The Condor 96:127-140 Q The Cooper Ornithological Society 1994

SYRINGEAL MORPHOLOGY AND THE PHYLOGENY OF THE ’

CAROLES.GRIFFITHS Departmentof Ornithology,American Museum of NaturalHistory and Departmentef Biology, City Collegeof City Universityof New York, Central Park West at 79th St., New York, NY 10024

Abstract. Variation in syringealmorphology was studied to resolve the relationshipsof representativesof all of the recognized genera of , falconets, pygmy falcons, and caracarasin the family Falconidae. The phylogenyderived from thesedata establishesthree major cladeswithin the family: (1) the Polyborinae, containingDaptrius, Polyborus, and ,the four genera of caracaras;(2) the , consistingof the Falco, (pygmy falcons),Spiziapteryx and (falconets)and Herpetothe- res (Laughing ); and (3) the genus Micrastur(forest falcons) comprising the third, . Two genera, Daptriusand Polihierax,are found to be polyphyletic. The phy- logeny inferred from these syringealdata do not support the current division of the family into two subfamilies. Key words: Falconidae;phylogeny; systematics; syrinx; falcons; caracaras.

INTRODUCTION 1. The Polyborinae. This includes seven gen- Phylogenetic relationships form the basis for re- era: Daptrius, Milvago, Polyborus and Phalco- searchin comparative and evolutionary biology boenus(the caracaras),Micrastur (forest falcons), (Page1 and Harvey 1988, Gittleman and Luh Herpetotheres() and Spiziapter- 1992). Patterns drawn from cladogramsprovide yx (Spot-winged Falconet). the blueprints for understanding biodiversity, 2. The Falconinae. This includes three genera: ,behavior, and parasite-hostcospe- Falco, Polihierax (pygmy falcons) and Micro- ciation (Vane-Wright et al. 199 1, Mayden 1988, hierax (falconets). Page 1988, Coddington 1988) and are one of the Inclusion of the caracarasin the Polyborinae key ingredients for planning conservation strat- is not questioned (Sharpe 1874, Swann 1922, egies(Erwin 199 1, May 1990). For many orders Peters 1931). The number of named of , however, these patterns or hypotheses genera, however, has varied from two to four. are not available and the higher level systematics Three other genera (Spiziapteryx, Micrastur and of many avian families and orders remain un- Herpetotheres)may not belong in the Polybori- resolved. nae. Spiziapteryx had traditionally been associ- The Falconidae (falcons, caracarasand falcon- ated with the pygmy falcons and falconets but ets) is an example of a family whosephylogenetic was placed with the caracaras based on an as- relationships are in question. Resolution of this sessmentof osteologicalsimilarity (Olson 1976). phylogeny is particularly important since it is one Once thought to be related to rather than of nine families identified as threatened in falcons (Sharpe 1874, Swann 1922) Micrastur CITES appendix II (Norton et al. 1990). In ad- and Herpetotheres were later considered to be dition, nine falconid speciesare listed by the In- either one (Peters 1931) or, subsequently, two ternational Council for Bird Preservation (ICBP) (Friedmann 1950) separate subfamilies within as vulnerable, rare or endangered. the Falconidae. Cladistic analyses of syringeal morphology Composition of the Falconinae has also (Griffiths, in press.)and osteology(Becker 1987) changed. Polihierax, Spiziapteryx and Micro- support the of the family, but sys- hierax were originally placed with Falco (Sharpe tematic ambiguities exist at the intrafamilial lev- 1874, Swann 1922), then placed in a separate el. Current classification allocates the 10 genera subfamily, the Polihieracinae (Peters 193 1, in the family into two subfamilies (Amadon and Friedmann 1950). More recently, Microhierax Bull 1988). and Polihierax were reunited with Falco (Strese- mann and Amadon 1979). Cladistic analysesof the family using osteology ’ ’ Received 6 May 1993. Accepted 7 October 1993. (Becker 1987) and allozyme frequencies (Boyce

~271 128 CAROLE S. GRIFFITHS

A. Micrastur r FdCO

Falconets

Herpetotheres Peciiohierax

spiziapteryx Spiziap teryx

: FdCO Caracaras

Falcon&s Herpetotheres

r-- Micrastur FIGURE 1. Alternative phylogenetichypotheses for the Falconidae derived from (A) Allozyme data (Boyce 1989) and (B) Osteology(Becker 1987).

1989) produced two alternative hypotheses of malin and storedin alcohol at the American Mu- generic relationships (Fig. 1). Osteological data seum of Natural History (AMNH), the National placed Micrastur and Herpetotheres basal to the Museum of Natural History (USNM), and the other genera, whereas allozyme data supported Louisiana State University Museum of Natural the falconets as the basal group. Science (LSUMNS). These were cleared and I analyzed the variation in syringeal mor- double stained to distinguish cartilaginous and phology of the Falconidae to derive a phyloge- ossifiedtissue (Cannel1 1988). Additional cleared netic hypothesis for this family. Syringeal my- and stained specimens prepared by Dr. Peter ology had been important in the classification of Cannel1were also used;these included specimens the major subdivisions of the Passeriformes at borrowed from the University of Kansas Mu- the end of the 19th century (see Ames 1971 for seum of Natural History (KUMNH). Observa- a detailed review), but the lack of intrinsic mus- tions were made using a Wild M5A dissecting cles in other orders obviated general taxonomic microscope and drawings made with a camera use of the syrinx. Within the last 20 years, ap- lucida. plication of staining techniques to the syrinx has All 10 currently recognized genera within the made detailed observations of anatomy possible, family (Stresemann and Amadon 1979) and 10 and the use of syringeal data in systematicshas outgroup specieswere examined, a total of 44 intensified. However, this work was centered on specimens of 32 (Appendix I). Species the analysis of oscines and suboscines (Ames from the monotypic genera Spiziapteryx, Polyb- 1971, Warner 1972, Lanyon 1984, Prum 1990) orus and Herpetotheres and both speciesin each and “higher birds” (Cannel1 1986). There have of the genera Daptrius, Milvago and Polihierax been no previous analyses of falconid syringes. were included. Sampling of specieswithin the remaining polytypic genera was limited by the MATERIALS AND METHODS availability of alcohol preserved specimens(one of three speciesin Phalcoboenus, two of five in MATERIALS AND SPECIMENS Micrastur, and one of five in Microhierax). An Syringes were obtained by dissecting fresh spec- additional consideration limiting the number of imens and specimens originally preserved in for- speciesexamined within the genus Falco (nine FALCON PHYLOGENY 129 of 38) was the minimal variation in syringeal RESULTS morphology in these species. SYRINGEAL MORPHOLOGY Multiple individuals from six specieswere ex- amined to assessvariation at the intraspecific The main structural components of the falconid level. For the American (F&o sparver- syrinx are shown in Figure 2; Ames’ (197 1) def- ius), collection data were available to allow as- initions of syringeal components are used. These sessmentof both sexual and ontogenetic varia- are as follows: tion. (1) A elements-occur on the trachea as single rings but may extend onto the bronchi as paired ANALYSIS double rings. The rings may be complete or in- Variation in syringeal morphology was coded as complete medially and are generally ossified in both binary and multistate characters. The or- birds (Ames 1971, Cannel1 1986). In the Fal- dering of statesfor multistate characterswas hy- conidae, all genera have at least one incomplete pothesizedusing the similarity criterion and test- double and one complete double ring and all A ed by examining the relationshipsof the character elements are completely ossified. statesto each other in the resulting cladograms (2) B elements-occur on the bronchi and (Lipscomb 1992). generally are cartilaginous. These are paired rings Characters were polarized using outgroup in- that may be either complete or incomplete me- formation (Maddison et al. 1984). Multiple out- dially. B elements are all incomplete medially (C groups were used to ensure global parsimony, rings) in the Falconidae. that is, that the phylogenetic hypothesesare the (3) Tympanum-fused and ossified A ele- most parsimonious both within the Falconidae, ments occur near the trachea-bronchial junction. and among the Falconidae and its sister taxa In the Falconidae, from three to eight A elements (Maddison et al. 1984). are fused (Appendix II, Characters 2-7). The PAUP 3.0s computer program (Swofford (4) Pessulus-a dorso-ventrally oriented car- 199 1) was used to derive the most parsimonious tilaginous or ossifiedbar located in the mid-sag- resolution of the data. The size of the data set ittal plane of the trachea between the bronchi. It precluded exact search algorithms; therefore, a may be fused to other elements at the dorsal or heuristic algorithm was used. However, this does ventral or both ends. In the Falconidae, the pes- not guarantee optimality. To avoid finding a so- sulus is always ossified and fused both dorsally lution that is only locally optimal, analyseswere and ventrally to the tympanum. repeated varying both the branch swapping and (5) Membranes-a. The internal or medial taxa addition options. In addition, the effect of tympaniform membranes comprise the medial two different characteroptimizations was tested, surface of the bronchial tubes, usually close to ACCTRAN, which increases reversals, and the trachea-bronchial junction and supported at DELTRAN, which increasesparallelisms. the edges by the ends of the divided A and B Three indices were used to assessthe congru- elements. The membranes may be continuous ence of charactershypothesized as synapomor- from the left to the right bronchus or may be phies: (1) the consistency index, the minimum separated by the pessulus. These are generally number of character state changes a character considered to be the sound producing structures may show, divided by the number of changes (Gaunt and Gaunt 1985). b. The external or lat- observed on a particular tree, (2) the resealed eral tympaniform membranes are on the lateral consistencyindex, a linear resealing to allow the walls of the bronchi, usually between one or two consistency index to vary between 0 and 1, and of the first four B elements. In the Falconidae, (3) the retention index, the proportion of hy- there is a large external membrane between Al pothesized synapomorphies retained as homol- and Bl. ogies (Farris 1989). (6) Musculature-a. Intrinsic musclesare short Strict consensus trees, which only include muscles which both originate and insert on sy- groups found in all of the most parsimonious ringeal elements. There are no intrinsic muscles cladograms, were used to summarize the agree- within the Falconidae. b. Extrinsic muscles are ment in taxonomic relationships among the set longer muscles which originate away from the of most parsimonioustrees. Consensus trees must syrinx and insert on it. M. tracheolateralis orig- be interpreted carefully as they may not be par- inates on the lateral surface of the cricoid carti- simonious reconstructions of the original data. lage of the larynx and extends down the lateral 130 CAROLE S. GRIFFITHS

m

e

FIGURE 2. Syrinx of F&o berigoru (AMNH 193358). Top: left, dorsal view; right, ventral view. Bottom: lateral view. Abbreviations: a (A elements),bi (double B 1 element), c (cartilaginousborder on internal membrane), e (external membrane), f (fusion of Al and Bl elements), im (internal membrane), m (M. tracheolateralis),p (pessulus),t (tympanum). In all drawings: 1. stippling indicates cartilaginoustissue; 2. cross-hatchingindicates dense ossified tissue; 3. the M. tracheolateralisis illustrated on one side only. surfaces of the trachea, inserting in the syringeal region. In this family, the insertion is on the PHYLOGENETIC ANALYSIS external membrane. M. sternotrachealis origi- Variations in syringeal morphology were ex- nates on the internal surface of the coracoid or amined for 32 taxa; 10 of these represented hy- costal process of the sternum, or on the internal pothesized outgroups of the Falconidae (five fal- surface of one or more ribs. It inserts on the coniform species and five species from three other lateral or ventral surface of the trachea or on the orders of birds). After the initial character state tissues surrounding the trachea, and may be con- coding, redundant outgroup species (those with tinuous with, or overlap, the M. tracheolateralis. identical character states) were deleted, resulting FALCON PHYLOGENY 131

TABLE 1. Data matrix of 25 syringealmorphological charactersfor 25 Falconidae and outgroup species.

Characters Tam 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

Pelecanusroseus 0000000000010000000000000 Otus asio 0000000000000000000000000 Garnpsonyxswainsonii 1000000000000000000000100 Daptrius americanus 1001001100010000101020101 D. ater 1001001101000000101010100 Falco sparverius 1010010210000001011100110 F. rujigularis 1010010200001001021020110 F. biarmicus 1010010200000001021100110 F. mexicanus 1010010200000001011110110 F. femoralis 1010010200001001021020110 F. cenchroides 1010010210000001011020110 F. berigora 1020010210000001021020110 F. columbarius 1010010200000001021020110 F. peregrinus 1010010200000001021100110 Herpetotherescachinnans 1010010100000001001000100 Micrastur gilvicollis 1100100100100100001000101 M. semitorquatus 1100100200100100001000100 Microhierax erythrogonys 1020010310000010001000110 Milvago chimachima 1001001101000000101011110 M. chimango 1001001101000000101011110 Phalcoboenusaustralis 1001001101000000101011110 Polihierax semitorquatus 1010010300000010001020110 P. insignis 1100010100000001011020101 Polyborusplancus 1002001101010000101020101 Spiziapteryxcircumcinctus 1020010100000001001020110

in a data matrix containing 25 taxa, 22 falconid by this analysis is summarized in the strict con- speciesand three outgroup species. sensustree (Fig. 3); there are three polytomies The 25 charactersincluded in this analysiswere (discussed below) reflecting the conflicting to- coded first as 20 binary and five ordered mul- pologies in the 27 most parsimonious clado- tistate characters.The cladogramsresulting from grams. This tree illustrates the distribution of the analysis of this data matrix were examined derived charactersand the effectofdiffering char- to assessthe congruenceof the ordering of char- acter optimizations (differencesin character 10, acter states of the multistate characters.One of Fig. 3). the five was highly incongruent; this character was reexamined and then treated as unordered. WITHIN THE FALCONIDAE The final data matrix contained 20 binary, four The phylogeny derived from syringeal data does ordered multistate and one unordered multistate not support the monophyly of the two currently character (Appendix II, ordered characters3, 4, accepted Falconidae subfamilies. Rather, all trees 8, 18, unordered character 2 1). are congruent in their support of three clades: (1) Analysis of this data matrix (Table 1) resulted Micrastur, (2) the four caracara genera, and (3) in 27 most parsimonious cladogramsof 50 steps, a clade composedof Herpetotheres, Spiziapteryx, consistencyindex of 0.620, resealedconsistency Microhierax, Polihierax, and the Falco species. index of 0.525 and retention index of 0.843. Be- Four derived characters support the mono- cause the consistency index is negatively corre- phyly of the two species of Micrastur (Fig. 4); lated with the number of taxa, there is a maxi- three of theseare unambiguous synapomorphies. mum value expected for different numbers of The Micrastur tympanum has minimal fusion taxa. The CI for this analysis comparesfavorably compared to other genera in the family (dorsal with the generalresult expectedfor 25 taxa (0.483, fusion, character 2, CI 0.5; ventral fusion, char- Sanderson and Donoghue 1989). acter 5, CI 1.O). The ends of the Al elements are Congruence among the cladograms produced flattened and enlarged (character 11, CI 1.O). The 132 CAROLE S. GRIFFITHS

Otus asio Pelecanus roseus 1.0,23.0 I Gampsonyx swainsonii 25 Micrastur gilvicoilis

M. semitorquatus 2,5,11,14 8.2 cwI- Daptrius ater Milvago chimachima

Milvago chimango

Phalcoboenus australis Polyborus plancus Daptrius americanus

Polihierax insignis

Herpetotheres cachinnans

Spiziapteryx circumcinctus

Microhierax etythrogonys Polihierax semitorquatus

Falco peregrinus

Falco biarmicus I I 8.2 20,21.1 Falco sparverius Falco mexicanus

Falco rufigularis

Falco femoralis

Falco columbarius

Falco berigora

Falco cenchroides

FIGURE 3. Strict consensustree derived from the 27 most parsimoniouscladograms. There are three polyt- omies: 1. Milvago and Phalcoboenus. 2. The Falco speciesberigora, columbarius, cenchroides and two clades. 3. The Falco species sparverius, biarmicus, mexicanus, and peregrinus. Character support for each node is indicated: statesfor the five multistate characters(3, 4, 8, 18, 21) are shown as decimals following the number. Optimization of character 10 is ambiguous;in the alternative DELTRAN optimization, charactersstates marked with asterisksare eliminated, character states in parenthesesare acquired. The effect is to delay the transfor- mations and to eliminate reversals.

Bl elements are straight medially; Bl ends as- dorsal tympanum fusion is most extensive in the tend abruptly (character 14, CI 1.0) and fuse caracaras(characters 4 and 7, CI 1.O), in number totally with A 1 ends, forming an inflexible frame of elements fused and degree of fusion of each for the lateral membrane. element (Fig. 5). The Bl elements also have a Monophyly of the clade of six speciesof cara- characteristic shape: thick in circumference and carasalso has strongsupport (three unambiguous concave medially with ends that ascend gradu- synapomorphies,characters 4,7,17). Ventral and ally (character 17, CI 1.O). Fusion of Bl to Al FALCON PHYLOGENY 133

a

t

ai

P

im

bi

m

FIGURE 4. Syrinx of Micrustursemitorquatus (USNM 507797). Top: left, dorsal view; right, ventral view. Bottom: lateral view. Abbreviations: a (A elements),ai (double Al elements),bi (double Bl elements),e (external membrane), im (internal membrane), m (M. tracheolateralis),p (pessulus),t (tympanum). ends is not as strong as in Micrastur; a cartilag- synapomorphy unites the caracara and Falcon- inous bridge connecting the ends allows some inae clades (character 21, CI 0.33, Fig. 3). flexibility and movement. The third clade comprises the current sub- MONOPHYLY OF FALCONID GENERA family Falconinae (the falcons, pygmy falcons Syringeal data suggest that three genera are not and falconets), with the addition of Spiziapteryx monophyletic. Two of the genera,Polihierax (Fig. and Herpetotheres.Two derived charactersunite 6) and Daptrius are polyphyletic; the two species the clade: (1) the pattern of ventral fusion of the within each of these genera are not sister taxa. tympanum (character6, CI 1.O), and (2) the broad Daptrius americanus (Red-throated Caracara) is knobbed ends of the Bl element (character 16, more closely related to Polyborusplancus(Crest- CI 0.5). Within the clade, Spiziapteryx is sister ed Caracara), whereasDaptrius ater (Black Cara- to Falco and two of the falconet species. cara) is closer to the Milvago clade. Herpetotheresis sister taxon to the Falco-falcon- Similarly, Polihierax semitorquatus (African et clade, while Polihierax insignis(Asian Pygmy ) forms a clade with Microhierax Falcon) is basal. erythrogonus(Philippine Falconet), while P. in- All trees are also congruent in the resolution signis (Asian Pygmy Falcon) is sister taxon to of the interrelationship of thesethree clades.Mi- Herpetotheres,Spiziapteryx, Falco and the other crastur is supported as the basal clade while one falconet species. 134 CAROLE S. GRIFFITHS

r ’ , ,” P k /T

a m

t

ai

C e b

FIGURE 5. Syrinx of two caracaras.Top: Milvagochimachima (LSUMNS 120427). Bottom: Duptriusater (AMNH 10128). Left, dorsal view; right, ventral view. Abbreviations: a (A elements), ai (double Al elements), b (B elements), c (cartilaginousborder on internal membrane), e (external membrane), m (M. tracheolateralis), p. (pessulus),t (tympanum).

The monophyly of Milvago is also uncertain. species),but are unable to resolve the relation- In this analysis, Phalcoboenusaustralis occursin ships of these species.One clade of four species, a polytomy with the two Milvago species.This F. mexicanus ( Falcon), F. sparverius clade is supportedby two synapomorphies(char- (), F. peregrinus(Peregrine Fal- acters 22 and 24); there are no syringeal char- con) and F. biarmicus (), is united acters that distinguish any of these three species by two synapomorphies (characters20 and 21). (no autapomorphies). Relationships of the other five Falco species,F. These data support the monophyly of the Fal- cenchroides(Australian Kestrel), F. columbarius co speciesexamined for this study (nine of 38 (), F. berigora (Brown ), F. rujigu- FALCON PHYLOGENY 135

t

ai P c e

bi

FIGURE 6. Syringesof the twoPolihierax species. Top: P. semitorquatus(USNM 6 15218). Bottom: P. insignis (AMNH 8627). Left, dorsalview; right, ventral view. Abbreviations:a (A elements),ai (doubleAl elements), bi (doubleBl elements),c (cartilaginousborder on internal membrane),e (externalmembrane), p (pessulus),t (tympanum). laris ( Falcon), and F. femoralis (Aplomado not generally be able to resolve generic relation- Falcon) are ambiguous. In all trees, however, F. ships. Systematistsmust choosecharacters with rujigularis and F. femoralis are sister taxa; both rates of consistent with the taxonomic have A 1 elements that are medially straight and level of the group in question. However, rates of not concave (character 13). change of charactersmay vary among taxa. For example, osteologicalcharacters have been used DISCUSSION successfully in genus-level analyses in Anseri- SYRINGEAL VARIATION formes (Livezey 1986), but in the Cathartidae In order to resolve phylogeny, the patterns of they were useful only at the familial and ordinal variation of characters must be informative at level (Emslie 1988). This study examined the the level of the question asked. Thus, characters levels of usefulnessof syringeal data for the Fal- varying among individuals within a specieswill conidae. 136 CAROLE S. GRIFFITHS

Intraspecific variation was examined in nine monious trees found in an analysis (Hauser and specimens of F. sparverius (American Kestrel). Presch 199 1). There have been, however, no de- There was variation among adults only in the finitive studies about the effect of these assump- number of rings fused in the tympanum. Six tions on phylogenetic analyses and results that specimens (including both males and females) have been reported are contradictory. For ex- had three rings fused, whereastwo (one male and ample, ordering characters may result in phy- one female) had four. There was additional vari- logenies with greater resolution (Mickevich and ation between adult and juvenile specimens. In Weller 1990, Slowinski 1993) or may have no all adult falconid specimensexamined, the A rings effect on resolution (Hauser and Presch 199 1). were completely ossified. However, the juvenile Ordering characters may or may not constrain kestrel had cartilaginous medial sections, both the number of most parsimonious trees found in dorsally and ventrally. Similar ontogenetic vari- an analysis; the effectsmay, in fact, be data-set ation in A element ossificationhas been observed specific (Hauser and Presch 199 1). in passerines(Ames 197 1) as well as in the Ac- The decision to order a multistate character cipitridae and the Tytonidae (Griffiths, in press). should be made on a characterby characterbasis. Neither of these two morphological variations If there is evidence for relationships of the states was used in this analysis. in a multistate character, then to treat that char- Syringeal morphology is relatively conserva- acter as unordered is discarding information tive within genera and there may not be enough (Lipscomb 1992, Maddison and Maddison 1992). variation within speciosegenera to resolve re- In this study, similarity of stateswas the criterion lationships. Thus, among the nine speciesof Fal- used to hypothesize character state order. For co examined, there was slight variation in the characters 3, 4 and 18 (increases in amount of fusion of the tympanum, in the appearance of a ossification or fusion of various elements), the ridge over the dorsal attachment of the pessulus ordering patterns were also observed in onto- to the tympanum, and in the method of insertion genetic sequencesand are in agreement with gen- of the M. tracheolateralis. While this variation eral developmental processes.In addition, sim- may be useful in identifying major cladesor some ilar patterns were observed in syringes from small groups of sister taxa, it is not enough to juveniles and adults in specieswithin the Strigi- infer the phylogeny of 38 species. formes, Ciconiiformes, Cathartidae, Falconidae and , and through descriptionsin the MULTISTATE CHARACTERS literature for the Passeriformes(Ames 197 1). Although multistate characters are used exten- sively in phylogenetic analysis, there is a lack of MONOPHYLY OF GENERA consensusas to the best method for describing There were no discrete charactersdistinguishing the transformation between the different char- the two Milvago speciesfrom Phalcoboenus. The acter states.The most commonly used transfor- speciescomposition of caracara genera and the mations are ordered and unordered characters, relationships among these genera have always both ofwhich entail assumptionsabout character been ambiguous. For example, Sharpe (1874) evolution. Unordered character states assume placed Daptrius, Phalcoboenus and Milvago in that any state can transform directly into any one genus, Ibycter. Milvago was separated first other, while ordering states implies a (usually (Swann 1922) and then all four were recognized linear) relationship among the character states as separate genera (Peters 1931). Brown and (Swofford and Olsen 1990). Amadon (1968) proposeda close relationship of Currently, the use of ordered charactersis be- Polyborus, Phalcoboenus and Milvago, and Vuil- ing questioned. There may be three possiblerea- leumier (1970) recommended that the three be sonsfor the trend towards unordered characters: placed in one genus. This analysis suggeststhe (1) the prevalence of molecular phylogenetic need for additional study of these genera. studies which use unordered characters, (2) the Daptrius was found to be polyphyletic. The conviction that ordering entails a risk that the two Daptrius species have traditionally been wrong order may be chosen (Slowinski 1993), united by color and by tarsal and toe and (3) the possible constraining effect that or- characters(Friedmann 1950). Brown and Ama- dering may have on the number of most parsi- don (1968) however, noted that and be- FALCON PHYLOGENY 137 havioral differencessuggest that thesetwo should geal hypothesis; in both, Micrastur is basal and be separatedgenerically and that the genus name Spiziapteryx is related to Falco and the falconets, Ibycter be used again for D. americanus. Syrin- rather than to the caracaras. Only the position geal data, by demonstrating that D. americanus of Herpetotheresand Polihierax insignis differs and Polyborus plancus are sister taxa, support between the two. The topology derived from that conclusion. allozyme data (Fig. 1A, Boyce 1989) differs from The two species of Polihierax are not sister the syringeal and osteologicalphylogenies. How- taxa. P. semitorquatusis in the falconet clade, ever, if the allozyme hypothesis were rooted at sister taxon to Falco. P. insignis, on the other Micrastur rather than at the falconets,there would hand, is basal to Falco and the other falconet be substantial congruenceamong all three. species.Morphological differences(tail length and This study hasdemonstrated that syringealdata shape,and 2nd primary length) between the two can be used to resolve phylogenetic questions at Polihierax specieshave also been recognizedpre- the generic and family levels of the Falconidae. viously, leading to P. insignis being placed in a The value of syringeal morphology for system- monotypic genus, Neohierax (Swann 1922). atics has been known for at least one hundred Brown and Amadon (1968) proposed that ge- years (Beddard 1898). Avian systematists,how- neric status be accorded to these species;this is ever, have not used syringeal characters to de- also supported by syringeal data. velop phylogenies for orders of birds other than the Passeriformes,and avian biologists, in gen- PHYLOGENETIC RELATIONSHIPS OF eral, have ignored the syrinx. In 1960, Andrew THE FALCONIDAE Berger observed, “There are few anatomical Previous designations of falconid subfamilies structures throughout the families of birds that have been based on combinations of characters, need study as badly as the syrinx” (King 1989, many of which may be plesiomorphic. Cladistic page 106). By reinforcing the value of syringeal analysis of syringeal data (Fig. 3) results in a morphology as a systematic tool, this analysis division of the family into three comprehensive should encourage systematists to explore little clades;(1) the genusMicrastur basal to the other known morphological structures as sources of two clades, (2) the Polyborinae (including only information for phylogenetic reconstruction. the four caracaragenera), and (3) the Falconinae (consisting of Falco, the pygmy falcons and fal- ACKNOWLEDGMENTS conets, and Herpetotheres). It does not support I am indebted to Drs. G. Barrowcloughand R. Rock- the following currently accepted(Stresemann and well for their insight, support and advice throughout Amadon 1979) designations: the courseof this study. 1 thank Drs. R. Prum and P. Cannel1for early guidance on syringeal morphology, (1) The division of the Falconidae into two and the following curators for lending me specimens subfamilies, in their collections:Dr. G. Barrowclough,Dr. R. Zusi, (2) The position of three genera (Spiziapteryx, and Dr. V. Remsen. Helpful comments on earlier ver- Herpetotheresand Micrastur) in the Polyborinae, sionsof this manuscript and much-needed moral sup- (3) The clade of pygmy falcons and falconets port were provided by E. Griffiths, J. Groth, S. Hackett, S. Ratner, and P. Sweet. Final versionswere improved (based on similarity of tarsal and nostril char- by reviews from D. Amadon, J. Cracraft, C. Farquahr, acters, Friedmann 1950). F. Gill, L. Marcus, M. Novacek, R. Zusi and two anon- Syringeal data also indicate that two genera ymousreviewers. This researchwas supportedby grants are not monophyletic, suggestingthat more de- from the Frank M. Chapman Memorial Fund of the American Museum of Natural History, a Frank M. tailed investigations of speciesrelationships in Chapman Pre-doctoral Fellowship, and a City Uni- this family must be performed using all extant versity of New York DissertationImprovement Grant. taxa. Finally, as a raptor systematist,I would like to ac- Congruence of these conclusions with the two knowledge the debt we all owe to Dr. D. Amadon, previous cladistic analyses of the family (Fig. 1) whose work provides the basis for researchon raptor biology and systematics. cannot be assessedwith rigor since neither of these examined all the speciesanalyzed in this LITERATURE CITED paper. Nevertheless, some comparisons can be AMADON,D., AND J. BULL. 1988. Hawks and owls made. Becker’s (1987) hypothesis based on os- of the world: a distributional and taxonomic list. teology (Fig. 1B) agreesgenerally with the syrin- Proc. West. Found. Vert. Zool. 3. 138 CAROLE S. GRIFFITHS

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APPENDIX I. List of specimensexamined. Abbre- TYMPANUM viations for the institutions are given in the Materials (1) Presenceof a tympanum or tracheal drum. and Specimenssection. [0] There is no tracheal drum. [l] The first A elements are ossified totally and Falconidae more extensively than more craniad A elements. The Daptrius americanus AMNH 8667, unnum first A elementsare fusedmedially and may be partially 24/l/90 or completely fused to each other along their margins, Daptrius ater KUMNH 041874, dorsally,laterally and ventrally forming a trachealdrum AMNH 10128 to which the pessulusis attached. The tracheal drum Falco berigora AMNH 193358 is alwaysformed from elements Al and A2, which are F. biarmicus AMNH 15927 double elements.A3, which is usuallysingle, and single F. cenchroides AMNH 193394 elements from A4 to A8 may also be fused to the F. columbarius AMNH 19752, 14713 tympanum (see below). F. femoralis LSUMNS 123309 The following 8 charactersdescribe variations in the F. mexicanus KUMNH 053827 tympanum within the Falconidae. The tympanum is F. peregrinus AMNH 8499, 19751 either primitively: (a) absent(within the speciesof Gal- F. rufigularis KUMNH 04 1874 liformes, Pelecaniformes, Strigiformes and Ciconi- F. sparverius AMNH 8413, 8430, iformes examined) or (b) has a different pattern of fu- 8688, 15808, sion and different shape (within the Accipitridae). 15931, 16307, Degree of dorsal fusion of tympanum (2-4) CSG21, CSG9210 Herpetotherescachinnans AMNH unnum (2) The first 2 singleA elements are fused medially Mcrastur gilvicollis LSUMNS 98021 only, by an ossified bar which is an extension of the M. semitorquatus USNM 507797 pessulus. Mcrohierax erythrogonys AMNH 8623 (3) The first 3 or 4 A elements are fused lightly but Milvago chimachima LSUMNS 120427 entirely along their margins. This is an ordered char- M. chimango USNM 346421 acter: Phalcoboenusaustralis USNM 511795; (3.1) Margins are apparentalong the edgesofeach ring. LSUMNS 120728 (3.2) Margins are somewhatobliterated and only light Polihierax semitorquatus USNM 615218 suturesare apparent medially. P. insignis AMNH 8627 Polyborusplancus AMNH 9094 (4) At least 5 A elements are fused entirely along Spiziapteryxcircumcinctus LSUMNS unnum their margins. This is an ordered character: 8/9/90 (4.1) Suturesare apparent along the margins of all 5 Outgroups A elements except medially. (4.2) Suturesare always obliterated between the first Pelecanusroseus AMNH 8619 two A single elements (usually A3 and A4). Gampsonyxswainsonii AMNH 8529 Otus asio AMNH 8310 Degree of ventral fusion of tympanum (5-7) Mycteria americanus AMNH 8513 (5) The first three or four A elements (both double, Sula bassanus AMNH 8618 usually Al and A2, and single A elements) are fused Buteojamaicensis AMNH 18764 along their margins. Spacesare apparent between the Aegypiustracheliotus AMNH 8 1668 elements. Accipiterstriatus AMNH 18761 (6) The first three or four A elementsare fusedlight- Cathartesaura AMNH 20933 ly but entirely along their margins. (7) At least five A elements are fused entirely along their margins with some sutures apparent along the APPENDIX II. DESCRIPTIONS OF 25 margins, except medially. SYRINGEAL CHARACTERS Tympanum shape (8-9) The charactersfor the syringeal analysis are divided (8) The shape of the fused A elements forming the into the following categories: tympanum varies from cylindrical (the most caudal and cranial elements having the same diameter) to a 1. Tympanum (charactersl-9) graduatedA shape (the most caudal element wider in 2. A and B elements (characters10-18) diameter than the most cranial). This is a partially 3. Membranes and muscles(characters 19-25) ordered character:the transformationsbetween states Characters3, 4, 8 and 18 are ordered multistate char- 0, 1, and 2 are treated as unordered;the transformation acters. Character 21 is an unordered multistate char- from state 2 to 3 is ordered. acter. The plesiomorphic or primitive state for each (8.1) Tympanum shape is graduatedand widens cau- character is described either as state [0] for the char- dally. acter, or in the generaldescription for a group of char- (8.2) Tympanum is cylindrical. acters. (8.3) Tympanum is cylindrical; in addition, Al lat- 140 CAROLE S. GRIFFITHS

erally is flattened causinga ‘pinching in’ of the Fusion of A and B ventral ends most caudal element. (18) Fusion of additional B elements ends to form (9) Dorsal tympanum shape, medially, at pessulus a ridge bordering the internal membrane. This is an ascent. ordered character: [ 1] A ridge ofossified tissueforms a medial bridge (18.0) There is no fusion of B element ends. or connectionbetween the dorsal A 1 element ends and (18.1) B2 ends are fused to Bl/Al. covers the dorsal ascent of the pessulus. (18.2) B3 ends are also fused. A AND B ELEMENTS MEMBRANES AND MUSCLES In all Falconidaegenera, A 1 and B 1 dorsal and ventral (19) Existence of external (lateral) membrane on ends are fused (A 1 left to B 1 left, A 1 right to B 1 right). bronchi. Al elements (10-13) [0] There is no membrane, or, if one exists, the membrane lies between Bl-4 elements. In all Falconidaegenera, Al is a double element; both [ 11 An external membrane is located between Al rings are incomplete medially, and Al ends border the which is concave up and Bl which is concave down. internal membranes. ( 10) Separationof dorsal A 1 element ends. M. tracheolateralis(20-22) [0] Al dorsal ends are separated. Within the Falconidae the M. tracheolateralisalways [ 11 The dorsal ends of A 1 are close medially and insertson the external (lateral) membrane. The follow- are fused together by ossified tissue. ing 3 characters describe variations in this derived (11) Size of Al ends. character; the primitive state is hypothesized to be [0] Al is a single element or the width of the Al absenceof the insertion on the membrane. ends is proportionally similar to the width of Al me- (20) A cartilaginousbar exists on the lateral mem- dially. brane onto which the M. tracheolateralisinserts. [1] The dorsal ends of Al are very flattened and (21) M. tracheolateralis inserts on a membranous very enlarged. extension of the external membrane. (12) Flattening of the paired A 1 elements. [0] Al is a singleelement or each half is rounded (2 1.1) There is a thick, bulbousmembrane on the dor- and forms a C shapedring. sal half of the external membrane. The M. [ 1] EachAl is flatteneddorso-ventrally into a par- tracheolateralisinserts on the bulbousextension enthetical shape.When viewed laterally, the Al dorsal and on the external membrane. and ventral ends protrude out. (2 1.2) The bulbousmembrane covers the entire width (13) Appearance of A 1 on lateral view. of the external membrane. [0] Al is concave up medially. (22) The M. tracheolateralisinserts on the dorsal [ 1] Al is flattened medially. half of the lateral membrane. Bl elements (14-17) Cartilaginousborder on internal membrane (23-25) The following 4 charactersdescribe modifications of (23) Appearanceof the internal (medial) membrane. the dorsal ends of the first B element and subsequent [0] There is no membrane, or, if one exists, the variations in the fusion of A 1 and B 1. The primitive membrane is thin and has no crania1border. statefor thesecharacters is hypothesizedto be Bl ends [1] The internal (medial) membrane has a thick- which are rounded and end at the medial membrane ened cartilaginouscrania1 border. without fusing to A 1. The following 2 charactersdescribe the appearance (14) B 1 ends are very thick and wide and ascend of the cartilaginousborder, which is primitively hy- sharply in an L shape to fuse with Al ends. pothesized to be absent. (15) B 1 ends are thin and ascendgradually to fuse (24) The cartilaginousborder is thick and even, and with Al. concave up from Al dorsal to Al ventral ends. (16) There is a knobbing of Bl craniad edges;the (25) Additional thin, amorphous cartilage edges craniad extension or knob fuseswith A 1. the border, forming a straight caudal edge from Al (17) B 1 endsare thick and roundedand ascendgrad- dorsal to Al ventral ends. ually to fuse with Al.