Apsaravis ukhaana Norell and Clarke, 2001

Skull

The skull is crushed against the right forelimb (fig. 1). The left(?) orbit contains a poorly preserved ring formed by an uncertain number of sclerotic ossicles (fragments of approximately 12 are visible; fig. 1). Close to the left orbit, and near phalanx 1 of right manual digit II, the partial right mandible is preserved as a crushed arch of bone (fig. 1). Part of the midsection of the left jaw is visible on the underside of the holotype block (figs. 2, 3, 5–7). A splint of bone lying parallel to the left jaw may be part of the left jugal (figs. 5, 6). If so, it would lack an ascending process separating the orbit from the subtemporal fenestra. Conservatively, Apsaravis ukhaana was scored as missing data for jugal characters (e.g., 50) in our analysis, because the element preserves no morphologies to unambiguously identify it as the jugal. The dentaries are edentulous and fused into an osseous symphysis (figs. 1, 7); posteriorly they are strongly forked (figs. 5, 6). The ossified symphysis is short, in contrast to some other basal avialans (e.g., Confuciusornis sanctus). On the lateroproximal surface of the right dentary, a row of small foramina parallels its dorsal edge; however, due to abrasion, they are now preserved as a shallow groove (fig. 7).

A fragment of the left quadrate identified as the otic process is pressed against the posterior cranium (fig. 5). Norell and Clarke (2001) tentatively made this identification, which is considered supported on further study of the specimen. Two additional characters were then scored for Apsaravis ukhaana (i.e., 35 and 36) to reflect this new information. The capitulae are not widely separated by a deep intercapitular incisure (fig. 5); however, as these articular surfaces are abraded, it is not possible to discern their degree of individuation (see character 36). The expanded posterodorsal tip of the otic process of the quadrate is slightly hooked. The morphology of the ventral portion of the quadrate is not discernable.

Vertebral Column

Twelve cervical vertebrae are preserved. However, the anteriormost cervicals are poorly preserved, and the atlas–axis complex is not distinguishable, making the total number of presacral vertebrae unknown in Apsaravis ukhaana. The midseries cervicals are comparatively well preserved and clearly heterocoelous (fig. 8). These vertebrae have conspicuously elongate pre- and postzygapophyses and arched postzygapophyses. Cervical ribs are fused and completely enclose transverse foramina (fig. 8).

Six opisthocoelous thoracic vertebrae with very shallow lateral depressions are exposed (fig. 9). An additional rib indicates the presence of a seventh vertebra. Aves possess 5–10 thoracics, while more primitive avialans have 12 or more (Chiappe, 1996). Well-developed ventral processes are not preserved on either the posterior cervicals or anterior thoracics. Two of the anteriormost thoracics are extremely poorly preserved and may have been fused to each other (fig. 9). Because fusion only in this anteriormost part of the thoracic series is not known in Aves, it is considered more likely that the edges of these vertebrae are simply not preserved. Martin (1983) considered two fused anterior thoracics to be present in Archaeopteryx lithographica and to comprise an avian “notarium”. Gauthier (1986) considered the presence of a notarium to be a synapomorphy of the crown clade. However, the presence of a notarium does not optimize as primitive to the crown clade (Clarke, 2002; this analysis). The Archaeopteryx lithographica condition would not optimize as homologous with either the condition in Apsaravis ukhaana or that derived within Aves, even if fusion was established to be present in both of these fossil taxa.

The sacrum is formed of 10 completely ankylosed vertebrae (figs. 1, 10). Ten or more sacral vertebrae are only known for Hesperornithes, Ichthyornis dispar, and Aves, while nine or fewer are present in more basal avialans (e.g., Chiappe, 1996). All sacral vertebrae in Apsaravis ukhaana have conspicuous transverse processes in ventral view (fig. 10), and spinal nerve openings along the entire sacral series are equally spaced (fig. 10), indicating that midseries sacral vertebral centra are equal in length. In contrast, in Ichthyornis dispar (and optimized as primitive to Aves) three or more midseries sacral vertebrae have short centra with diminutive, dorsally directed transverse processes (not visible in ventral view; Clarke, 2002).

Apsaravis ukhaana has five free caudal vertebrae and a completely ankylosed and strongly mediolaterally compressed pygostyle. The pygostyle is broken at its base and is missing its distal tip. However, it appears to have been short (figs. 10, 11). Because we cannot be certain of its exact length, we have scored this character (68) as missing data for Apsaravis ukhaana. No chevrons are preserved. The length of the transverse processes of the caudals approximates the width of their centra (fig. 11).

Pectoral Girdle and Ribs

Only the anterior margin of the sternum is preserved. The coracoid grooves are dorsoventrally broad (fig. 12) and adjacent to each other on this anterior edge of the sternum (fig. 13). Unlike the condition in Ichthyornis dispar, Ambiortus dementjevi, and Lithornis, they did not cross each other on the midline. In Hesperornithes, these grooves are widely separated. Coracoidal processes of the sternum and facets for articulation of the sternal ribs are not preserved. A ventral median ridge extends posteriorly from the anterior edge of the sternum (fig. 12). This ridge is interpreted as indicative of the presence of an anterior sternal carina. An anterior ridge has so far been associated with an anteriorly developed keel in all known Avialae with this region preserved (Norell and Clarke, 2001; Clarke, 2002). An exclusively posterior medial ridge or keel is present in some enantiornithines and in Confuciusornis sanctus (Chiappe et al., 1999), but it is not associated with the presence of an anterior midline ridge. On the anterior surface of the sternal rostrum, there is a midline fossa bordered in part by a slight anterior projection of the dorsal lip of the sternum (figs. 13, 14A). No uncinate processes, gastralia, or a furcula are preserved.

The scapula is slightly less than twice the length of the coracoid; its narrow blade is curved and tapers distally (fig. 1). The acromion is long and has a strongly hooked anterior tip (fig. 12, 14), which does not narrow to a point as it does in the hooked acromion of lithornithids (Houde, 1988). The scapular articular surface for the coracoid is not developed as a robust hemispherical tubercle like in Ichthyornis dispar (Marsh, 1880). Instead, it is virtually unprojected and is developed as a slight boss (fig. 14). In Hesperornis regalis, the entire anterior end of the scapula is rounded and fits into the concave end of the coracoid while fusion of the coracoid and scapula is primitive for Avialae (e.g., Chiappe, 1996).

A concave scapular cotyla on the coracoid is developed in Apsaravis ukhaana, Hesperornis regalis, and Ichthyornis dispar (Clarke, 2002). However, the scapular cotyla in Apsaravis ukhaana is much shallower than in Ichthyornis dispar, corresponding to the more weakly developed coracoid articular surface of the scapula. The acrocoracoid process lies dorsal to a prominent, laterally projected, glenoid facet, and it does not hook medially (fig. 12). A procoracoid process is not present. Where this process is developed in other avialans, there is only a very slight bulging of the medial surface of the coracoid (fig. 14). Penetrating the medial surface of the coracoid, near its midpoint, is the supracoracoideus nerve foramen (fig. 14). A groove extends just proximal and distal to this foramen (fig. 14). The supracoracoideus nerve foramen exits into a deeply concave dorsal surface just distal to the scapular cotyla (fig. 15). The concave dorsal coracoidal surface, location of the foramen, and development of a groove at its medial opening are morphologies developed in enantiornithine taxa (e.g., Chiappe, 1991; Chiappe and Calvo, 1994) as well as in Apsaravis ukhaana.

The coracoid's lateral margin is straight to slightly concave (fig. 12), unlike the convex margin of Enantiornithes (Chiappe, 1996). At the sternal articulation, the lateral margin flares into a diminutive lateral flange (fig. 12) of uncertain homology with the lateral process developed in some Aves and other avialans. This process bears a conspicuous muscle impression that extends proximally along the lateral margin of the coracoid (fig. 13). Elliptical foramina with irregular edges on the ventral surfaces (fig. 13) of the coracoids are probably artifacts.

Pectoral Limb

Both humeri were preserved in articulation with the radii and ulnae. However, the distal end of the right humerus was removed and prepared to expose its anterior surface (fig. 16). The humeral head is globose and projects more proximally than does the deltopectoral crest (fig. 12), a condition known for Ichthyornis dispar and Aves, but not present in Patagopteryx deferrariisi or Enantiornithes (Chiappe, 1996). The deltopectoral crest in Apsaravis ukhaana is dorsally directed, as opposed to the condition in Aves where it is anteriorly projected (fig. 12). The deltopectoral crest is relatively large and projects dorsally approximately the width of the humeral shaft (fig. 12).

The posterior surface of the deltopectoral crest is concave proximally (fig. 12). A shallow pneumotricipital fossa is present but does not contain a pneumatic foramen (fig. 12). The ventral tubercle lies adjacent to the pneumotricipital fossa (fig. 12). A marked capital incisure is not developed. An unusual, second, equally developed tubercle (“tub” in fig. 12) protrudes from the posterior surface distal to the humeral head and dorsal to the pneumotricipital fossa. It lies in the position of a muscle insertion that within Aves (e.g., in Galliformes and Tinamidae) sometimes distally “closes” the capital incisure. However, this insertion where developed in Aves is not projected as extensively as it is in Apsaravis ukhaana. On the anterior surface of the bicipital crest of the right humerus lies a pit-shaped fossa (figs. 2, 8). This area of the left humerus is covered by matrix. A fossa in the position observed in Apsaravis ukhaana has been considered a synapomorphy of Enantiornithes (Sanz et al., 1995; Chiappe, 1996). The entire anterior surface of the bicipital crest is projected and slightly bulbous (fig. 8). On the anteroventral edge of the left humerus, the impression of the lig. acrocoracohumerale (“transverse groove”) is developed as a fossa rather than as a groove (fig. 8).

The anterior surface of the distal humerus is somewhat crushed, but the condyles are clearly visible developed on this surface as in other basal avialans (Chiappe, 1996; fig. 16). The distal humerus is anteroposteriorly compressed and expanded dorsoventrally, giving the entire distal end a “spatulate” appearance (fig. 16). The dorsal condyle angles ventrally at a relatively high angle (more than 45;dg) to the axis of the humeral shaft. The ventral condyle is developed as a weak, “straplike” ridge at the distal edge of the anterior surface (fig. 16). These last three conditions have been considered characteristic of enantiornithines (Chiappe, 1996). A brachial fossa or scar is not visible.

The posterior humeral surface is depressed ventrally by a poorly defined olecranon fossa and by the impression of the m. humerotriceps (fig. 16). The m. scapulotriceps groove is not developed. The entire distal margin of the humerus angles ventrally as in Enantiornithes (Chiappe, 1996; fig. 16). This morphology has also been referred to as the presence of a well-developed flexor process in Enantiornithes (e.g., Chiappe, 1996).

The ulna and humerus are approximately the same length (fig. 1). Proximally, the ulna has a well-developed olecranon process and a large bicipital tubercle (fig. 17). The dorsal and ventral cotylae were not separated by a groove as in some enantiornithines (Chiappe, 1991; fig. 17). The distal end of the ulna is semilunate, and the carpal tubercle is well developed (fig. 2).

The nearly straight radius is approximately half the width of the ulna (fig. 17). Proximally, it has a conspicuous bicipital tubercle (fig. 17), which is also present in Ichthyornis dispar. It lacks the deep longitudinal groove seen in Enantiornithes (Chiappe and Calvo, 1994) and bears a flat muscle scar in this area as in Aves. Radiale are preserved in rough articulation with the carpal trochlea in both wrists (figs. 3, 18). The ventral ramus (“long arm”) and part of the body of the ulnare are visible in close association with the posterior carpometacarpus (fig. 18).

The semilunate carpal and metacarpals I, II, and III are firmly ankylosed proximally (fig. 18). Whether metacarpals II and III were also fused distally is unknown because the distal extreme of the left carpometacarpus is not preserved and that of the right is almost completely obscured by the right humerus (figs. 5, 6). A pisiform process is connected by a low ridge to metacarpal III (fig. 18). A shallow infratrochlear fossa is developed just proximal to the pisiform process (fig. 18). The carpal trochlea is incised with a strong midline groove (fig. 18), unlike the condition in Ichthyornis dispar. Metacarpal III is flat, bowed caudally, and much less than half the width of metacarpal II (fig. 18). Its anterior surface bears a muscular depression. Such a depression in Aves is associated with the attachment of the mm. interossei (Baumel and Witmer, 1993) and is notably present in Enantiornithes, Ichthyornis dispar, and Aves. In Aves, these muscles are responsible for flexion, extension, and elevation of the phalanges of the second digit (Raikow, 1985).

A projected extensor process is developed on the proximal end of metacarpal I (fig. 18). The anterior margin of metacarpal I is concave between the process and the slightly flared phalanx 1 articulation (fig. 2) and unlike the broadly convex condition found in Confuciusornis sanctus and enantiornithines (Norell and Clarke, 2001). The proximal surface of metacarpal I is excavated by a deep anterior carpal fovea (fig. 18). Distally, the articulation for the first phalanx is developed as a weak ridge, rather than primitively as a ginglymus (fig. 2). A small fragment of the first phalanx of digit I of the left hand is preserved against this surface (fig. 2).

The right proximal phalanx of digit II is preserved in articulation with metacarpal II (figs. 1, 5). The posterior surface is strongly compressed dorsoventrally, and its edge is bowed posteriorly (fig. 1). The posterior margin of this phalanx is not bowed in Ichthyornis dispar or in more basal avialans with this digit preserved (e.g., Confuciusornis sanctus, Enantiornithes, or Ambiortus dementjevi).

Pelvic Girdle

The pre- and postacetabular blades of the ilium are approximately equal in length (fig. 1). The ischium and pubis are approximately equal in length, and lie parallel to the ilium (fig. 10). The ischium and pubis are not ankylosed distally although they are extremely closely appressed. All three pelvic bones are firmly ankylosed proximally. Unlike the primitive avialan condition seen in Confuciusornis sanctus and Enantiornithes (Chiappe, 1996), the pubes do not contact each other distally and the pubic apices are widely separated. The pubes are very narrow and mediolaterally compressed throughout their length. By contrast, the pubes in enantiornithines and Patagopteryx deferrariisi and other more basal avialans are rodlike, robust, and uncompressed (Chiappe, 1996). The mediolaterally compressed pubic shaft in Apsaravis ukhaana (fig. 10) is otherwise only known with certainty from Hesperornis regalis and Aves (Chiappe, 1996). The pubes in Apsaravis ukhaana are notably more delicate than those in Ichthyornis dispar (Clarke, 2002). The obturator foramen is slightly demarcated distally by a flange of the ischium (fig. 10). A well-developed antitrochanter lies on the posterodorsal corner of the acetabulum (figs. 10, 19). No pectineal process is present.

Pelvic Limb

The femur is moderately bowed and longer than the tarsometatarsus (fig. 1). The capital ligament fossa is visible on the head of the left femur, which is exposed through the left acetabular opening (fig. 10). The lateral surfaces of the femora are not well exposed. A hypertrophied projection of the posterolateral edge of the femur forms a large trochanteric crest, an autapomorphy of Apsaravis ukhaana (fig. 19). The morphology of the proximal portion of this crest is not well preserved. A patellar groove extends onto the anterior surface of the distal femur, a condition known only for Hesperornithes, Ichthyornis dispar, and Aves (Chiappe, 1996). The posterodistal surface is poorly preserved, and the presence of a popliteal fossa cannot be determined. An intermuscular line, visible on the right femur, follows the medial edge of the posterior surface proximally for about one-half the length of the bone.

Only the distal ends of the tibiotarsi are preserved (figs. 1, 20, 21). The right is preserved in articulation with the tarsometatarsus (fig. 21). The astragalus and calcaneum are completely fused to the tibia; no sutures are visible. Although neither fibula is preserved, they are inferred not to have reached the tarsal joint; no associated indentation or groove is present on the lateral edges of the either tibiotarsus.

Paired ridges are developed on the anterodistal surface of both tibiotarsi (fig. 21). These ridges are identified, based on their position and morphology, as topologically correspondent to the tubercles for attachment of the extensor retinaculum in Aves (tuberositas retinaculi extensoris; Baumel and Witmer, 1993; fig. 21). An extensor groove and a supratendinal bridge are not developed in Apsaravis ukhaana.

A slight depression on the distal end of the tibia in Patagopteryx deferrariisi was previously identified as a possible homolog with an avian extensor groove (Alvarenga and Bonaparte, 1992; Chiappe, 1996). Here it is reinterpreted as morphologically correspondent to the area demarked by the attachments of the retinaculum (Clarke, 2002) because it is shallower and more proximally developed than an extensor groove in other avialans.

The extensor retinaculum in Aves directs the passage of the m. tibialis cranialis as well as the m. extensor digitorum longus (Baumel and Raikow, 1993), two primary avian foot extensors (Baumel and Raikow, 1993). Evidence for the retinaculum tubercles (associated with both the m. tibialis cranialis and m. extensor digitorum longus) occurs phylogenetically earlier (synapomorphy of Confuciusornis sanctus + Aves; Clarke, 2002 and this analysis) than evidence for the extensor groove, an additional constraint on the passage of the m. extensor digitorum longus (a synapomorphy of Hesperornithes + Aves; Clarke, 2002 and this analysis).

Shifts in the function and/or relative importance of the m. tibialis cranialis and m. extensor digitorum longus may explain the variation in position and development of metatarsal tubercles in basal avialans (Chiappe, 1996) vs. in Aves and near outgroups (Clarke, 2002). A large tubercle on the anterior surface of metatarsal II in some basal avialans (e.g., Confuciusornis sanctus [Chiappe et al., 1999], Vorona berivotrensis [Forster et al., 1996], and Enantiornithes [Chiappe, 1996]) appears topologically correspondent to the m. tibialis cranialis tubercles in Aves (Chiappe, 1996). In Apsaravis ukhaana, and optimized as primitive to Aves (Clarke, 2002), the tubercles associated with the m. tibialis cranialis are less pronounced and are located on the anteromedial edge of metatarsal II and/or on the anterior surface of metatarsal III. In Apsaravis ukhaana, a single tubercle is visible on the medial edge of metatarsal III (fig. 21).

A deep, subcircular fossa excavates the proximal surface of the lateral condyle (figs. 20, 21) of the tibiotarsus. A similar fossa has been described for Vorona berivotrensis and Enantiornithes (Forster et al., 1996), and it is very faintly developed or absent in Ichthyornis dispar and Aves. The intercondylar groove is shallow and located far medially. It is also narrow; its width is less than a third of that of the distal tibiotarsus, unlike the comparatively broad groove in Patagopteryx deferrariisi, Hesperornis regalis, Ichthyornis dispar, and Aves, for example (Chiappe, 1996; Marsh, 1880).

Neither distal condyle of the tibiotarsus tapers medially, which gives the distal tibiotarsus in Apsaravis ukhaana the “barrel-shaped” aspect found only in some Enantiornithes (e.g., Nanantius eos; Molnar, 1986) and Vorona berivotrensis (Forster et al., 1996). However, the latter taxa, Patagopteryx deferrariisi, and other basal avialans share the condition seen in nonavialan theropods where the medial condyle is broader than the lateral one (Chiappe, 1996; Forster et al., 1996). In contrast, in Apsaravis ukhaana the opposite is true; the lateral condyle is more than twice the width of the medial one (fig. 20). In Hesperornithes, Ichthyornis dispar, and most Aves, the condyles are approximately equal in width, or the lateral is slightly larger. The extreme difference in condylar proportions in Apsaravis ukhaana is also similar to the condition in Vorona berivotrensis (Forster et al., 1996) and Nanantius eos (Molnar, 1986) and is more marked than seen in nonavialan theropods (e.g., Norell and Makovicky, 1999), Confuciusornis sanctus (Chiappe et al., 1999), and Patagopteryx deferrariisi (Chiappe, 1996), for example.

In Apsaravis ukhaana, the cartilage-covered distal articular surface of the tibiotarsus extends up its posterior surface to approximately even with the proximal edge of the condyles. This surface is demarcated by pronounced posteriorly projected medial and lateral edges as well as a slight difference in bone texture. A large, similarly demarcated, posterior trochlear surface is also seen in Aves. In Aves, this surface (trochlea cartilaginis tibialis; Baumel and Witmer, 1993) serves as the articular surface for the tibial cartilage. The condition in Apsaravis ukhaana and Aves is derived (see character 185) relative to the condition in more basal theropods where there is no indication of a posterior component to the distal articular surface and textured bone is limited to the distal end of the tibia and distal surfaces of the proximal tarsals (e.g., Velociraptor mongoliensis; Norell and Makovicky, 1999).

The edges of this posterior surface of the tibiotarsus (trochlea cartilaginis tibialis; Baumel and Witmer, 1993) are developed as extremely pronounced wings in Apsaravis ukhaana. The medial wing of this surface is conspicuously more strongly projected than the corresponding lateral wing, and its distal edge is prominently notched (figs. 1, 21). These hypertrophied wings of the posterodistal tibiotarsus are identified as an autapomorphy of Apsaravis ukhaana (see diagnosis).

Metatarsals II through IV are fused with the distal tarsals and to each other throughout their lengths; they ankylose distally to enclose the distal vascular foramen (figs. 21, 22). However, the edges of the shafts of the metatarsals remain distinguishable throughout their lengths (fig. 21) unlike the condition in Ichthyornis dispar, Hesperornis regalis, and most Aves. Metatarsal V is absent. The proximal end of metatarsal III is displaced posteriorly (fig. 21), a derived condition also seen in Hesperornis regalis (Marsh, 1880), Ichthyornis dispar (Marsh, 1880), and Aves (e.g., Baumel and Witmer, 1993). Proximally, intercotylar eminence is not developed. The lateromedial width of the medial cotyla is approximately one-third that of the lateral cotyla. However, the anterior edge of this medial cotyla is projected farther proximally than that of the lateral cotyla (fig. 21).

A single proximal vascular foramen is developed between metatarsals III and IV (fig. 21). In the position of an avian hypotarsus in Apsaravis ukhaana is a flat, weakly projected, discrete area similar to that of Hesperornis regalis (Marsh, 1880) and Patagopteryx deferrariisi (Chiappe, 1996; fig. 23). This surface is considered the topological equivalent of the hypotarsus in Aves where at least one well-developed hypotarsal crest or groove is present on this surface. In Apsaravis ukhaana, this surface has relatively little distal extent and is defined distally by a midline depression of the shaft. A conspicuous ossified tendon extends down the midline of the tarsometatarsus distal to the hypotarsus in both the right and left foot (fig. 23). This ossified tendon may correspond to that of the m. flexor digitorum longus in Aves (Hutchinson, in press). As such, it would be the earliest known occurrence of an ossified tendon associated with this muscle (Hutchinson, in press). Plantar crests are visible bordering a slightly depressed flexor sulcus (fig. 22).

The distal vascular foramen angles obliquely ventrodistally and exits in a small depression on the plantar surface. This foramen has only one distal exit, whereas in Aves two exits are present: one is plantar (that present, for example, in Apsaravis ukhaana and Ichthyornis dispar [Clarke, 2002]) and the second is directly distal, between metatarsals III and IV. Digit I is not preserved and may not have been present. If this absence is not an artifact, then lack of digit I in Apsaravis ukhaana represents the phylogenetically earliest known such loss among avialans. Loss of digit I in Aves occurs in some ground-dwelling birds (e.g., some ratites; Baumel and Witmer, 1993; Stidham, personal commun.) as well as an array of other avians of highly varied ecologies (Raikow, 1985).

Metatarsal III is the longest, and metatarsal II is the shortest in Apsaravis ukhaana. Metatarsal II projects only as far as the base of the trochlea of metatarsal IV. Livezey (1997b) found a short metatarsal II to be derived within Aves (e.g., within Anseriformes); however, no outgroups of Aves were included in that analysis. In Hesperornithes (Marsh, 1880; Martin and Tate, 1976), Ichthyornis dispar (Marsh, 1880), Gansus yumenensis, and Apsaravis ukhaana, metatarsal II is shorter than metatarsal IV (i.e., it extends only as far as approximately the base of metatarsal IV). This condition is derived in Avialae but is optimized as primitive for Aves; having metatarsal II equal in length to metatarsal IV is optimized as a derived condition in some basal avians (Clarke, 2002; contra Livezey, 1997b).

Metatarsal II projects plantar to metatarsals III and IV and has a well-developed wing on the medial edge of its trochlear surface (fig. 22). A correspondingly developed lateral wing is also present on the lateral plantar trochlear surface of metatarsal IV. The trochlea of metatarsal III is widest, and those of metatarsals II and IV are approximately equal in width (fig. 21).

Phalanges are associated with both tarsometatarsi; some are in partial articulation. Phalangeal length appears to decrease distally in digits II–IV as typical in birds that spend at least part of their time on the ground (e.g., Hopson, 2001). The first phalanx of digit II has strong flexor keels, with the lateral keel better developed than the medial one. Small collateral ligament pits are present. Both articular surfaces of the shorter second phalanx of digit II are ginglymoid, and the collateral ligament pits are large, taking up most of the medial and lateral surfaces of the distal end.

The proximal end of the first phalanx and the complete second phalanx of digit III are preserved in partial articulation with the right tarsometatarsus (figs. 21, 22). Only the complete first phalanx of digit III is preserved in articulation with the left (fig. 1). The shaft of the phalanx tapers distally. The third and fourth phalanges of digit III are visible and associated with the left foot. On the third phalanx of digit III, collateral ligament pits are not visible and are either absent or extremely weakly developed. The fourth phalanx is slightly broken distally but would have been approximately equal in length to the third phalanx. It is recurved with vascular grooves and a large flexor tubercle.

The proximal three phalanges of digit IV are preserved in partial articulation on the right pes (figs. 21, 22). The first phalanx has well-developed flexor keels, with the medial keel better developed than the lateral one. The second phalanx is approximately one-half the length of the first. The third phalanx (IV:3) is slightly shorter than the second phalanx. All of the preserved unguals are recurved, including three preserved in a separate (and unfigured) block.

Of “Transitional Shorebirds” and Ornithurine Ecology

In Norell and Clarke (2001) and Clarke and Norell (2001) we responded to Feduccia's (e.g., 1995, 1996, 1999) statements regarding the ecology of ornithurine birds (sensu Martin, 1983). For example, Feduccia (1999: 152) wrote, “Given the near absence of ornithurine birds in Late Cretaceous continental deposits and their near exclusive occurrence as ‘transitional shorebirds’, ichthyornithiforms and hesperornithiforms, it is tempting to speculate that ornithurines may have been more or less restricted to shoreline and marine deposits during this time”. Feduccia's (1995, 1996, 1999) statements are the latest avatar of an oft-discussed, but often nebulous, hypothesis concerning the “shorebird ecology” of Mesozoic avialan taxa placed as basal parts of, or close to, Aves.

Martin (1987: 17) attributed to Brodkorb the idea that “[a]ll of the Mesozoic birds that have affinities with Cenozoic birds are also recognized to have basically charadriiform postcranial skeletons”. Brodkorb, in his Catalogue of Fossil Birds (Brodkorb, 1967), indeed included Mesozoic taxa such as Ichthyornis, Apatornis, the “Graculavidae”, and Cimolopterygidae with Charadriiformes, the crown clade taxon referred to as “shorebirds”. Martin (1983: 311) later identified Ichthyornis dispar and Apatornis celer (as well as Hesperornithes) as outgroups of the avian crown clade (contra Brodkorb, 1967). Despite that these taxa were no longer placed with crown shorebirds, Martin emphasized that they, and, in fact, “[a]ll Mesozoic Ornithurae are aquatic in one way or another” (Martin, 1983: 311). He also commented of ornithurines, “The basic adaptive zone of the group seems to be wading along the shoreline. This is still an important avian adaptive zone and one for which few other Mesozoic vertebrates would have been well suited” (Martin, 1983: 311). The characters used to place these Mesozoic taxa with Charadriiformes (e.g., Brodkorb, 1967), and what constituted the perceived “key” ecological “variable” (e.g., aquatic lifestyle or wading) in common amongst ornithurines (Martin, 1983, 1987), were not articulated.

In 1987, Martin elaborated, “I think that this situation will be maintained as the Mesozoic record becomes better known and that the entire modern avian radiation had its origin within these so-called ‘basal charadriiforms’. In this case, it is probably better to think of these as primitive charadriiform-like birds but perhaps not really members of the modern order Charadriiformes, and all modern orders may be post-Mesozoic in age” (Martin, 1987: 17). In these statements, Martin (1983, 1987) further developed the ideas that (1) ornithurines are occupying, perhaps exclusively, a “shorebird adaptive zone”, and (2) that “modern” or crown clade birds had their “origin in” (Martin, 1987: 17) taxa with a “shorebird ecology”. Feduccia (1995, 1996, 1999) went further, positing the existence of a “bottleneck of avian morphotypes transcending the K/T boundary, like mammalian insectivores” (Feduccia, 1995: 638), and suggested the competitive exclusion of ornithurines from other “continental” environments by enantiornithines, which he has referred to as “the dominant land birds of the Cretaceous” (e.g., Feduccia, 1995: 637; see also Feduccia, 1999).

Olson and Parris (1987) took a different stance in their evaluation of the Late Cretaceous Hornerstown birds (e.g., parts of “Graculavidae”) often cited (e.g., Feduccia, 1995; Chiappe, 1995) as evidence of Cretaceous crown (or “modern”) orders. These authors wrote: “As far as can be determined, all of the birds in this assemblage were probably marine or littoral in habits. We certainly would not interpret this as an indication that waterbirds are primitive and that they gave rise to land birds … (Olson, 1985)” (Olson and Parris, 1987: 19). These authors, while agreeing that these birds had marine or littoral ecologies, apparently differed in their interpretation of the implications of these data (Olson, 1985; Olson and Parris, 1987).

Finally, Feduccia (2001; contra Feduccia, 1995, 1996, 1999; Martin, 1983, 1987), described ornithurine taxa as abundant and well known from continental deposits, including those with “no particular adaptations for near-shore habitats” (Feduccia, 2001: 507). He further commented, “What correlation is there between the distribution of shorebirds (waders; Charadriiformes) and the marine shoreline deposits of the continental margins? These birds are quite cosmopolitan …” (Feduccia, 2001: 507).

For the point of argument, we accepted (Norell and Clarke, 2001) that previously described Mesozoic ornithurines were identified as exhibiting an “ecological” restriction to littoral or marine habitats based on evidence of some kind, either (1) from their depositional environment or (2) from morphology. Inferring ecology from either form of evidence is complex and often problematic (e.g., Anderson, 2001; Behrensmeyer, 2001; Kidwell, 2001; Skelton, 2001). Further, it remains unclear what ecological character was interpreted (Martin, 1983, 1987; Feduccia, 1995, 1996, 1999) as held in common among, for example, Ichthyornis (with an ecology likened to that of a tern; Marsh, 1880), Hesperornis (a highly modified flightless diver (Marsh, 1880), and, for example, the filter-feeding, wading, anseriform Presbyornis (Olson and Feduccia, 1980). However, these points were not the basis for our argument.

We accepted that the ornithurines that formed the basis for the “shorebird hypothesis” had been described from littoral, marine, or lacustrine deposits, and that formed part of the evidence used to argue that they were restricted to these environments (Martin, 1983; Feduccia, 1996, 1999). In contrast to these taxa, we pointed out that Apsaravis ukhaana is from a semi arid dunefield (Loope et al., 1998; Norell and Clarke, 2001), data not easily construed as supporting evidence of a restriction of ornithurines to shorebird habitats.

Although morphological evidence is also used to infer ecology, the often discussed “shorebird morphologies” are notoriously hard to define. Livezey (1997b) aptly remarked in reviewing the “transitional shorebird” hypothesis (in the context of the phylogenetic relationships of Presbyornis pervetus) that even identifying derived morphologies diagnosing Charadriiformes (i.e., crown clade “shorebirds”) remains problematic (e.g., Strauch, 1978; Chu, 1995). Further, the presence of morphologies convergently seen in extant Charadriiformes in taxa supported as outgroups of the crown clade, does make these taxa shorebirds, or these morphologies indicative of a shorebird ecology. Indeed, several morphologies that have been considered characteristic of Charadriiformes (e.g., the presence of fewer sacral vertebrae, prominent lateral excavations of the thoracic vertebrae and an unpneumatized humerus) are optimized as plesiomorphic for much more inclusive avialan subclades (e.g., Ornithurae) as well as derived within Aves and present in Charadriiformes (as well as other neoavians; Clarke, 2002). Further, although there are several characters that are optimized specifically as convergently present in some Charadriiformes and Ichthyornis dispar (Clarke, 2002), these morphologies are not seen in Apsaravis ukhaana.

No morphological or paleoenvironmental data from Apsaravis ukhaana support its identity as a shorebird even if we accept the kinds of evidence used by proponents of the “ecological bottle neck” hypothesis (Clarke and Norell, 2001). However, as illustrated in Feduccia (2001), there are general problems with the testability of this hypothesis and the style of argumentation used to support it. For example, Feduccia (2001: 507) wrote, “Because shoreline habitats were as common in continental interiors as on continental margins during the Late Cretaceous and shorebirds are equally at home in freshwater and marine environments, Apsaravis has no bearing on the habitat of Late Cretaceous birds”. If this position is taken, then no paleoenvironmental data can be used to corroborate or test the shorebird hypothesis. It cannot be deemed exceptionable only in the case of Apsaravis ukhaana. If any fossil could be a cryptic shorebird regardless of depositional environment and morphology, how is this shorebird hypothesis able to be investigated?

We (Clarke and Norell, 2001) proposed optimizing ecology on a phylogeny of Aves and its near outgroups as a potential test of this hypothesis. We used a phylogeny supported by morphological and molecular data (reviewed in Cracraft and Clarke, 2001), in which Palaeognathae and Galloanserae are, respectively, two of the basalmost divergences within the avian crown clade. Charadriiformes (“shorebirds”) are placed as part of Neoaves, the sister taxon of Galloanserae, which includes all other non-galloanserine neognaths in what is essentially an unresolved polytomy (reviewed in Cracraft and Clarke, 2001). We (Clarke and Norell, 2001) attempted to roughly “bracket” (e.g., Witmer, 1995) the ecology basal to Aves considering extant taxa for which ecology can be observed. No extant palaeognaths or galloanserines have been considered to have a “shorebird ecology” and Neoaves would be polymorphic for such a character (Clarke and Norell, 2001). Even if Ichthyornis dispar is considered to have a “shorebird ecology”, (e.g., per Marsh, 1880), this ecology cannot parsimoniously optimize as primitive to Aves (Clarke and Norell, 2001). It is optimized as independently derived within Neoaves and for Ichthyornis dispar. For this rough optimization, Hesperornis regalis and Apsaravis ukhaana were not considered to evidence a “shorebird ecology”.

Feduccia (1996, 1999, 2001) has also commented that several Paleogene taxa described as “shorebird mosaics” were further evidence that a shorebird ecology was primitive to the avian crown. For example, he wrote “the basal status of the transitional shorebirds … is evidenced not only by the presence of numerous latest Cretaceous and early Paleocene fossils of transitional shorebirds but by the discovery of a number of shorebird-modern order mosaics in the Eocene: Juncitarsus, Presbyornis and Rhynchaeites …” (Feduccia, 1999: 165). Of these three taxa, Presbyornis has been placed most basally within Aves (in Galloanserae; Ericson, 1997; Livezey, 1997b), but, because of its position nested within extant Anseriformes, it cannot alone affect the optimization of ecology primitive to Galloanserae, let alone for all of Aves. However, more inclusive analyses of fossil and extant parts of Aves and its near outgroups are the necessary next step toward further investigation of these issues.

Here, and in Clarke and Norell (2001), we outlined an approach that places the ornithurine ecological restriction argument in a testable frame, in marked contrast to the intuitive approach taken by others (e.g., Feduccia, 1995, 1996, 1999, 2001). Future work optimizing the ecological characters ancestral to Aves will be particularly effected by (1) inclusion of Tertiary fossil taxa on the stem lineages of subclade crowns, (2) resolution of neoavian relationships, and (3) the discovery, phylogenetic placement, and inferred ecology of other new near-outgroups of Aves. Finally, it is essential to rigorously discriminate the various ecological variables referred to collectively as a “shorebird ecology” for potential inclusion in, or optimization on, such a phylogeny.

Diagnosis of Enantiornithes

While 27 characters have been proposed as derived morphologies of Enantiornithes (e.g., Walker, 1981; Chiappe, 1991, 1996, 2001; Kurochkin, 1996; Sereno et al., 2002; listed in the supplementary information of Norell and Clarke, 2001), in the current analysis, only 4 characters support monophyly in both most parsimonious trees. The strict consensus of these is presented in figure 24. Enantiornithine monophyly collapses with a tree length one step longer than the most parsimonious topologies.

As noted in Norell and Clarke (2001), as further avialan taxa, such as Apsaravis ukhaana, are described, many previously proposed unique enantiornithine morphologies are discovered to have a broader distribution within Avialae. They are optimized as having alternatively homoplastic distributions or as primitive to an avialan subclade including Aves and Enantiornithes (see two examples discussed below). One implication of the more complex known distributions of these characters is that the identification of isolated elements as part of Enantiornithes (e.g., Nanantius eos; Molnar, 1986) based on the presence of one, or a few, such characters need to be reevaluated. For example, the narrow intercondylar groove and barrel-shaped aspect of the condyles of the tibiotarsus used to refer Nanantius eos to Enantiornithes (Molnar, 1986) are also seen in Apsaravis ukhaana and Vorona berivotrensis. Such fragmentary fossils may be found to be part of Enantiornithes, but further analyses of their phylogenetic relationships that include recently discovered taxa, such as Apsaravis ukhaana, are recommended.

Two examples of characters that, with the discovery of Apsaravis ukhaana and our increasing knowledge of the morphology of basal avialans, are no longer optimized as unique to Enantiornithes are from the coracoid (Norell and Clarke, 2001). The condition in which the dorsal surface of the coracoid is strongly concave versus flat to convex throughout the majority of the shaft has been considered a derived feature of Enantiornithes (Walker, 1981; Chiappe, 1991, 1996). However, as discussed in Norell and Clarke (2001), the dorsal surface of the coracoid in Dromaeosauridae is broadly concave, and it is deeply concave in Confuciusornis sanctus and Apsaravis ukhaana (Norell and Clarke, 2001). It appears that it is the loss of the depression or fossa, rather than its presence, that is derived within Avialae.

Further, in both Apsaravis ukhaana and Neuquenornis volans (Chiappe and Calvo, 1994) the posterodorsal opening of the supracoracoideus nerve foramen lies in the depressed dorsal surface, or dorsal fossa, of the coracoid. The medial opening of the supracoracoideus nerve foramen being developed in a groove was also considered a derived feature of Enantiornithes (Chiappe, 1991). However, in Dromaeosauridae, this medial opening of the foramen lies into a broad depression on the anteromedial surface of the coracoid. In Neuquenornis volans, Concornis lacustris, Cathayornis yandica, Gobipteryx minuta, as well as Apsaravis ukhaana, the medial opening of the foramen lies in an elongate groove that we consider the topological equivalent of the broad depression in Dromaeosauridae. In Confuciusornis sanctus, the morphology of the supracoracoideus nerve foramen is unknown. Previous descriptions of this morphology (see excluded character 97) considered the dromaeosaurid condition equivalent to that in the avian crown clade as state “0” for purposes of analysis (e.g., Chiappe and Calvo, 1994). However, while the foramen lies in a depression in Dromaeosauridae, it lies on a flat surface in Aves.

To consider the effect of the previous interpretation of these coracoidal morphologies, characters 89 and 97 were swapped in to replace 88 and 98. When 89 and 97 were included (and 88 and 98 removed), two most parsimonious trees resulted that were two steps longer (length = 394; CI = 0.68; RI = 0.81; RC = 0.55) than the analysis including 88 and 98 (and excluding 89 and 97). In neither of these trees do characters 89 and 97 optimize as synapomorphies of Enantiornithes. Given that a “dorsal fossa” (89:1) is present in Confuciusornis sanctus and in Apsaravis ukhaana, this feature optimizes as a synapomorphic gain of Confuciusornis sanctus + Aves followed by a loss outside of Hesperornithes + Aves. In the case of the medial opening of the supracoracoideus nerve foramen into an elongate groove (97:1), it is equally parsimoniously gained at Enantiornithes + Aves and lost in Hesperornithes + Aves as it is independently gained in Enantiornithes and in Apsaravis ukhaana.

Assembly of the Avian Flight Stroke

We noted in Norell and Clarke (2001) that Apsaravis ukhaana provides insight into the assembly of the avian flight apparatus, as the basalmost avialan with an avian extensor process. In Aves, a strong, anteriorly projected “extensor” process on metacarpal I is developed at the insertion of the m. extensor metacarpi radialis and the propatagial ligaments (e.g., Ostrom, 1976). The m. extensor metacarpi radialis functions to “automate” extension of the manus with extension of the forearm in Aves (Vasquez, 1994). This automation has been considered a “key innovation” in the origin of flight (e.g., Ostrom, 1995) and has been proposed to be present in nonavialan theropods (Ostrom, 1995; Gishlick, 2001).

We argued (Norell and Clarke, 2001) that the strongest inference of the point of origin of avian automatic extension of the forelimb is at the Apsaravis + Aves node because Apsaravis ukhaana is the phylogenetically earliest avialan to have a morphology of metacarpal I associated with m. extensor metacarpi radialis function in extant parts of Aves. Here, we elaborate ideas presented in that paper (Norell and Clarke, 2001).

In Apsaravis ukhaana, a muscular process developed on the anterior tip of metacarpal I is pointed and extends well past the anterior tip of the articular surface for phalanx I:1 (fig. 2). The degree of projection (see above) and pointed morphology in Apsaravis ukhaana is seen in Ichthyornis dispar and optimized as primitive to Aves (Clarke, 2002). However, they are not seen in more basal avialans with this region preserved. In Archaeopteryx lithographica and nonavialan theropods (to varying degrees), the proximoanterior edge of metacarpal I flares slightly but does not extend past the anterior limit of the articular surface for phalanx I:1. In Confuciusornis sanctus and enantiornithines, the entire surface of metacarpal I is bowed, or broadly convex, anteriorly (Clarke and Chiappe, 2001). Additionally, two new basal avialan taxa were recently described from China (Zhou and Zhang, 2002a, 2002b). Both lack the convex anterior edge of metacarpal I seen in Confuciusornis sanctus and Enantiornithes, having instead an hourglass-shaped anterior surface like that seen in Archaeopteryx lithographica and nonavialan outgroups. However, metacarpal I projects more in these taxa than in Archaeopteryx and nonavialan theropods but less than in Apsaravis ukhaana, Ichthyornis, and Aves. Because the degree of projection thus appears continuously variable, at what point the “key innovation” in the development of the avian function might be identified is unclear.

We proposed that at the Apsaravis + Aves node, where a morphology associated with “automatic” extension in Aves is optimized as first present, constitutes the best supported (and most conservative) inference of its point of origin. Avian “automatic” extension may have originated earlier, either associated with the unusual morphologies of metacarpal I seen in Confuciusornis sanctus and enantiornithines, in more basal avialans, or perhaps in nonavialan theropods (Gishlick, 2001); however, this inference awaits further support.

For example, it has so far not been explained how avian automatic extension would have functioned in nonavialan theropods without morphological features that participate in the avian “automated” extension kinematic chain (Vazquez, 1994). These morphologies include a radiale with a depression to receive the end of the radius, a V-shaped ulnare, and anteriorly located humeral condyles. All of these features are present in Apsaravis ukhaana and can be bracketed for at least the Apsaravis + Aves node (e.g., Chiappe, 1996; Sereno and Rao, 1992; Norell and Clarke, 2001; Norell et al., 2001) in addition to the derived metacarpal I process.

That precursors to the avian flight stroke developed in nonflighted outgroups of Avialae makes evolutionary sense. This conclusion is also supported by abundant fossil evidence (e.g., Gauthier and Padian, 1985; Padian and Chiappe, 1999). However, the proposal that specifically the “automatic” extension seen in living birds was present in these taxa (Gishlick, 2001) requires further investigation. In conclusion, we do not propose that the shift to the morphology seen in Apsaravis + Aves node is the “key innovation” in the origin of automatic extension, but that it is this point that is the most justifiable minimal estimate of its origin. Generally, focusing on key innovations may often obscure, more than it illuminates, the complex assembly of avian flight. The inferred “key” points of origin of many such identified novelties are often harder to defend with denser taxon sampling and can appear increasingly like arbitrarily defined points in continuous variation.