Monophyly of the Falconiformes Based On

Home , Accipitrinae, Cathartes, Falconinae, Microhierax, Parabuteo, Polihierax

The Auk A QuarterlyJournal of Ornithology Vol. 111 No. 4 October 1994

The Auk 111(4):787-805, 1994

MONOPHYLY OF THE FALCONIFORMESBASED ON SYRINGEAL MORPHOLOGY

CAROLE S. GRIFFITHS Departmentof Ornithology,American Museum of NaturalHistory, Central Park West at 79thSt., New York, New York 10024, USA; and Departmentof Biology,City College of CityUniversity of New York, ConventAvenue and 138thStreet, New York,New York 10037,USA

ASSTRACT.--Thesystematic relationships of the diurnalbirds of prey (Falconiformes)are unresolved.The monophylyof the orderhas not beenestablished, and the relationshipsof the familieswithin the orderand of generawithin the threepolytypic families are unclear. To derivea phylogenyfor the orderand to assessthe usefulnessof thesyrinx for resolving the systematicsof nonpasserines, I analyzed variation in syringealmorphology of genera within eachof the currentlyrecognized families in the orderas well asamong four orders of outgroups.The phylogeny derived from these syringeal data supports the monophyly of theFalconiformes. In addition, syringeal data provide strong support for themonophyly of threeclades within the Falconiformes:the Cathartidae;the Falconidae;and an Accipitrinae- Sagittariidae-Pandioninaecluster. The Cathartidaeare positionedas basalto the other two clades.Overall results indicate that syringealmorphology is conservative,with mostof the informativevariation occurring at highersystematic levels. Received 10May 1993,accepted 24 October 1993.

OF THEAPPROXIMATELY 30 orders of birds, the previously(Jollie 1976, Sibley and Ahlquist order Falconiformes offers some of the more 1990),and only a summarywill be presented interestingsystematic questions; the monophy- here.The orderhistorically has been united by ly of the order is in question,as are relation- several external morphological characters shipsof familieswithin the order,and of genera (hookedbeak and curvedtalons) and by several within each of the families. Falconiformes cur- internal characters(biceps slip absent,ambiens rently consistsof 76 generaand 290 speciesdi- present, caeca rudimentary; Beddard 1898). vided into four families (Stresemann and Area- However, four current classificationsdisagree don 1979):Accipitridae, including Accipitrinae on the monophyly of the order, and on sub- (hawksand eagles,59 genera,217 species)and ordinal and familial relationships(Fig. 1). Two Pandioninae(Osprey, monotypic); Falconidae considerthe order monophyletic(Stresemann (falcons, 10 genera, 62 species);Cathartidae and Amadon 1979,Storer 1971),while the other (New World vultures,5 genera,7 species);and two propose either removal of the Cathartidae Sagittariidae(Secretarybird, monotypic). from the order (Sibley and Ahlquist 1990) or Comprehensivereviews of the historyof fal- inclusionof Strigiformes(owls) within the or- coniform classificationhave been published der (Cracraft 1981).

787 788 CAROLE S. GRIFFITHS [Auk, Vol. III

Cathartidae Cathartidae

Accipitrinae

Pandioninae F AccipitrinaePandioninae

Falconidae Falconidae

Sagittariidae Sagittariidae

Storer 1971 Stresemann and Amadon 1979

Cathartidae Cathartidae

-- Accipitrinae Ciconiidae Falconinae -- Accipitridae

-- Pandionidae Pandionidae

Strigidae Sagittariidae Sagittariidae Falconidae

Cracraft 1981 Sibley and Ahlquist1990

Fig. I. Four recent, conflicting classificationsof the Falconiformes.

The idea that the Cathartidaemay not belong 1898, Brown and Amadon 1968) have been sug- in the orderhas been proposed previously based gestedas links between falconiformsand stri- on morphologicaland behavioraldifferences of giforms. this family from othersin the Falconiformes.In Relationships of the Falconiformes to other addition, similarities of cathartids to other ordershave alsobeen proposed,including the groupshave been noted, including the Cicon- orders Pelecaniformes, Ciconiiformes and Psit- iidae (Garrod 1873, Beddard 1898, Ligon 1967, taciformes(reviewed in Sharpe 1891, Shufeldt Rea 1983), Pelecaniformes (Beddard 1898, Jollie 1909), Gruiformes (Shufeldt 1909), Cuculi- 1976), Procellariiformes (Jollie 1976), and Grui- formes and Columbiformes (Verheyen 1950, formes (Pycraft 1902). Friedmann (1950:6)stat- reviewed in Jollie 1977). The AOU (1983) Check- ed that the Cathartidaewere a primitive group list places the Falconiformesbetween Anseri- not differentiatedfrom the "primitive stockfrom formes and Galliformes, whereas Sibley and which the Ciconiiformes, Pelecaniformes and Ahlquist (1990) position the order (with Ca- Procellariformeshave been developed." thartidae removed) as sister taxon to a group Hypothesesof a falconiform-strigiformrela- includingthe Podicipedidae,Sulidae, Phalacro- tionship have been advancedat various times, coracidae, and Phaethontidae. basedon similaritiesof palatal and myological Syringeal morphology had been used in the characters(reviewed in Sharpe 1891, Cracraft classificationof the major subdivisionsof the 1981, McKitrick 1991). Pandioninae (Sharpe Passeriformes at the end of the nineteenth cen- 1891, Pycraft 1902) and Falconidae (Beddard tury (Ames 1971). Within the last 20 years, sy- October1994] FalconiformMonophyly 789 ringeal data have again becomeimportant in cussedin the character descriptions(Appendix 2). the systematicsof oscinesand suboscines(e.g. Multistate characters were coded as unordered if states were alternative variations of a character. Ames 1971, Warner 1972, Lanyon 1984, Prum 1990, 1992), but have not strongly influenced I used outgroup information to polarize characters (Maddison et al. 1984).However, the relationshipsof the systematicsof other orders.There havebeen other orders to the Falconiformes are unclear, and the no detailed reports on falconiform syringeal choiceof an appropriateoutgroup is not readily ap- anatomysince Beddard (1903), and no system- parent. Species from four orders of birds were in- atic analysisof that anatomy. cluded in the analysis.A comprehensivesubset of I examined patternsof variation in syringeal generain the Ciconiiformesand Strigiformeswas ex- morphologywithin the Falconiformesto assess amined becausethere are phylogenetichypotheses of the usefulnessof the syrinx for systematicsof relationshipsof theseorders to the Falconiformes.In nonpasserines(i.e. whether there are phylo- addition, species within the Pelecaniformeswere genetically informative syringeal characters) added becauseseveral authors suggesteda relationship of this order to the Falconiformes(Beddard 1898, and to answer two primary systematic ques- Shufeldt 1909, Friedmann 1950, Jollie 1976). Because tions: (1) Is the order monophyletic?(2) What monophyly of the Falconiformescould not be as- are the relationshipsof the majorclades within sumed,species from theseother orderswere not treat- the order? ed as outgroupsin the analysis,nor was there a con- straint on monophyly imposed in the analysis (Maddisonet al. 1984).Species within the Galliformes MATERIALS AND METHODS were used to root the cladogram.I used PAUP 3.0s (Swofford 1991)to derive the most-parsimoniousres- Specimens.--Iexamined syringesfrom collectionsat the American Museum of Natural History (AMNH), olution of the data.The sizeof this dataset precluded the use of exact algorithms for resolving the data; the National Museum of Natural History (USNM), therefore,the heuristicalgorithm wasused. However, the Royal Ontario Museum (ROM), the University of this option does not guarantee optimality and may KansasMuseum of Natural History (KUMNH), the Museum of Vertebrate Zoology of the University of identify a solution that is only locally optimal. To increasethe probabilityof finding solutionsthat were Californiaat Berkeley(MVZ), and the LouisianaState globallyoptimal, analyses were repeatedvarying both University Museum of Natural Science(LSUMNS), the branch-swappingand taxa-additionoptions. someof which I dissectedfrom fresh or alcohol-pre- Three indices were used to assessthe congruence served specimens.These were cleared and double- of the charactershypothesized as synapomorphies stainedto distinguishcartilaginous and ossifiedtissue (Farris 1989):(1) consistencyindex, which is the min- (Cannell 1988).Observations were made using a Wild M5A dissectingmicroscope, and drawingsmade with imum amountof changeof a characterdivided by the amount observedon the tree; (2) rescaledconsistency a camera lucida. Drawings were scanned into a Mac- intosh computerand final illustrations prepared us- index, which is a linear rescalingof the consistency index sothat valuesvary from 0 to 1; and (3) retention ing Aldus Freehand 2.0. index, which is the proportion of original characters I analyzed 124falconiform syringes and 66 syringes remaining as synapomorphies.Consensus methods from purportedoutgroups (Appendix 1). Three of the were used to summarize information from the set of five cathartid genera and all falconid genera were most-parsimonioustrees. I used strict-consensustrees, included. Within the Accipitridae, genera were cho- which include groups found in each of the most- sento representeach of the previouslyproposed sub- groups;these totaled 60% of the currentlyrecognized parsimonious cladograms,and majority-rule trees, genera.In general,sampling within the ingroup was which include groupsfound in a definedproportion of cladograms.Consensus trees must be interpreted constrainedby the availability of specimens.Two or more individuals from 27 specieswere analyzed to with care as they may not be parsimoniousrecon- structionsof the original data (Swofford 1992). Nev- assessvariation at the intraspecificlevel. Analysis.--Variationin morphology was codedus- ertheless,consensus trees remain an efficientway for highlighting congruentclades, and the charactersand ing both binary and multistate characters.Multistate characters were ordered if either of two criteria was taxa causing incongruence. satisfied.Similarity of derivedstates was the primary criterion used (Patterson 1982). Thus, transformation serieswere proposedif adjacentderived stateswere RESULTS similar, and eachsucceeding state was a modification of the previous state (i.e. the derived statesformed a Syringealmorphology.--The main components nestedset of synapomorphies).Transformation series of a typical accipitridsyrinx (i.e. supporting also were proposed using ontogenetic information elements, membranes, and muscles) are illus- (character7). Justificationsused for ordering are dis- tratedin Figure2. Definitionsof syringealstruc- 790 CAROLES. GmFHTHS [Auk, VoL 111

p al

Fig. 2. Accipitridaesyrinx (Broad-wingedHawk, Buteoplatypterus, AMNH 20008).Left-dorsal view and right-ventralview. Abbreviations (numbers following refer to charactersin Appendix2): (a) A elements(1.2); (al) A1 elements (3, 23); (ac) complete double A elements (5); (bl) B1 elements(34.4, 36); (c) accessory cartilaginousstructure (44, 45.2);(ce) cartilaginous extension of A1 and A2 (12); (im) internalmembrane; (p) pessulus(22.4); (t) tympanum(20, 21.124.2, 29.3); (m) M. tracheolateralis.See text for definitionsof structural elements.In all illustrations,scale bar is 1 mm, stippling indicatescartilaginous tissue, and gray shading indicates ossified tissue. turesfollow Ames(1971 ) and include four types tures to the tracheo-bronchialjunction. There of supporting elements:A and B ringlike ele- are no homologiesthat canbe postulatedusing ments,the pessulus,and accessorycartilaginous traditional names. For example, the external structures. Ames (1971) used three criteria for membrane in falconid genera is located be- defining A and B elements:composition, cross- tween the second and third, third and fourth, sectionalshape, and orientation of concavity.A or fourth and fifth bronchialrings. When these elements are ossified and flattened in cross sec- rings are recognizedas A and B elements,how- tion, occurring on the trachea as single rings ever, this membraneis alwaysbetween A1 and but sometimesextending onto the bronchi as B1,a synapomorphyfor the family. Definitions paired double rings. They may be complete of rings as A and B elementshave been used in (forming a closedring) or incomplete. In ad- systematicstudies of oscines and suboscines dition, they may be fusedpartially or complete- (Ames 1971, Lanyon 1984, Prum 1990, 1992, ly near the tracheo-bronchialjunction, forming 1993)and, in limited detail,to a broadrange of a drum or tympanum.B elementsare generally orders (Cannell 1986). My analysis is the first cartilaginousand D-shapedin crosssection, oc- application of these definitions to detailed curring as paired rings on the bronchi. These structures in orders other than Passeriformes. may be completerings or may have an opening Ames' (1971) criteria for defining A and B on the medial surface of each bronchus. The elements are sufficient for most of the families pessulus,a cartilaginousor ossifiedbar, is lo- used in this analysis.A1 and B1 can be differ- cated on the midsagittal plane between the entiated by cross-sectionalshape and compo- bronchi.The dorsaland ventral endsof the pes- sition in the Cathartidae, Ciconiidae, Ardeidae, sulusmay be free or mayfuse to A or Belements. Falconidae, and Strigiformes. However, be- Finally, accessorycartilaginous structures occur causethe first B elementsin severalAccipitridae on the craniadedge of the internal membranes. speciesare highly ossified,these criteria alone The definitions of A and B elements differ couldnot alwaysdifferentiate A and B elements. from traditional terminology in which ringed I used an additional criterion, the distinctive structuresare tracheal or bronchial rings (King shape of the B1 element, for the accipitridsin 1989)based on the relative positionof the struc- this analysis.The first B element is wider me- October1994] FalconiformMonophyly 791 dially than other A and B elements, with specimen,laterally on the trachea,ending cra- narrower ends. This was corroboratedby the nial to the junction. These muscleshave also congruenceof muscleinsertion; the M. tracheo- been describedin Cathartes(Maynard 1897)and lateralis always inserted on B1 when B1 was are probably the M. tracheolateralis,but this defined using these criteria. diagnosismust be confirmed in intact speci- In additionto structuralelements, the syrinx mens. is composedof two kinds of syringeal mem- Intraspecificvariation in morphology.--Assess- branes. The internal membranes are located on ment of intraspecificvariation revealed several the medial surface of the bronchi between the charactersthat were polymorphic in species dorsal and ventral ends of incompleteA and B within the Falconidaeand Accipitridaeand were elements. These are considered to be the sound- not used in this analysis.The number of A el- producing structures(Gaunt and Gaunt 1985) ementsfused ventrally in the tympanumvaried and occur in all speciesexamined except the in Buteoplatypterus (5, 6, or 7), in Accipiterstriatus ciconiids. The external membranes are on the (5 or 6), and in Falcosparverius (3 or 4). The size lateral walls of the bronchi, usually betweenA1 of the ventral, ossifiedpatch covering the fused and one or two of the first four B elements. tympanum rings varied within Buteoand Leu- Although the locationof an externalmembrane copternisspecies. Finally, the B1 element, al- is a synapomorphyfor the Falconidae,the ex- though normally cartilaginous,was partially to istence of external membranes is variable with- totally ossified within several species, the in most of the other families examined and may amountof ossificationvarying intraspecifically. be correlated with structural modifications in I found no sexualdimorphism in the species elementsbordering the membranes.Therefore, for which this information was available. Gen- this characterwas of limited usein my analysis. eral patterns in ontogenetic variation were There are also two classesof syringeal mus- found. Ossificationof the tympanum and A el- cles. Intrinsic musclesoriginate and insert on ements increasedin adults compared to juve- syringealelements and are important in the sys- niles in Tyto,Buteo, Falco, Pandion, Accipiter and tematics of the Passeriformes. These do not exist Cathartes.Fusion of the elementsin the tym- in falconiforms.The two extrinsicmuscles orig- panum also increasedslightly in adults com- inate outsidethe syrinx. The M. sternotrachealis pared to juveniles of Pandion,Tyto and Falco. originates on the internal surface of the cora- Both of these patterns are consistentwith ob- cold or costalprocess of the sternumand inserts servationsin the Passeriformes(Ames 1971). An on several A elements on the trachea. The M. additional pattern was found in the Catharti- tracheolateralisoriginates on the lateral surface dae.In nestlingCathartes, single A elementsim- of the cricoid cartilage of the larynx and de- mediatelycranial to the tracheo-bronchialjunc- scendslaterally down the trachea.In many taxa tion are complete rings. In adults, these are it is contiguouswith or underlies the M. ster- incomplete,with gaps dorsally (character7). notrachealis, and the insertion of this muscle Phylogeneticanalysis of Falconiformes.--Varia- can be somewhat obscured as a result. Because tion in syringeal morphology was coded ini- muscle fibers are damaged in cleared speci- tially for 103 taxa as 49 characters,of which 33 mens, the insertions of these muscles were not were binary and 16 were multistate (Appendix always apparent in specimensI examined and 2). Redundant species (those with identical were of limited use phylogenetically.Where character states)were merged, resulting in a visible, the M. tracheolateralis inserts: on A1, final matrix of 88 taxa (Table 1). Analysis of B1 and possiblyB2 in the Ardeidae; on B1 in these data resulted in more than 5,000 most- the accipitrids(including Pandion and Sagittar- parsimonious cladograms,which is not unex- ius) and in the Strigiformes;and on the lateral pected for a matrix with more taxa than char- membrane in the falconids. This muscle has been acters.The shortesttrees found had a length of claimed to be lost in Struthio,Casuarius, Dromaius, 195, consistencyindex of 0.401, rescaled con- Rhea,Apteryx, the Cathartidae,Ciconiidae, most sistencyindex of 0.358, and retention index of Pelecaniformes, and some Galliformes (Bed- 0.865. dard 1898,King 1989).Within the ratites,how- The strict-consensustree (Fig. 3) indicates ever, the muscle exists but ends where the M. supportfor the monophyly of the order Fal- sternotrachealisbegins (King 1989). Similarly, coniformes. Within the order, Cathartidae is I observedmuscle fibers in a Coragypssyringeal basal to a clade of two sister taxa, the Falconidae 792 CAROLES. GRIFFITHS [Auk, Vol. 111

TABLE1. Distributionsin 88 taxa of statesof 49 syringeal charactersused in phylogeneticanalysis. See Appendix 2 for descriptions.

Character

1 2 3 4 Taxon 1234567890123456789012345678901234567890123456789

Accipitddae Accipitercooperii 1010100000012011001114120000400003010012000120101 A. gentilis 1010100000010011001114120000400002010010000120011 A. virgatus 1010100000011011001114120000400002010001000120010 A. striatus 1010100000011011001114120000400002010010000120001 Aegypius 1010100000012011001112120000200003010000000120000 Aquila 1010100000010011001112110000300003010001000110000 Aviceda 1010100000002011001123110000300003010012000120000 Busarellus 2010100000012011001124130000400004010012000120000 Butastur 1010100000010011001113021000400001010001000120000 Buteo albicaudatus 1010100000010011001114120000300004010000000110000 B. buteo 0010100000010011001112120000300004010000000110000 B. jamaicensis 1010100000011011001114120000300004010000000120000 B. magnirostris 1010100000010011001112120000300003010000000120000 Buteogallus 1010100000010011001112110000300004010002000110000 Circaetus 1010100000011011001102110000300003010002010110000 Circus 1010100000012011001114120000400002010002000120010 Elanoides 1010100000011011001112120000300003010001000120000 Elanus 2010100000000011001122110000100003010000000110000 Gampsonyx 2010100000000011001122130000400001000000000110000 Geranospiza 2010100000010011001123120000300002010011000120100 Gypaetus 1010100000010011001112120000300003010000010121000 Haliaeetus 1010100000010011001112110000300003010000000110000 Haliastur 1010100000011011001112121000300003010001000120000 Harpagus 1010100000010011001112120000300005010001000120000 Henicopernis 1010100000010011001123120000300005010000000120000 H eterospiz ias 1010100000010011001112120000300003010002000120000 Hieraaetus 1010100000011011001113120000300003010001000120000 Ichthyophaga 1010100000012011001112120000300003010001000120010 Ictinia 1010100000011011001112120000300003010002000120100 Kaupifalco 1010100000011011001123120000400001010002000120000 Leptodon 2010100000010011001123130000300002000000000120000 Leucopterniskuhli 1010100000010011001113120000300003010000000120000 L. albicollis 1010100000010011001114120000300004010001000120000 Melierax 1010100000010011001112120000300005010000000120001 Milvus 1010100000011011001112121000300003010001000120010 Necrosyrtes 1010100000010011001112120000200003010000000111000 Neophron 1010100000000011001112121000200003010000010111000 Parabuteo 1010100000011011001114120000300004010001000120000 Pithecophaga 1010100000010011001112120000300003010000010110010 Rostrhamus 1010100000011011001122120000400004010001000120001 Spilornis 1010100000011011001112120000300003010002000120000 Spizaetus 1010100000011011001112121000300003010002010120000 Terathopius 1010100000011011001112110000300003010002000120000 Pandion 1010100000013011001115010000300001000002100120000 Sagittariidae Sagittarius 2010100000000011001122130000020000110002010120000 Falconidae Daptrius americanus 2010100000000011001121000100030010004100100130000 D. ater 2010100000000011001121000100030010004100100140000 Falcoberigora 2010100001000011001121000202020010003300100130000 F. columbarius 2010100000000011001121000201020010003301100130000 F. mexicanus 2010100000000011001121000201020010003200100130000 F. rufigularis 2010100000000011001121000201020010003300100130000 F. sparverius 2010100001000011001121000201020010003200100130000 H erpetotheres 2010100000000011001121000101020010003000100000000 October 1994] FalconiformMonophyly 793

TABLE 1. Continued.

Character

1 2 3 4 Taxon 1234567890123456789012345678901234567890123456789

Micrasturgilvicollis 20101000000001110011210001100100100 01100100130000 M. semitorquatus 20101000000001110011210002100100100 01100100140000 Microhierax 20101000010000110011210003020200100 02100100130000 Polihieraxinsignis 20101000000000110011210001100200100 03200100140000 P. semitorquatus 20101000000000110011210003010200100 02100100130000 Polyborus 20101000000000110011210001000300100 04100100130000 Spiziapteryx 20101000000000110011210001020200100 03000100130000 Cathartidae Cathartes 20101121000000110110000000000000000 00000000000000 Coragyps 20101111000000110010000000000000000 00000000000000 Vultur 20101121000000110100000000000000000 00000000000000

Ardeidae A rdea 20110000000000111000000000000000000 10000001000000 Bubulcus 20100000000000111000000000000000000 00000011000000 Butorides 20100000000000111000000000000000100 00000001000000 Egretta 10100000000000111000000000000000000 00000001000000 Ixobrychus 20110000000000111000000000000000000 00000001000000 Nycticorax 20100000000000111000000000000000000 00000001000000 Ciconiidae Mycteria 21000000000000100000000000000010000 00000000000000 Tytonidae Phodilus 20100000100000210100000000000000020 00000000000000 Tyto 20101000100000110100000000000000020 00000000130000 Strigidae Aegolius 20110000101000110100000000000001020 00000000000000 Asio otus 20110000101000210100000000000001030 00000000000000 A. stygius 20110000101000110100000000000001030 00000000000000 Bubovirginianus 20111000101000210100000000001001030 00000000000000 Ciccaba huhula 20110000101000210100000000000001020 00000000000000 C. virgata 10110000101000210100000000000001020 00000000000000 Ketupaketupu 00110000101000210100000000001001030 00000000000000 Ninox connivens 20110000100000110100000000000001030 00000000000000 N. odiosa 20111000101000110100000000001001030 00000000130000 N. jacquinoti 20110000101000210100000000001001030 00000000000000 Nyctea 10110000100000210100000000001001030 00000000000000 Otus asio 20111000101000210100000000000001030 00000000000000 O. watsonii 20111000101000110100000000000001030 00000000000000

Sulidae Sula 20100000000000110000000000001000000 00000001000000

Pelecanidae Pelecanus 00100000000000000000000000000000000 00000100000000 Galliformes 00100000000000110000000000000000000 00000000000000

and the Accipitridae(including Sagittariusand 19). Four characters unite the Falconidae and Pandion).Two derived charactersunite the three the Accipitridae as sister taxa. Speciesin these cladesin the order. All specieshave complete, families have a tympanum composedof A ele- double A elements on the bronchi; these also ments fused ventrally and dorsally, to which occurin severalstrigiform genera(character 5). the pessulusis attached(characters 20, 22). In Speciesalso have an ossifiedpessulus, which is addition, these specieshave sheetsof cartilag- connecteddorsally and ventrally to A elements; inous tissue forming a border cranially on the the dorsal attachment is lost in Vultur (character internal membranes(character 44). The tym- 794 C•ROLES. GmFRTHS [Auk, Vol. 111

Ardeidae . Sula 2, 3, 32 Mycteria 33, (s) Strigidae Tyro 9,18 Phodilus Haliastur Elanoides Ictinia 39,49 Accipiterstriatus A. gent#is Circus Accipitercooperii ! Busarellus 13.2,39 Aviceda Leucopternisalbicollis Parabuteo Spilornis Buteojarnaicensis Terath.opius Aegyplus Pandion Haliaeetus Ichthyophaga Gypaetus Necrosyrtes Neophron Pithecophaga Butastur Kaupifalco Accipitervirgatus Melierax Milvus Rostrharnus Henl•opernis Buteo albicaudatus Buteo buteo 36 Circaetus Hieraaetus Buteogallus Geranospiza Heterospizias Leptodon 22.2, 23, 24.3 Leucopterniskuhli Spizaetus Buteomagnirostris 2021.2, Harpagus Aquila Sagittarius Elanus Garnpsonyx

-19 Falconidae . ß Vultur ß Cathartes

41 Coragyps Pelecanus Galliformes

Fig.3. Summaryof strict-consensustree derived from the set of 5,000most-parsimonious trees found from analysisof syringealdata. Synapomorphies supporting nodes are numbered;descriptions of charactersin Appendix 2. October1994] FalconiformMonophyly 795

Fig.4. Falconidaesyrinx (Brown Falcon, Falco berigora, AMNH 193358).Left-dorsal view and right-ventral view. Abbreviations:(a) A elements(1.1); (al) A1 elements(3); (ac)complete double A elements(5); (bl) B1 elements(33, 37); (be) fusion of elementends (38.3); (c) accessory cartilaginous structure (44, 45.3); (e) external membrane(41); (im) internalmembrane; (p) p.essulus (15, 16); (r) ossifiedridge (9); (t) tympanum(20, 21.2, 26.2, 28.2, 30.2).

panum is ossifiedtotally in falconidspecies and ventrally to the tympanum,a lateral membrane in the mostbasal accipitrid species, but an al- located between A1 and B1 on which the M. ternativepattern (lack of ossificationdorsally) tracheolateralisinserts, B1 elements evenly existsin mostof the other accipitrids(character wider than other B elements, and fusion of the 21). ends of incompleteA1 and B1 elements(char- Thereis strongsupport for the monophyly acters26, 28, 33, 37, 41). A phylogenyof the of the Falconidae.The falconidsyrinx (Fig. 4) Falconidaeis presented in a separatepaper (Grif- is characterizedby a completelyossified tym- fiths 1994). panum,an ossifiedpessulus fused dorsally and The three genera of cathartidsincluded in

Fig. 5. Cathartidaesyrinx (Turkey Vulture, Cathartes aura, AMNH 20933).Left-dorsal view and right- ventralview. Abbreviations: (a)complete double A elements(6, 8);(al) A1 elements;(as) incomplete single A element(7); (bl) B1elements; (im) internalmembrane; (p) pessulus(16, 18). 796 CAROL•S. GPdl•I•ITHS [Auk, VoL 111

Haliastur 991. Milvus Elanoides Ictinia

98 Terathopius ß Pandion Circaetus Spizaetus 96•HeterospiziasSpilømis I-'-- Accipiters tria tus 93 86,_•--L• A. gentills 8_• • A. virgatus II Circus 96-Lj Accipitercooperii 83I_[--- Busarellus -- 98 L--- Aviceda 93 90 Parabuteo 88 ButeoLeucopternisjamaicensis albicollis Rostrhamus 93 911"ButasturKaupifalco Hieraaetus Ichthyophaga Aegypius 94 96I---- Melierax -- Harpagus Henicopernis 991 LeptodonGeranospiza 98 Leucoptemis kuhli Buteo magnirostris •_•_• Gypaetus Necrosyrtes Neophron Pithecophaga

96]"• Buteo buteoalbicaudatus 99 Haliaeetus 99• Buteogallus -- Aquila Elanus Sagittarius Gampsonyx Fig. 6. An 80%majority-rule consensus tree of generain Accipitridae.Clades illustrated are supportedin at least 80% of the most-parsimonioustrees. Numbers indicate percent support; nodes without numbersare supportedin 100%of most-parsimonioustrees. October1994] FalconifortnMonophyly 797 my studyare united by three unambiguoussyn~ not supportedby syringealdata. The serpent apomorphies.Coragyps is the sistertaxon to Ca- eagles (Terathopius,Spilornis, and Circaetus)are thartes(Fig. 5) and Vultur. Cathartid speciesare in a clade with four other speciesand are not commonlyconsidered as lacking a syrinx (Li- sister taxa. The five genera of sub-buteonines gon 1967, Rea 1983, Gill 1990). Although the included in this analysisare widely separated. cathartid syrinx does lack some modifications However, two taxa, Parabuteo and one of the occurring in other falconiform syringes,it has Leucopternisspecies, form a monophyleticgroup internal membranes,an ossifiedpessulus, char- with Buteojarnaicensis. acteristicossification of A elements,and prob- Thereare no syringealcharacters uniting the ably (as noted above) the M. tracheolateralis. four Old World vultures included in this anal- The unique modificationscharacterizing ca- ysis.Aegypius is separatedfrom a clade of three thartidsyringes include dorsal gaps in the most genera (Gypaetus,Necrosyrtes, and Neophron), caudal single A elements, and a minimum of which are united by one unambiguoussyna- four complete, medially thin, double A ele- pomorphy (character47). Similarly, there are ments on the bronchi (characters 6, 7, 8). no derived characterssupporting the mono- Phylogenyof Accipitridae.--Syringeal data phyly of the two largest genera, Accipiterand groupSagittarius and Pandionwith the accipitrid Buteo.Three of the Accipiterspecies are clustered genera;this cladeis supportedby three derived together, while the fourth, A. cooperiLis in a characters (characters 22.2, 23, 24.3). In these sister clade with Circus, Busarellus and Aviceda. genera, A1 is not fused ventrally to the tym- There are alsono characterssupporting the sis- panum, although fusion and ossificationof the ter taxa relationship of Heterospiziasand Buteo- tympanum is more extensive ventrally than gallus,two speciesthat have recentlybeen syn- dorsally.In addition, the dorsalattachment of onymized (Areadon 1982). the pessulusto the tympanumforms character- Outgrouprelationships.--I used outgroupsin istic patterns different from the falconid pat- this study to polarize characters.Sampling of tern. generawithin the four ordersof outgroupswas Limited sampling of genera and the lack of not comprehensiveenough, nor were enough phylogenetically informative variation of the ordersincluded to derive a phylogenyat the syrinx preclude my deriving a fully resolved ordinal level. Findingsof my study, therefore, phylogeny for the Accipitridaeand imposecon- should be interpreted with care. Nevertheless, straints on the inferences that can be derived as a result of the more extensive examination from this analysis.Nonetheless, there are some of genera within the Ciconiiformes and Stri- findings of interest, illustrated in the majority- giformes, some conclusionscan be drawn. Sy- rule tree (Fig. 6), and someresults that indicate ringeal characterssupport the monophyly of the need for further research. each of the two families of Ciconiiformes in- Syringealdata supportthe polyphyly of the cluded in the analysisbut do not support the kites.The 17 generacurrently considered to be monophylyof the order. Three derived char- kites have been grouped based on their pred- acters cluster the three genera of Ciconiidae atory and social behavior and have been con- (characters3, 4, 47; Fig. 7), while one derived sideredprimitive to the other accipitrids(Brown character(character 20) unites the six genera of and Areadon 1968),but the monophyly of this the Ardeidae examined. group has been questioned(Areadon and Bull Syringeal data also support the monophyly 1988).There is supportfor the closerelationship of the Strigiformes.Of the two currently rec- of the Old World railvine kites, Haliastur and ognizedfamilies, Tytonidae and Strigidae,there Milvus, which are sister taxa in 99% of the trees are derived charactersuniting only one, the (Fig. 6). Two kites, Elanusand Garnpsonyx,cur- Strigidae (characters6, 12, 48, 52). Tyto and rently grouped togetherwith Chelictiniain the Phodilusare in unresolved positions relative to Elaninae (Brown and Areadon 1968) are not sis- the Strigidae. ter taxa,but are among the mostbasal accipitrid genera. DISCUSSION Butasturand Kaupifalcoare thought to be closely related (Areadon and Bull 1988), and Systematicsand the syrinx.--Syringeal data, in theyare sister taxa in thisanalysis. Several other particular the variation in intrinsic muscula- speciesgroupings within the Accipitridaeare ture, have been important in the systematicsof 798 ½^ROLES. GmF•rHs [Auk,Vol. 111

-- b2

Fig. 7. Ciconiidaesyrinx (White Stork, Ciconiaciconia, AMNH 1936).Left-dorsal view and right-ventral view. Abbreviations:(al) A1 element;(a2) A2 element(2); (bl) B1 elements;(b2) B2 elements(31); (p) pessulus. the oscines and suboscines, but these data have charactersto resolve relationshipswithin the beenvirtually ignoredin the systematicsof most Accipitridae,a family of approximately60 gen- other orders of birds. This may have been the era and more than 200 species,there is sufficient result of a perception that the structural ele- variation to producea robustphylogeny for a mentsof the syrinx offer minimal phylogenetic family with 10 genera (Griffiths 1994). information,and that only the intrinsicmuscles Phylogeneticrelationships.--Estimates of phy- are informative. One goal of my researchwas logeneticrelationships of the five generawith- to assessthe usefulnessof syringealdata in re- in the Cathartidaeare ambiguous,but there is solving phylogenetic relationshipsfor orders consensusthat the smaller cathartids (Cathartes other than the Passeriformes.This analysishas and Coragyps)are sistertaxa to the othergenera demonstrated that there is sufficient variation (Fisher1944, Emslie 1988).Syringeal data sup- in the morphologyof syringealstructural ele- port the basalposition of Coragyps,whereas Ca- ments to derive credible phylogenetichypoth- thartes and Vultur are sister taxa. A more com- eses for the Falconiformes. plete taxonomicsampling is neededto resolve There are, however, a limited number of the phylogeny of the cathartids. structurescomprising the syrinx and a limit to Syringeal data resolve relationships in the the variation. Thus, the presenceof major struc- falconids(Griffiths 1994),but not the Accipit- tural elements (e.g. presenceof a tympanum, ridae. One surprising result is the inclusion of presenceand location of lateral membranes,or Sagittariusand Pandionwithin the Accipitridae. different pessulusmorphologies) provides syn- Sagittariusis divergent in externalmorphology, apomorphiesdefining ordersor familiesof birds. behavior,and osteologyfrom the other accip- Minor structuralvariants provide characters that itrid genera, and has been consideredcloser to define genera and resolve some generic rela- the Gruiformesthan the Falconiformes(Pycraft tionshipswithin families.These include changes ! 902,Mayr and Amadon! 95!). Thisdivergence in the shapeof B1 or A! elements,the shapeof hasbeen the justificationfor elevatingSagittar- the ends of incomplete elements,and variations iusto a monotypicfamily separatefrom the oth- in the degree of ossificationor fusion of the er clades within the order. Pandion has received tympanum. Although there are not enough similar taxonomic treatment. The distinctive October1994] FalconiformMonophyly 799

treatment of these two specieshas not been angle above the antitrochanterin the Ciconi- supportedby my phylogeneticanalysis. Thus, idae and Cathartidae, and a 45ø angle in the the characterssuggesting the distinctivenessof Accipitridae. However, my observationsindi- these two speciesmay be autapomorphiesand cate that the curvature in the Cathartidae is in- may suggesthigh ratesof phenotypicevolution termediate between the other two families. Us- in these speciesrelative to other accipitrids. ing this characterto unite the cathartidswith Monophylyof Falconiformes.--Thecomposi- either of the other two groups requires an ex- tion of the Falconiformeshas been a point of tremely subjectivedecision. Similarly, the lo- contentionsince the order was defined. At pres- cation of the anterior iliac crest is intermediate ent, the mostproblematic taxon is the family of in the Cathartidaecompared to the other two New World vultures (Cathartidae). There is a families,as is the crossingof the coracoidalsul- growing consensusthat this family is the sister ci, the shape of the ilioischiatic fenestra, and taxon to the Ciconiidae(Emslie 1988, Holdaway the angle at which the bicipital crestjoins the 1991),with three studiesoffered as support:Li- humeral shaft. In addition, several of Ligon's gon (1967), Rea (1983), and Sibley and Ahlquist characters are composites that oversimplify (1990). variation or ignore variation in the accipitrids Ligon (1967) and Rea (1983) each reviewed a (e.g. the cathartidsand ciconiidshave a stocky range of charactersfor taxain the Ciconiiformes or stoutand sigmoidalhumeral shaft). Within and Falconiformes, and each concluded that Ci- the accipitrids, the shaft is "often slender"; it coniidae and Cathartidae were sister taxa. How- appearedto be stockyin my observationof Hi- ever, these studies were produced before cla- eraaetus. distic methodology was in general use in Rea (1983) presentedlists that are diagnoses ornithologicalanalyses, and the data in these of the Ciconiiformes(including the Catharti- studies were not analyzed phylogenetically. dae) and major groupswithin that order. His Each study simply lists the taxa and the char- choiceof charactershas similar problemsto Li- acter statesdiagnosing the taxa. gon's. For example, Rea listed charactersunit- There are additional problemswith their con- ing Ciconiidae and Cathartidae, which should clusions because of the limited number of taxa be absentin Accipitridae,but are presentin that sampled.Ligon listed49 osteologicalcharacters family. These include the presenceof M. am- and examined three genera within the Cathar- biens(George and Berger1966, McKitrick 1991), tidae, three within the Accipitridae, and six the presence of full spread-wing postures in within the Ciconiidae. Of these, 27 cluster Ci- sunning (Simmons 1986), and the absenceof coniidae with Cathartidae, and only 6 cluster the accessoryM. femorocaudal(George and Ber- Accipitridae with Cathartidae. I examined skel- ger 1966).Some of his charactersignore or over- etons of 10 genera (Ciconia,Leptotillus, Sarcor- simplify variation. Thus, a "variably degener- hamphus,Vultur, Hieraaetus, Buteo, Aquila, Accip- ate" syrinx unites Ciconiidae and Cathartidae. iter, and Falco) and researched additional However, the syrinx is not one organ but a se- anatomicalstudies. At best,only 8 of Ligon's 27 ries of modificationsof structures,and my anal- characterssupport grouping the Ciconiidaeand ysis indicates that the variation in syringeal Cathartidae. Several characters he used to unite morphologycannot be describedin one char- ciconiids and cathartids, or to separatecathar- acter. When fully described,the variations do tids and accipitrids, occur in accipitrids or ca- not unite Ciconiidae and Cathartidae. thartids that he did not sample. Ligon listed Finally, Rea (1983) listed charactersuniting basipterygoidprocesses as not present in the Ciconiidae and Cathartidae, which are, presum- Accipitridae.However, they existin severaltaxa ably, unique to those two families. However, (Shufeldt 1909, pets. obs.),and his illustration these also can be found in other orders of birds. on page 5 showsthese processes in Necrosyrtes. Thus, urohydrosis(urination usedas a cooling He lists a prominent foramen on the humeral mechanism),listed as occurringonly in Cicon- shaft, and one pair of sternal manubrial fenes- iidae and Cathartidae, also occurs in the Sulidae trae as occurring in Accipitridae only. These (order Pelicaniformes; Carboneras 1992). The also occur in the Cathartidae. pattern of macrochromosomesshared by Cicon- Someof the describedcharacter states grade iidae and Cathartidae are, in fact, more closely into one another. The curvature of the pelvic sharedby the Cathartidae,Galliformes, Grui- girdle is describedby Ligon as having a slight formes,and Phoenicopteriformes(de Boer1975). 800 CmtOLES. GPd•m•HS [Auk, Vol. 111

M. pectoralis major is described as double in within the Falconiformes.In addition, syrin- storks and cathartids. However, it is also double geal data provide support for the monophyly in Gruidae, Procellariiformes, and Pelecani- of three major cladeswithin the Falconiformes: formes (George and Berger 1966). The most se- the Cathartidae, the Falconidae, and an Accip- rious problem in both studies is that, without itrinae-Sagittarius-Pandiongroup. a phylogeneticanalysis, none of the characters describedby Ligon and Rea canbe usedto dem- ACKNOWLEDGMENTS onstratea relationship between the Ciconiidae and Cathartidae;the charactersmay all be ple- This studywould not have been completedwithout siomorphicor convergent.Determining wheth- the guidanceand supportof G. Barrowcloughand R. er any of their dataare derivedcharacters shared F. Rockwell.I thank the following curatorsfor lend- by thesetwo familiesawaits an extensivesurvey ing me specimensfrom their collections;G. Barrow- of generawithin eachof thesetwo familiesand clough,R. Zusi, V. Remsen,A. Baker,and N. Johnson. other families within the two orders,and a phy- Discussionswith R. Prum and P. Cannell provided logenetic analysisof the resulting data. insightinto the useof the syrinxin systematics.Com- ments on earlier versions of this manuscript were Sibley and Ahlquist (1990) used DNA-DNA provided by C. Farquahr, E. Griffiths, J. Groth, M. hybridization data to generatephylogenies for Novacek, S. Rather, and P. Sweet. Final versions were all birds. Although widely cited, there are some improvedby reviews from J. Bates,J. Cracraft,F. Gill, problemswith the methodology,analysis, and S. Hackett,and D. Zusi. This researchwas supported results of these data (e.g. Barrowclough 1992, by grantsfrom the FrankM. ChapmanMemorial Fund Cracraft1992, Lanyon 1992,Mindell 1992).One of the AmericanMuseum of Natural History,a Chap- primary claim of these data is the sister-taxa man Pre-doctoralFellowship, and a City University relationship of the cathartidsand ciconiids.Sib- of New York DissertationImprovement Grant. ley and Ahlquist (1990) presentedtwo different hypothesesof cathartid relationships:a Fitch LITERATURE CITED tree (their fig. 338), which doesnot assumerate constancy,placed the cathartidswith the stri- AMADON, D. 1982. A revision of the sub-buteonine giforms as a sister clade to the other Falconi- hawks(Accipitridae, Aves). Am. Mus. Novit. 2741. formes; and an UPGMA analysis, which does AMADON, D., AND J. BULL. 1988. Hawks and owls of the world: A distributional and taxonomic list. assumerate constancy,placed the cathartidsas Proc. West. Found. Vert. Zool. 3. sistertaxa to the ciconiids.I reanalyzedthe data AMERICAN ORNITHOLOGISTS' UNION. 1983. Check-list in figure 338 of Sibley and Ahlquist (1990) using of North American birds, 6th ed. Am. Ornithol. the samemethod they mentioned, the Fitch op- Union, Washington, D.C. tion of Phylip (Felsenstein1990). My reanalysis AMES,P.L. 1971. The morphology of the syrinx in produced a tree different from the one they passerinebirds. Bull. PeabodyMus. Nat. Hist. 37. reported, one that is congruentwith the results BARROwCLOUGH,G. F. 1992. Biochemical studies of of my syringealanalysis; the cathartidsare sister the higher level systematicsof birds. Bull. Br. taxa to the falconids and accipitrids (see also Ornithol. Club (Centenary Suppl.) 112A:39-52. Mindell 1992). Sibley and Ahlquist (1990) dis- BEDDARD,F.E. 1898. The structure and classification of birds. Longmans, Green and Co., London. missedtheir Fitch tree by concluding that dif- BEDDARD,F. E. 1903. On the modifications of struc- ferent ages at first breeding cause problems. ture in the syrinx of the Accipitres,with remarks However, the additional assumptions,data, and upon other points in the anatomy of that group. corrections used to produce the UPGMA tree Proc. Zool. Soc. Lond. 1903:157-163. are not presented,and there is no way to assess BROWN,L., AND D. AMADON. 1968. Eagles,hawks the rigor of that hypothesis. In summary, the and falcons of the world. Wellfleet Press, Secau- tree derived from my syringealanalysis fits the cus, New Jersey. DNA-DNA hybridization data better than the CANNELL,P. F. 1986. Syringeal complexity and the tree reported by Sibley and Ahlquist (1990). ordinal systematicsof "higher birds." Ph.D. dis- Although the notion that the cathartidsshould sertation,City Univ. New York, New York. be removed from the Falconiformes is becom- CANNELL,P. F. 1988. Techniquesfor the study of avian syringes.Wilson Bull. 10:289-293. ing acceptable(Emslie 1988,Snyder and Snyder C•d•BON•,•S,C. 1992. Order Pelicaniformes,family 1991), the data and analysisoffered in support Sulidae. Page 314 in Handbook of the birds of of this notion are ambiguousat best.However, the world, vol. I (J. del Hoyo, A. Elliott, and J. my phylogenetic analysis of syringeal data Sargatal,Eds.). Lynx Ediciones,Barcelona. strongly supports inclusion of the cathartids CRACRAFr,J. 1981. Toward a phylogenetic classifi- October1994] FalconiformMonophyly 801

cation of the recent birds of the world (classAves). and some other species.C. J. Maynard, Massa- Auk 98:681-714. chusetts. CRACRAI•r,J. 1992. [Review of] Phylogenyand clas- MAYR, E., AND D. AMADON. 1951. A classificationof sificationof birds:A study in molecular evolution Recent birds. Am. Mus. Novit. 1496. by C. G. Sibleyand J. E. Ahlquist. Mol. Biol. Evol. MCKITRICK,M.C. 1991. Phylogeneticanalysis of avi- 9:182-186. an hind limb musculature. Misc. Publ. Mus. Zool. DEBOER, L. E. M. 1975. Karyologicalheterogeneity Univ. Mich. 179. in the Falconiformes(Aves). Experientia 31:1138- MINDELL,D. M. 1992. [Review of] Phylogeny and 1 !39. classificationof birds: A study in molecular evo- EMSI,IE, S. D. 1988. The fossil history and phyloge- lution by C. G. Sibley and J. E. Ahlquist. Syst. netic relationships of condors (Ciconiiformes: Biol. 41:126-135. Vulturidae) in the New World. J. Vertebr. Pa- PA•rm•SON,C. 1982. Morphological charactersand leontol. 8:212-228. hornology.Pages 21-74 in Problemsof phylo- FARRIS,J. S. 1989. The retention index and the res- genetic reconstruction (K. A. Joysey and A. E. caled consistencyindex. Cladistics 5:417-421. Friday, Eds.).Academic Press, New York. FELSENSTEIN,J. 1990. PHYLIP (phylogeny inference PRUM,R. O. 1990. A test of the monophyly of the package),version 3.2. Dep. Genetics,Univ. Wash- manakins(Pipridae) and of the cotingas(Cotin- ington, Seattle. gidae)based on morphology.Occ. Pap. Mus. Zool. FISHER,H. 1944. The skulls of the cathartid vultures. Univ. Mich. 723:1-44. Condor 46:272-296. PRUM,R. O. 1992. Syringealmorphology, phylog- FRmDM^NN, H. 1950. The birds of North and Middle eny, and evolution of the Neotropical manakins America, part XI. U.S. Natl. Mus. Bull. 50. (Aves: Pipridae). Am. Mus. Novit. 3043. GAP,ROD, A.J. 1873. Part I. On certain musclesin the PRUM,R. O. 1993. Phylogeny, biGgeography,and thigh of birds and their value in classification. evolution of the broadbills (Eurylaimidae) and Proc. Zool. Soc. Lond. 1873:626-644. asities(Philepittidae) basedon morphology.Auk GAUNT,A. S.,AND S. L. GAVNT. 1985. Syringealstruc- ! 10:304-324. ture and arian phonation. Curr. Ornithol. 2:213- PyCRAI•r,W.P. 1902. Contributionsto the osteology 245. of birds. Part V. Falconiformes. Proc. Zool. Soc. GEORGE,J. C., ANDA. J. BERGER.1966. Avian royol- Lond. 1902:277-320. ogy. AcademicPress, New York. REA, A. 1983. Cathartid affinities: A brief overview. GII,I., F. B. 1990. Ornithology. W. H. Freemanand Pages26-56 in Vulture biology and management Co., New York. (S. R. Wilbur and J. A. Jackson,Eds.). Univ. Cal- GRIFFITHS,C.S. 1994. Syringealmorphology and the ifornia Press,Berkeley. phylogenyof the Falconidae.Condor 96:!27-140. SHARPE,R. B. 1891. A review of recent attempts to HOLDAWAY,R.N. 1991. Systematicsand paleobiol- classifybirds. Taylor and Francis,London. ogy of Haast'sEagle (Harpagornismoorei Haast, SHUFELDT,R. W. 1909. Osteologyof birds. Bull. N. 1872).Ph.D. dissertation,Univ. Canterbury,New Y. State Mus. 130:1-381. Zealand. SIBLEY,C., AND J. AHLQUIST.1990. Phylogeny and JOLLIE,M.T. 1976. A contribution to the morphology classification of birds of the world. Yale Univ. and phylogeny of the Falconiformes,part 1. Evol. Press, New Haven. Theory 1:285-298. SIMMONS,K. E. L. 1986. The sunning behaviour in JOLI.IE, M.T. 1977. A contribution to the morphology birds. Bristol Ornithol. Club, Bristol, United and phylogeny of the Falconiformes,part 2-3. Kingdom. Evol. Theory 2:115-300. SNYDER, N. F. R., AND H. A. SNYDER. 1991. Birds of KING,A. $. 1989. Functionalanatomy of the syrinx. prey: Natural history and conservationof North Pages105-192 in Form and function in birds, vol. American raptors.Voyageur Press,Inc., Stillwa- 4 (A. S. King and J. McLelland, Eds.). Academic ter. Press, New York. STORER,R.W. 1971. Classificationof birds. Pages1- LANYON,S. M. 1992. [Review of] Phylogeny and 19 in Arian biology, vol. ! (D. S. Farner and J. classificationof birds:A studyin molecularevo- King, Eds.).Academic Press, New York. lution by C. G. Sibley and J. E. Ahlquist. Condor STRESEMANN,E., AND D. AM•DON. 1979. Falconi- 94:304-307. formes. Pages271-424 in Checklist of the birds LANYON,W.E. 1984. A phylogenyof the kingbirds of the world, vol. 1, 2nd ed. (E. Mayr and G. W. and their allies. Am. Mus. Novit. No. 2797. Cottrell, Eds.).Harvard Univ. Press,Cambridge. LIGON,J.D. 1967. Relationshipsof the cathartidvul- SWOFI•ORD,D. L. 1991. Phylogeneticanalysis using tures.Occas. Pap. Mus. Zool. Univ. Mich. No. 651. parsimony(PAUP). Illinois Natural History Sur- MADDISON, W. P., M. J. DONOGHUE,AND D. R. MAD- vey, Urbana. DISON. 1984. Outgroup analysisand parsimony. SWOFFORD,D. L. 1992. When are phylogeny esti- Syst.Zool. 33:83-103. mates from molecular and morphological data MAYNARD,C.J. 1897. Vocal organsof talking birds incongruent? Pages 295-334 in Phylogenetic 802 C•ROLES. GRIFFITHS [Auk,Vol. 111

analysisof DNA sequences(M. M. Miyamotoand 193358. F. biarmicus, AMNH 15927. F. cenchroides, J. Cracraft, Eds.). Oxford Univ. Press, New York. AMNH 193394. F. columbarius, AMNH 19752, 14713. WARNER,R.W. 1972. The anatomy of the syrinx in F. femoralis,LSUMNS 123309.F. mexicanus,KUMNH passefinebirds. J. Zool. (Lond.) 168:381-399. 053827.F. peregrinus,AMNH 8499,19751. F. rufigularis, KUMNH 041874.F. sparverius,AMNH 8430 male, 8688 female, 8413 male, 15808, 15931, 16307, [CSG9210], APPENDIX 1 (UNS) AMNH [CSG 21, 1216 male, 1217 imm. female]. H erpetotherescachinnans, AMNH unnum.Micrastur gil- Syringealspecimens examined. Specimens cleared vicollis, LSUMNS 98021. M. semitorquatus,USNM and double-stainedunless designatedas unstained 507797. Microhieraxerythrogonys, AMNH 8623. Mil- (UNS). Abbreviations for institutions from which vagochimachima, LSUMNS 120427.M. chimango,USNM specimenswere borrowedare given in the Materials 346421. Phalcoboenusaustralis, USNM 511795, LSUMNS and Specimenssection. Uncataloged specimens iden- 120728.Polihierax semitorquatus, USNM 615218. P. in- tified by a collector'snumber in brackets. signis,AMNH 8627. Polyborusplancus, AMNH 9094. ACCIPITRIDAE: Accipiterstriatus, AMNH 18761, Spiziapteryxcircumcinctus, LSUMNS 8 Sep 1990. 18762,8686, 8482,15938 imm. female, [CSG9212, 9215], CATHARTIDAE: Coragypsatratus, AMNH 19607, 1 Dec 1985 imm. female, (UNS) AMNH unnum. 1985 (UNS) [PRS 245]. Cathartesaura, AMNH 20933, un- male,[CSG 9213]. A. gentilis,AMNH 17 Dec 1984male, hum. Dec 1985, [PFC443], nestling. C. melambrotus, 11 Apr 1991imm. male.A. virgatus,AMNH 8030.A. LSUMNS 114336. C. burrovianus,USNM 227269. Vultur cooperii,AMNH 20007, 20623, [CSG 16, 9217, 9218, gryphus,AMNH 8498. 9264 imm. female]. Aegypiustracheliotus, KUMNH ARDEIDAE: Ardea herodias, AMNH 8933. Bubulcus 81668. Aquila audax, USNM 289389. A. chrysaetos, ibis, AMNH 8624. Butorides striatus, AMNH 20736. LSUMNS 126432. Aviceda subcristata,AMNH unnum. Egrettacaerulea, AMNH [PFC 427 imm. female]. Ixob- 1950. Busarellusnigricollis, LSUMNS 120424. Butastur rychussinensis, AMNH 8621. Nycticoraxnycticorax, indicus,AMNH 8497. Buteoalbicaudatus, AMNH 8683. AMNH 8625, 20335, (UNS) AMNH 8432. B. buteo,USNM 541690.B. jamaicensis,AMNH 18764, CICONIIDAE: Ciconiaciconia, AMNH unnum. 1936. 20546, unnum. 1985. B. magnirostris,ROM 104270.B. C. nigra,AMNH 6377.Ephippiorhyncus asiaticus, USNM platypterus,AMNH 18763, 8687, 20008, [CSG 9211], 510447(incomplete). Mycteria americana, AMNH 8513, (UNS) AMNH 21464.B. regalis,AMNH 19629.Buteo- (UNS) AMNH 9038, 9062, 9063, [MYC 85003, 85004, gallus urubitinga,LSU 114340. Circus approximans, 85006-85009]. AMNH 4-24. C. macrourus,USNM 615215.C. cyaneus, TYTONIDAE: Tyto alba,AMNH 14715, 8680, 8682, USNM 226415.Elanoides forficatus, AMNH [ROP270]. 20624, [CSG 9216]. T. tenebricosa,AMNH 7495. Phodilus Elanusleucurus, KUMNH 56804. Gampsonyxswainsonii, badius, AMNH 6419. AMNH 8529.Geranospiza caerulescens, LSUMNS 120423. STRIGIDAE: Aegoliusacadicus, AMNH 8489, [CSG Gypaetusbarbatus, AMNH 6398. Haliaeetusleucoceph- 9214].Asio otus, AMNH 8312.A. stygius,AMNH 7466. alus, KUMNH 46189, ROM 132599. Haliastur indus, A. fiammeus,AMNH 8684. Bubobubo, AMNH 7450. B. AMNH 8496. Harpagusbidentatus, LSUMNS 114345. shelleyi,AMNH 8414.B. virginianus,AMNH 16092,[SC Henicopernislongicauda, USNM 615210. Heterospizias 957 imm.]. Ciccabahuhula, AMNH [SC407]. C. virgata, meridionalis,AMNH unnum. Hieraaetusmorphnoides, (UNS) AMNH 7408. Ketupaketupu, BM A1981. Glau- AMNH unnum.Ichthyophaga nana, AMNH 8399.Ictinia cidiumbrasilianum, AMNH [SC302, 410, 268].G. gnoma, plumbea,AMNH [ROP271].I. mississippiensis,KUMNH AMNH 7404.Ninox jacquinoti, AMNH 7422.N. odiosa, 049239.Kaupifalco monogrammicus, USNM 615217.Lep- AMNH 7423. N. connivens,AMNH 7442. N. philippen- todoncayanensis, LSUMNS 120426. Leucopternisalbi- sis, AMNH 8490. N. scutulata,AMNH 8615. Nyctea coilis,AMIqH 8492,[ROP377]. L. kuhli,LSUMNS 114338. scandiaca,AMNH 8836. Otus asio,AMNH 8310, 20625. Melieraxca norus, USNM 615216.Milvus migrans, USNM O. watsoniœAMNH 8685.O. nudipes,AMNH 7438.O. 615213.Necrosyrtes monachus, USNM 34631.Neophron guatemalae,AMNH 7437.Pulsatrix perspicillata, AMNH percnopterus,USNM 615217. Parabuteounicinctus, 2784.Speotyto cunicularia, AMNH 8679,7447. Strix var- AMNH 19590.Pithecophaga jefferyi, AMNH 6396.Ros- ia, AMNH 7439. trhamus sociabilis,USNM 615212, AMNH [CSG 232, PHALACROCORACIDAE: Phalacrocorax auritus, 711]. Spilornischeela, AMNH 8616. Spizaetusornatus, (UNS) AMNH unnum. LSUMNS 3053.Terathopius ecaudatus, AMNH unnum. SULIDAE: Sula bassanus, AMNH 8618, 8846. Sula PANDIONINAE: Pandion haliaetus, AMNH 8488 nebouxi,(UNS) AMNH 8618. imm. male, 18808 female, [PFC445 female], USNM PELECANIDAE: Pelecanus roseus, (UNS) AMNH 615209. 8619. SAGITTARIIDAE:Sagittarius serpentarius, YPM 3721, CRACIDAE: Crax alector,AMNH 15006, (UNS) [PFC MVZ 4611. 412]. FALCONIDAE: Daptriusamericanus, AMNH 8667, PHASIANIDAE: Tetraoparvirostris, (UNS) AMNH [ROP266].D. ater, KU068951.Falco berigora, AMNH 14100. October1994] FalconiformMonophyly 803

APPENDIX 2 9. IncompleteA1 elementswider laterally, thicker and moreossified than other double A elements.--(1)Yes. In Descriptionsof 49 syringealcharacters used in anal- Strigiformes.(0) No. ysis. Derived statesare describedfirst. Characters7, 10. Dorsalends of incompleteA1 elementsconnected 26, 28, 38, 40 are multistate, ordered characters;jus- mediallyforming ridge of ossifiedtissue.--(1) In several tification for ordering follows descriptions.Charac- Falcospecies and in Microhierax.(0) Not present. ters I, 13, 15, 21, 22, 24, 29, 30, 34, 37, and 45 are 11. Ventralends of incompleteA1 elementsextend onto multistate unordered characters. Distribution of char- internalmembrane forming amorphous, ovoid accessory acter states shown in Table 1. Characters illustrated cartilaginousstructures.--(1) In strigid genera.(0) Not in Figures 2, 4, 5, and 7. present. 12. Ventralends of incompleteA1 and A2 elements A elements extendonto cranial surface of internalmembrane.--(1) In accipitrid genera. (0) Not present. 1. Ossificationof A elementscranial to tracheo-bronchial 13. Modificationsof caudaledges of dorsalends of in- junction.--(1)Completely ossified in all generain Fal- completeA1 elements.--(1)Slight pointed cartilaginous conidae and Cathartidae, and in most genera in Stri- extensionof ends. (2) Large cartilaginousextension giformes,Ardeidae, and in severalaccipitrids. (2) Os- bordersedge of internalmembrane. (3)Ends fused siftedventrally and laterally,but cartilaginousdorsally to ends of B2 elementsforming rings in Pandion.(0) in most accipitrid genera. (0) No ossification.Ele- A1 ends unmodified or single element. ments cartilaginousin Pelecanus,the two speciesof 14. Dorsalends of incompleteA1 elementsfiattened and Galliformes,and in juveniles in Strigiformes,Acci- enlargedforming a paddleshape.--(1) In Micrasturspe- pitridae, Cathartidaeand Falconidae. cies. (0) Not present. 2. A elementsimmediately cranial to tracheo-bronchial junctionthinner than subsequent elements and incomplete Pessulus laterally.--(1) In the Ciconiidae. (0) Not present. A elementscomplete rings in lateral view. 15. Pessuluscomposition.--(1) Pessulus ossified. (2) 3. Incompletedouble A elementson bronchicaudal to Pessuluscartilaginous in several strigid genera. (0) tracheo-bronchialjunction.--(1)Yes. One or two present Pessulusnot presentin Pelecanus,Phalacrocorax, Pod- in speciesin all families examinedexcept Ciconiidae. iceps,Spheniscus, Struthio, Casuarius, Dromaius, or Ap- Gapsbetween ends of incompleteelements on medial teryx. walls of bronchi, forming lateral bordersof internal 16. Pessulusan extensionof A elements.--(1)Yes. (0) membranes. (0) No A elements on bronchi in ciconiid No. Pessulusnot presentin Pelecanus.In Ciconiidae, genera. pessulusan extensionof B elements,an autapomor- 4. More thanthree incomplete double A elements.--(1) phy for that family and not included in this analysis. At leastfour incompletedouble A elements;in several 17. Ossifiedridges at dorsaland ventralends of pes- generain the Ardeidae; in all generawithin the Stri- sulus.--(1) In Ardeidae. (0) Not present. gidae. (0) No. A4 either single element or complete 18. Dorsally,pessulus ends medially.--(1) In Strigi- double elements. dae, Vultur; Cathartespolymorphic for this character 5. Completedouble A elementson bronchicaudal to (see character 19). (0) No. tracheo-bronchialjunction.--(1) Yes. In all genera in 19. Dorsaland ventral ends of Pessulusextend caudally Cathartidae,Accipitridae and Falconidae;in several from A elements.--(1)Yes. In all specieswithin Fal- genera in Strigiformes.(0) Not present. conidaeand Accipitridae.In Coragyps,in some adult 6. More than three completedouble A elements.--(1) Cathartesand in juvenal Cathartes.(0) No. Yes.All cathartidgenera have at leastfour complete double A elements. (0) No. Tympanum 7. SingleA elementsimmediately cranial to tracheo- bronchialjunction incomplete, with gap in elementdor- 20. Fusionof A elementscranial to tracheo-bronchial sally.-(1) One or two A elementsincomplete with junction.--(1)In accipitridand falconidgenera and in small gaps between ends in Coragyps(2) More than Sagittarius,tympanum formed from lateral, ventral, threeA elementsincomplete with largegaps between and dorsal fusion of A elements. Patterns of fusion the ends of each element, in Cathartes and Vultur. and ossificationvary among families; describedin Unique to Cathartidae. Transformationfrom state 1 following characters.(0) No fusion of A elements. to 2 observedin ontogeny of Cathartes.(0) No. In all 21. Degreeof dorsal ossification of tympanum.--(1) Os- other families, single A elements complete when siftedmedially and laterally only in most accipitrid viewed dorsally. genera.(2) Ossifiedcompletely in all falconidgenera 8. Medial cartilaginoussection of completeA elements and severalaccipitrids. (0) Tympanum not present. narrowerthan lateral,ossified section.--(1) Yes. In Ca- 22. Dorsal pessulusattachment to tympanum.--(1) thartidae. (0) No. Narrow, more highly ossified medial strip extends 804 CAROLES. GRIFFITHS [Auk, Vol. 111 cranially connectingseveral A elements;in falconid B elements genera. (2) Ossifiednarrowly, ends at or just above tracheo-bronchialjunction; in some accipitrids and Sagittarius.(3) Ossifiedbroadly, ends at or just above 31. All B elementscomplete rings.--(1) In Ciconiidae. tracheo-bronchialjunction in ovoid- or diamond- (0) In other taxa, B elementswith medial gaps. shaped pattern; in some accipitrids. (4) Ossified 32. B1at obliqueangle transversely.--(!) In Strigidae. broadly, extendscranially connectingone or two sin- (0) In other taxa,B1 perpendicular to transverseplane. gle A elementsmedially; in someaccipitrids. (5) Os- 33. B1 evenly wider than other B elements,concave siftedbroadly, extends cranially and laterallyforming caudally.--(!) In all falconids;in Butorides.(0) B! not a cross-likepattern, in Pandion.(0) Tympanum not concavecaudally in any other genera;same width as present. other B elementsin all other taxa exceptaccipitrids (character 35). 23. A1 not fusedventrally to tympanum.--(1)In all accipitridsand Sagittarius.(0) A! fusedin the Falcon- 34. Modificationsof shapeof incompleteB1 elements.-- idae. In other taxa, there is no tympanum. (!) Wider at dorsal ends. (2) Slightly wider laterally, 24. Patternof partialdorsal fusion of A elements.--(!) with narrowed ends. (3) Small arc-shapedextension Slight fusionmedially along caudaland cranialmar- on cranial margin laterally. (4) Large arc-shapedex- gins of two elements.(2) Medial, triangular-shaped tension on cranial margin laterally. (5) Very wide cartilaginousplug fusesseveral elements. (3) Medial dorsally, with slight narrowing at ventral ends. In plug ossified,elements also fused somewhatalong accipitridsand some strigids. (0) Not present. margins.Derived unorderedstates describe accipitrid 35. B1, B2 and B3 concavecranially.--(1) In Sagittar- ius. (0) No. tympanum. (0) Total fusion in Falconidae;in other taxa, no fusion of elements. 36. B1 overlapsA1 laterally.--(!) In accipitrid gen- 25. More thanseven rings fused to dorsalcartilaginous era. (0) Membrane separatesA1 and B! in other taxa. plug.--(!) In five accipitrid genera. (0) Six or fewer 37. Modificationof shapeof dorsalends of B1 elements rings fusedin all other accipitridsand falconids.No fusingwith A1 elements.--(!)Ends very thick and wide, dorsal fusion in other families. ascendsharply in L-shapeto fuse with A! ends. (2) 26. Shapeof ossifiedand fused tympanum.--(!) Grad- Endsthin, ascendgradually to fuse with A1 ends. (3) uated, widens caudally.(2) Almost cylindrical. (3) Al- Knobbing of craniadedges; craniad extensionfuses most cylindrical, A1 flattened laterally. In the Fal- with A! ends. (4) Ends thick, rounded, ascendgrad- conidae. State 3 modification of state 2. (0) No ually to fusewith A1. Derived statesin falconidgen- systematicvariation in accipitrid tympanum shape. era. (0) B! elementscomplete in Ciconiidae;ends not In other taxa, no tympanum present. modified in other species. 27. Dorsalfusion of first two single A elementsmedially 38. Fusionof A1 andB ventralends.--(!) A! and B1 endsfused. (2) B2 endsalso fused. State 2 modification by ossifiedbar.--(!) Yes.In Micrastur.(0) Not present. of state 1. (3) B3 ends also fused. State 3 modification 28. Dorsalfusion of first three or fourA elementsalong their margins.--(!) Margins apparent along edgesof of state2. In falconidgenera. (0) Not present. eachring. (2) Marginssomewhat obliterated and only 39. Fusionof B1 andB2 dorsalends.--(!) In Accipiter light suturesapparent medially. Derived statesin fal- and three other accipitrid genera. (0) Not present. conidgenera except Micrastur. State 2 modificationof 40. Fusionof B ventralends forming ridge bordering internal membranes.--(!) B! and B2 ends fused. (2) B3 state 1; fusion increased.(0) No. Partial fusion in the ends fused also. State 2 modification of state !. (0) accipitrids(character 29), and in Micrastur(character 27). In other taxa, no dorsal fusion. Not present. 29. Patternof partial ventral fusion of tympanum.--(!) Slight roedialfusion of A elementsalong margins. (2) Membranes and muscles Triangular-shapedossified patch coversmedial fusion of A elements.(3) Irregular, small ovoid ossified 41. External membrane between A1 and B1 elements.-- patch coversroedial fusion. (4) Large ossifiedpatch (1) In all falconid genera;in Pandionwhich hasmem- coversfusion of A elements medially and laterally. brane between B! and B2 also. (0) Not present. In Accipitridae,Sula and some Strigiformes. (0) Fusion 42. External membranesbetween B2-4 elements.--(1) total in falconids,lacking in other taxa. In severalaccipitrids and Sagittarius.These have ex- 30. Patternof total ventralfusion of tympanum.--(!) ternal membranebetween B1 and B2, alsooccurring First three or four A elementsfused along margins. in many accipitrid generaand not usedas a character Spacesapparent between elements. (2) First three or becausegenerally small, with intraspecificand indi- four A elementsfused lightly, suturesapparent along vidual variation in its occurrence;may be an artifact margins.(3) At least five A elementsfused entirely of preservation.(0) Not present. alongmargins, sutures apparent only laterally.In fal- 43. M. tracheolateralisinserts laterally on A1.--(!) In conids. the Ardeidae and in Sula. (0) In Falconidae, M. tra- (0) Fusionpartial in accipitrids,lacking in other taxa. cheolateralisinserts on lateral membrane, in Accipit- October1994] FalconiformMonophyly 805 ridae and Strigiformes,inserts on B1. Not coded in 46. Borderossified.--(1) In three taxain Accipitridae. analysisbecause correlated with other characters.See (0) Not present. text for discussion of M. tracheolateralis in Galli- 47. Smallcartilaginous paddle-shaped accessory struc- formes, Cathartidae and Ciconiidae. turesextend onto internal membranes from dorsal A 1 ends.- (1) In severalaccipitrid species. (0) Not present. Accessorystructures 48. Smallcartilaginous peaks extend caudally onto internal membranesmedially.--(1) In several accipitrid 44. Cartilaginousborder located on cranialedge of in- species.(0) Not present. ternalmembrane, extending from dorsalto ventralends of 49. Internalmembranes almost parallel.--(1) In Accip- membrane.--(1)Present. (0) Not present. iter (0) No internal membranes in Ciconiidae. Internal 45. Shapeof cartilaginousborder.--(1) Narrow, thick- membranesat angle to each other when viewed dor- er dorsallythan ventrally. (2) Wide, thickerdorsally sally in all other species. than ventrally. (3) Wide and even. (4) Narrow and even. (0) Not present.