Limenavis patagonica, Clarke & Chiappe, 2001

CLARKE, JULIA A. & CHIAPPE, LUIS M., 2001, A New Carinate Bird from the Late Cretaceous of Patagonia (Argentina), American Museum Novitates 3323, pp. 1-24 : 6-14

Limenavis patagonica (new taxon)

HOLOTYPE: Limenavis patagonica , including associated distal portions of a right wing given brief reference in Chiappe (1992b, 1996a). PVL 4731 consists of a portion of the shaft and distal end of the humerus; proximal and distal ends of the ulna; proximal end of the radius; proximal and distal ends of the carpometacarpus; ventral ramus (crus longus) of the ulnare; radiale; most of the proximal phalanx of digit II including the distal end; and several indeterminate fragments. The material is generally unabraded but crushed. The radius is cemented to the humerus, partially obscuring its cranial surface. The proximal carpometacarpus distal to the carpal trochlea of the incorporated semilunate carpal is covered by the attached distal end of the ulna, and the ventral surface is partially obscured by the fragment of the ulnare. The radiale is preserved roughly in articulation with the carpal trochlea.

ETYMOLOGY: Limen, Latin for ‘‘threshhold,’’ avis, Latin for bird, and patagonica , from the provenience of the specimen from northern Patagonia, for the window it offers into the origin of the radiation of the avian crown clade.

LOCALITY AND HORIZON: Salitral Moreno, 20 km south of General Roca, Province of Río Negro, Argentina ( fig. 1 ); Allen Formation, Upper Cretaceous (Campanian–Maastrichtian; Powell, 1987; Heredia and Salgado, 1999).

DIAGNOSIS: Carinate bird with the attachment of the pars ulnaris of the trochlea humeroulnaris on the proximal ulna developed as a pit­shaped fossa, the location of the pisiform process with its proximal surface at approximately the same level as the proximal surface of metacarpal I, and the scar of the ligamentum collaterale ventrale of the ulna proximodistally elongate, extending down the caudal margin of the brachial impression (23:1). These autapomorphies, along with the presence of three other characters with restricted distributions: (1) a well­developed tendinal groove on the ulnare, (2) the deep infratrochlear fossa of the carpometacarpus, and (3) the presence of three fossae on the proximal surface of the dorsal supracondylar process of the humerus, provide a unique suite of characters diagnosing Limenavis patagonica .

ANATOMICAL DESCRIPTION

The humerus is crushed craniocaudally. However, most of its morphology is still

readily discernible ( fig. 2A ). The dorsal and to this larger fossa on the craniodorsal edge ventral condyles are clearly developed on the of the humeral shaft. The more ventral of cranial surface. The dorsal condyle is orient­ these forms a short groove. A similar group­ ed primarily in the long axis of the humerus ing of three fossae occurs in Lithornis cele­ and angling toward the ventral surface. The tius ( YPM­PU 23485), Ichthyornis dispar , ovoid ventral condyle is oriented dorsoven­ Ichthyornis spp. (e.g., YPM 1738, YPM trally at the distal edge of the humerus. In 1447), and Ichthyornis antecessor ( fig. 3 ). Confuciusornis sanctus, Enantiornithes , Pa­ These fossae are especially prominently detagopteryx deferrariisi , Ichthyornis dispar , veloped in the latter taxon and one specimen and modern birds the condyles are similarly of Ichthyornis sp. ( YPM 1447) although they developed cranially (Chiappe, 1996b) and a are present in all Ichthyornis humeri. Brodventrally angled, elongate dorsal condyle is korb (1963) described comparable pits on the present. In enantiornithines, however, the dorsal supracondylar tubercle of the Late ventral condyle developed as a straplike Cretaceous bird, Torotix clemensi , and conridge as opposed to the hemispherical form sidered them peculiarities of the specimen. it has in the other listed taxa. The two proximal fossae were not observed

The measure of the long axis of the dorsal in any crown­clade taxa examined, though condyle is more than the same measure of the single large fossa is present in some exthe ventral condyle as in Confusiusornis tant taxa (e.g., Tinamidae ) ( fig. 3F ). sanctus , Ichthyornis dispar , Ichthyornis spp. The distal end of the dorsal surface of the ( YPM 1738, YPM 1447), and neognaths. humerus of Limenavis patagonica bears two The angle (declination) between the dorsal faint fossae ( fig. 2A, C ). These fossae are humeral margin and the long axis of the dor­ observed in varying degrees of development sal condyle is relatively high compared to in all crown­clade birds considered as well most taxa of the crown clade. It is roughly as in Ichthyornis dispar and Ichthyornis an­ 45° in Limenavis , whereas within the crown tecessor. They are have been identified as the clade, as well as in Confuciusornis sanctus origins of the m. extensor digitorum com­ and Ichthyornis dispar , it more closely ap­ munis and the m. extensor carpi ulnaris proximates 30°. In enantiornithines, it ap­ (Brodkorb, 1963; McKitrick, 1991). proaches 75° to 80°. Proximal to the ventral condyle, on the

The area where the brachial fossa (when cranioventral surface of the humerus, there is present) is developed is largely destroyed by a well­developed, pit­shaped fossa. A small crushing and obscured by the location of the and incompletely preserved facet, or flat, anattached fragment of the radius. No distinct gling bone surface, lies dorsally adjacent and fossa is discernible. However, close to the slightly distal to this fossa. These two feaproximal end of the radial fragment and tures are identified respectively as the attachslightly dorsal to it, there is a small area of ment of the m. pronator superficialis and lig. differently textured bone. The brachial fossa collaterale ventrale (m. pronator brevis and in Ichthyornis dispar and Ichthyornis spp. anterior articular ligament, respectively, sen­ ( YPM 1738, YPM 1447), as well as in some su Howard, 1929). The attachment of the m. crown­clade taxa, is also often not developed pronator superficialis is developed as a small as a fossa, but as a scar. pit­shaped fossa in enantiornithines, Ichthy­

The dorsal supracondylar tubercle of the ornis dispar and Ichthyornis spp. ( YPM humerus is well developed, though not as the 1738, YPM 1447), as well as within the avipointed process seen in Charadriiformes and an crown­clade. While located on the ventral Passeriformes (Baumel and Witmer, 1993). humeral surface in enantiornithines and some Further, although the process is of similar crown­clade taxa, it is developed obliquely proportion to that of other crown­clade birds cranioventrally in I. dispar and other taxa of (e.g., Tinamidae ), it is more cranially rather the crown. than dorsally projected. A shallow circular The flexor process of the humerus is short, fossa is located on the dorsal supracondylar extending less distally than either of the contubercle and opens proximally ( fig. 2A ). Two dyles. The ventral epicondylar surface may smaller fossae lie adjacent and just proximal bear two faint tendinal impressions. However, this area is incompletely preserved. The flexor process is short (as defined above) in Confuciusornis sanctus , I. dispar , and Ichthyornis spp. ( YPM 1447, YPM 1738), as well as in some taxa of the crown clade. In enantiornithines, the whole ventrodistal humeral margin angles farther distally than either of the condyles. The two distal fossae described above are present in both enantiornthines and Confuciusornis sanctus as well as within the avian crown. In enantiornithines, however, these fossae are positioned more ventrally and are aligned proximodistally rather than craniocaudally.

The morphology of the olecranon fossa could not be determined as the caudal surface of the humerus is severely crushed ( fig. 2B ). determine and its excavation is exaggerated It is, however, not strongly developed. There by breakage.

is no evidence of grooves for the m. scapu­ Just caudal and proximal to the area of the lotriceps or the m. scapulohumeralis. In I. ulnar brachial impression lies a well­predispar, the groove for the m. scapulotriceps served, flat, triangular area of textured bone is absent or extremely faintly developed, as that in extant birds marks the insertion of the appears the condition in Confuciusornis san­ lig. collaterale ventrale ( fig. 2A ). In Limetus, enantiornithines as well as the living pa­ navis patagonica , this attachment surface exlaeognath birds. It is clearly indicated in tends along the caudal edge of the brachial most extant neognath birds. impression and up the caudoventral surface The dorsal surface of the ulna is crushed, toward the olecranon. It terminates approxiwhile the ventral surface is relatively undis­ mately at the level of the lip of the ventral torted ( figs. 2D–F ). The olecranon and the cotyla where there is a distinctive circular pit cotylae are well developed. The impression in the approximate location of the insertion of the m. brachialis is also present with an of the pars ulnaris of the trochlea humeroulexcavated lip bounding it caudally. The cra­ naris in extant birds, a ligament that positions nial margin of this impression is difficult to the m. flexor carpi ulnaris (Benz and Zusi, 1982; Baumel and Raikow, 1993). The development of this attachment as a circular pit in Limenavis patagonica is distinct from the poorly defined depression observed in crown­clade taxa.

The olecranon arises directly from the dorsal edge of the ventral cotyla, with the excavation of this cotyla extending three­quarters of the way up the ventral surface of the process ( fig. 2D ). The caudal contact between the ventral cotyla and the olecranon appears concave in proximal view ( fig. 2F ). The ventral cotyla is slightly concave and larger than the flat to slightly convex dorsal cotyla.

In Limenavis , as in Ichthyornis dispar , the dorsal cotyla of the ulna does not appear to project cranially ( fig. 2E ). In contrast, a well­developed process of the dorsal cotyla is present in Patagopteryx deferrariisi (Chiappe, 1996b) and within the crown clade, where it forms a rounded flange. A weak ridge extends distally from the cranial edge of the dorsal cotyla and borders the radial depression. It terminates close to a small fossa, possibly marking the insertion of the m. biceps brachii. This fossa lies in the same position as the bicipital tubercle, the insertion of this muscle in extant birds. The morphology of the radial depression could not be determined.

Distally, the dorsal condyle of the ulna is developed as a semilunate ridge ( fig. 4A ). Its dorsal surface bears a tendinal pit and groove (sensu Howard, 1929) close to the cranial margin, a condition very similar to that of Ichthyornis dispar , Ichthyornis spp. ( YPM 1740, YPM 1462, YPM 1460) and seen in crown­clade birds. The tendinal groove lies distal to the pit and roughly parallel with the edge of the shaft. The pit is somewhat oblong and angles caudally toward the proximal end of the ulna. In enantiornithines, at least one tendinal impression is present.

On the caudal surface of the ulna, the semilunate ridge of the dorsal condyle appears truncated distally ( fig. 4A ). In Ichthyornis dispar , Ichthyornis spp. (e.g., YPM 1740, YPM 1462), enantiornithines, and some taxa of the crown clade this ridge slopes smoothly into the ulnar shaft. The morphology of the ventral condyle is obscured by the carpometacarpus and a fragment of the ulnare ( fig. 4B ). The distal trochlear ridge of the dorsal condyle appears longer transversely across the width of the ulnar shaft than it is in its extent down the caudal margin. In at least some enantiornithines (e.g., PVL 4020, PVL 4032–2) the reverse is true, while in Ichthyornis dispar and Ichthyornis spp. ( YPM 1453, YPM 1740, YPM 1462) these dimensions are subequal. This proportion is vari­ ken. Its proximal surface is approximately able across the crown clade. even with the proximal surface of metacarpal

The radius is preserved in articulation with I. This condition contrasts with that of enanthe distal humerus ( fig. 2A ) and a well­pro­ tiornithines, Ichthyornis spp. ( YPM 1775, jected bicipital tubercle is visible on its ventral YPM 1724), and crown­clade birds surveyed surface. A bicipital tubercle is present in Enan­ in which the proximal surface of the pisiform tiornithes, Patagopteryx deferrariisi , Ichthyor­ process is located conspicuously distal to the nis spp. (e.g., USNM 11641, YPM 1775), Lit­ proximal surface of metacarpal I in ventral hornis plebius , and some crown­clade taxa. view. The pisiform process is often in a dis­ Adjacent to this process is a slight groove, pos­ tinctly more distal position in these taxa; it sibly representing the ligamental papilla (How­ lies at the approximate midpoint of metacarard, 1929), which is developed as a depression pal I, or distal to it. in some crown­clade birds and Ichthyornis spp. Proximocranial to the pisiform process, ( YPM 1741, USNM 11641). there is a slight ridge that borders a deeply

A fragment of the ventral arm (crus lon­ excavated infratrochlear fossa. A shallow gus; Baumel and Witmer, 1993) of the ulnare muscle scar is located proximal and cranial is preserved crushed against the carpometa­ to the ridge. A comparable ridge and promcarpus ( fig. 4B ). A strongly developed lon­ inent infratrochlear fossa are present in Ichgitudinal groove is conspicuous on its con­ thyornis sp. ( YPM 1724) and Lithornis sp. vex and probably ventral (external) surface. ( AMNH 21903), but are uncommon within The development of such a groove varies the crown clade. across modern birds from a barely visible im­ On the dorsal aspect of the carpometacarpression to the deep incision present in the pus ( fig. 4A ), the supratrochlear fossa is a fossil. Enantiornithines have this groove al­ faint, ellipsoidal depression oriented craniothough it is but weakly developed. A well­ caudally and angling slightly proximally as developed groove is present in Lithornis ple­ in enantiornithines, Ichthyornis spp. ( YPM bius ( AMNH 21902). 1775, YPM 1724), Lithornis sp. ( AMNH

The radiale ( fig. 4C ) is somewhat abraded 21903), and crown­clade birds. A distinct but both the articular surfaces (carpal and ra­ notch or fossa just proximal and slightly cradial) seen in crown­clade birds are well­devel­ nial to the supratrochlear fossa is present. oped. A radiale is not preserved in any of the This feature is clearly seen in Ichthyornis sp. Ichthyornis material and although it is known ( YPM 1724) and in crown­clade taxa. It does in some specimens of Confuciusornis sanctus not appear to be present in enantiornithines. and Enantiornithes, little of its morphology In cranial view, metacarpal I has an eloncould be discerned beyond the apparent pres­ gate hourglass shape (i.e., a slightly dorsoence of both of the major articular facets. ventrally expanded extensor process and ar­

Pisiform and extensor processes are pre­ ticular surface for digit I). Metacarpal I is sent on the carpometacarpus of Limenavis also dorsoventrally thin ( fig. 4C ) compared ( fig. 4B ). A pisiform process, while not pre­ to the width of the carpal trochlea in proxisent in Confuciusornis sanctus , is present in mal view. In enantiornithines this metacarpal enantiornithines as well as in carinates. An is almost as wide as the carpal trochlea, extensor process is known only for carinate while in Ichthyornis spp. ( YPM 1775, YPM birds. Although Chiappe (1996b) described a 1724), it is, like Limenavis patagonica , sigsubcircular extensor process for Enantiornit­ nificantly narrower. This width varies across hes, it is the overall shape of the enantior­ modern birds. The distal articular surface of nithine metacarpal I that is best described as this metacarpal (for the first phalanx) is shelfsubcircular. A distinct process projecting like and angles slightly ventrally, as opposed from the proximocranial margin of this meta­ to opening directly distally. carpal is absent in enantiornithines but pre­ Metacarpals II and III are fused distally sent in Ichthyornis sp. ( YPM 1724) and ( figs. 4D–F ). In this region, they are subparcrown­clade birds. The pisiform process is allel, indicating that the intermetacarpal space slightly ovate at its base and angles slightly was probably narrow. The distal shaft of metacraniocaudally. The ventral tip may be bro­ carpal III is oval in cross section at the level of the proximal end of the synostosis. The facets for the proximal phalanges of these metacarpals are equal in distal projection ( fig. 4D ) as in Ichthyornis dispar . In Confuciusornis sanctus , metacarpal III is conspicuously shorter than metacarpal II (Chiappe et al., 1999), while in enantiornithines metacarpal III extends farther distally than metacarpal II (Zhou, 1995). Both conditions are widely distributed in the crown­clade taxa.

There are three visible grooves on the dorsal aspect of the distal metacarpal synostosis ( fig. 4D ). The most cranial of the three is identified as the tendinal groove for the m. extensor digitorum communis and is located on the dorsal surface of metacarpal II. A more caudal groove is probably for the m. interosseus dorsalis (Stegmann, 1978), and a third, in the deep interosseal groove, probably represents that for the m. interosseus palmaris (Stegmann, 1978). These three grooves The proximal phalanx of digit II is exappear in similar topological relations to one panded caudally ( figs. 4G, H ). In dorsal and another in Ichthyornis dispar and Limenavis . ventral views, its cranial and caudal edges Their development and position relative to are parallel for the distalmost 3.3 mm; the one another varies across the crown clade. rest of the caudal edge is broken. The cranial Best seen in distal view ( fig. 4E ), meta­ edge is dorsoventrally convex, flattening carpal II bears a ventrally directed distal pro­ somewhat distally. There is no distal projeccess (Stegmann, 1978; tuberosity of meta­ tion of the caudal edge past the articular surcarpal II sensu Howard, 1929). Another pro­ face. A conspicuous projection of this part of tuberance of comparable development de­ the phalanx, the internal index process (Stegfines the ventrocaudal edge of metacarpal II. mann, 1978), as well as a concave cranial These two ventral projections border a con­ surface, is present in some crown­clade taxa cave surface. These ridges also define a sim­ as well as in Ichthyornis sp. ( YPM 1726).

ilar concave area in Ichthyornis dispar , Ich­

thyornis sp. ( YPM 1724), and some crown­ PHYLOGENETIC RESULTS

clade birds. The distal process in Limenavis

is not, however, the extremely well­devel­ The dataset initially was composed of only oped process seen in Ichthyornis dispar or in the 54 characters from the thoracic limb (apsome crown­clade taxa. pendix 1). The resultant 30 most parsimonious trees (Length: 143 steps, CI: 0.44, RI: 0.52, RC: 0.23), from this preliminary analysis, could be divided into two basic classes of topologies. In one these classes, Limenavis , Ichthyornis , and Lithornis were outgroups of the crown clade, although varying in their placement relative to one another. In the other class of topologies, Limenavis , Ichthyornis , and Lithornis formed a clade with the extant palaeognaths (sometimes clustered with galliforms), that fell as the sister taxon of all neognaths or the nongalliform neognaths, respectively. The strict consensus tree of these fundamental cladograms was completely unresolved. Not surprisingly, a limited set of characters from the thoracic limb does not include synapomophies specifying all well­corroborated relationships (e.g., the monophyly of modern birds and of some traditional ‘‘orders’’). Eighteen additional characters considered by previous authors germane to further resolution of basalmost carinate relationships were added to the analysis (e.g., Houde, 1988; Cracraft, 1988).

The analysis of this expanded dataset resulted in a single most parsimonious tree (Length: 172 steps, CI: 0.47, RI: 0.57, RC: 0.27). In this tree, Limenavis patagonica is the sister taxon of a clade formed by Lithornis and the crown clade ( fig. 5 ), and Ichthyornis is the sister taxon of the clade formed by these carinate taxa. Because the interrelationships of extant avian clades are beyond the scope of this study, the topology of the resultant cladogram, although fully resolved, should not be taken as an explicit hypothesis of their phylogenetic relationships.

In this single tree, state changes in five characters are unambiguously optimized as synapomorphies of Carinatae relative to Enantiornithes ( fig. 5 ). These synapomorphies are as follows: brachial fossa of the humerus (9); one or two fossae on the distal, dorsal surface of the humerus (14); complete proximal and distal fusion of the distal carpals and metacarpals (36); extensor process on metacarpal I (41); and extensor groove on the distal tibiotarsus (64). Although two of these synapomorphies (i.e., 9, 64) are not preserved in the only known specimen and holotype of Limenavis patagonica , the presence of the three remaining synapomorphies place Limenavis closer to Aves than to Enantiornithes.

Two unambiguous synapomorphies indicate that Limenavis is phylogenetically closer to the crown clade than Ichthyornis and thus place it within Carinatae. These synapomorphies are the abruptly truncate contact of the dorsal trochlear surface of the ulna with the ulnar shaft (25), and the loss of a tubercle adjacent to the tendinal groove on the distal ulna (28).

The sister­taxon relationship between Lithornis and the crown clade is supported by only one unambiguous synapomorphy (for which Limenavis preserves the primitive state): metacarpal III extends further distally than does metacarpal II (48).

State changes in six characters are unambiguously optimized as synapomorphies of the crown clade. These synapomorphies include the following: loss of two small fossae on the dorsal supracondylar tubercle of the distal humerus (13); loss of a deeply excavated infratrochlear fossa of the carpometacarpus (37); intermetacarpal process developed as a small tuberculum (45); distalmost caudal margin of phalanx 1, digit II, bowed caudally (54); and loss of a foramen through the coracoid marking the passage of m. supracoracoideus nerve (66). Limenavis has the primitive state for four of these characters (13, 37, 52, 54); the states for the remaining two characters are not preserved in the holotype.

Figures

Fig. 1. Map of Argentina, indicating the locality of Salitral Moreno (Río Negro Province) where the holotype of Limenavis patagonica was collected.

Fig. 2. Limenavis patagonica, holotype (PVL 4731). Right distal humerus attached proximal end of the radius in A, cranial; B, caudal; C, distal views. Right ulna D, ventral; E, dorsal; and F, proximal views. (Casts were used in photographs). bim bicipital impression; bit bicipital tubercle; bri brachial impression; dca dorsal cotyla; dco dorsal condyle; ddf dorsal distal fossae; dst dorsal supracondylar tubercle; hut attachment humeroulnar trochlea; imb impression of m. brachialis; lev attachment lig. collaterale ventrale; ole olecranon; psa m. pronator superficialis attachment; rad radius; vca ventral cotyla; vco ventral condyle; vdf ventral distal fossae.

Fig. 3. Fossae associated with the dorsal supracondylar tubercle in A, Ichthyornis antecessor; B, Ichthyornis sp. (YPM 1447); C, Ichthyornis dispar; D, Lithornis celetius, YPM­PU 23485; E, Limenavis patagonica; F, Tinamus guttatus; G, Crax globulosa; H, Rallus longirostris; I, Burhinus capensis. J, Inset with details of fossae in Lithornis celetius (right) and Limenavis patagonica (left).

Fig. 4. Limenavis patagonica, holotype (PVL 4731). Right proximal carpometacarpus, distal ulna, radiale and ulnare (A–C), right distal carpometacarpus (D–F), and phalanx 1 of right digit II (G–H). A, dorsal view of carpometacarpus, with caudal surface of distal ulna; B, ventral view of carpometacarpus with ventral ramus of ulnare; C, proximal view of carpometacarpus with attached radiale; D, H, dorsal; E, G, distal; and F, ventral views. acf anterior carpal fovea, exp extensor process; fdI articular facet for first phalanx, digit I; fdII articular facet for first phalanx, digit II; fdIII articular facet for first phalanx, digit III; inf infratrochlear fossa; pip pisiform process; rae radiale; ras radial articular surfac; sdc sulcus m. digitorum communis; sid sulcus m. interosseus dorsalis; siv sulcus m. interosseus ventralis; spf supratrochlear fossa; tpg tendinal pit and groove; ule ulnare; uln ulna; vdp ventral distal process; vtg ventral tendinal groove.

Fig. 5. Cladogram depicting the single most parsimonious arrangement of 14 ingroup taxa with Confuciusornis sanctus and Enantiornithes as outgroups (Length: 172, CI: 0.48, RI: 0.57, RC: 0.27). Only autapomorphies for fossil carinates and unambiguous synapomorphies are indicated. Character states optimized as autapomorphies of extant species are not shown.