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Syringeal Morphology and the Phylogeny of the Falconidae’

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Syringeal Morphology and the Phylogeny of the Falconidae’ The Condor 96:127-140 Q The Cooper Ornithological Society 1994 SYRINGEAL MORPHOLOGY AND THE PHYLOGENY OF THE FALCONIDAE’ 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 falcons, falconets, pygmy falcons, and caracarasin the family Falconidae. The phylogenyderived from thesedata establishesthree major cladeswithin the family: (1) the Polyborinae, containingDaptrius, Polyborus, Milvago and Phalcoboenus,the four genera of caracaras;(2) the Falconinae, consistingof the genus Falco, Polihierax (pygmy falcons),Spiziapteryx and Microhierax (falconets)and Herpetothe- res (Laughing Falcon); and (3) the genus Micrastur(forest falcons) comprising the third, basal clade. 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(Laughing Falcon) and Spiziapter- 1992). Patterns drawn from cladogramsprovide yx (Spot-winged Falconet). the blueprints for understanding biodiversity, 2. The Falconinae. This includes three genera: biogeography,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 caracara of birds, 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 hawks rather than of nine bird 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 monophyly 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 species (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 Kestrel (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
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