypothetical,relative values by the lateral and caudal condyles.In the closed which functional properties of the jaw articulations position the latter condyles abut on the elon- October1987] Adaptationin NewWorld Jays 667 lateral cotyla Fig. 3. Quadrateand lower jaw of Aphelocomacoe- rulescens,showing right quadrate(upper two figures) and right ramusof lower jaw (lower three figures). Top to bottom: lateral, ventral, dorsal, caudal, and Fiõ. 2. Quadrate and lower iaw of Pica nuttalli, caudodorsolateral views. showinõriõht quadrate(upper two figures)and riõht ramusoœ lower iaw (lower three fiõures).Top to bot- tom: lateral, ¾entral, dorsal, caudal, and caudodor- the lower jaw is opened wide and the intercot- solatera1 ¾iews. ylar crestabuts the intercondylar groove of the quadrate.Most corvids conform to this descrip- tion. Somejays (illustratedby Aphelocomacoerules- gate, lateral cotyla of the lower jaw, and the censin Fig. 3) possessan additional condyle of medial condyle rests on the caudal end of a the quadratomandibular articulation, the ros- well-defined roedial cotyla of the lower jaw. tral condyle, and an additional cotyla of the Upon opening, the lower jaw slides caudolat- articular fossaof the lower jaw, the rostral cot- erally with respectto the quadrate,which itself yla. The rostral condyle consistsof a convex rotates rostromedially about its cranial articu- articular surface oriented rostroventrally on a lation. The medial condyleof the quadrateslides pedicel of the quadrate,located rostrodorsal to restrally along the medial cotyla, guided by its the lateral condyle. Facing it is the articular prominent lateral wall. Backwardsliding of the surfaceof the rostral cotyla of the lower jaw, partially opened lower jaw is resisted weakly located rostral and