Chin. Sci. Bull. csb.scichina.com DOI 10.1007/s11434-014-0669-8 www.springer.com/scp

Article Geology

A new species from an ornithuromorph (Aves: Ornithothoraces) dominated locality of the Jehol Biota

Shuang Zhou • Jingmai K. O’Connor • Min Wang

Received: 10 July 2014 / Accepted: 16 September 2014 Ó Science China Press and Springer-Verlag Berlin Heidelberg 2014

Abstract We report on a new species of ornithuromorph 1 Introduction bird, Iteravis huchzermeyeri gen. et sp. nov., from the previously unreported Sihedang locality of the Lower The Early Cretaceous Jehol Biota in Northeastern China Cretaceous Yixian Formation, the oldest ornithuromorph comprises the most important avifauna in the world, con- bearing deposit in the world. Unlike most other Cretaceous taining the earliest members of every clade of Cretaceous localities, specimens from this new quarry are largely bird including the oldest member of Ornithuromorpha, the referable to Ornithuromorpha, similar to the Lower Cre- derived clade of birds that includes living birds (Neornithes) taceous Aptian Xiagou Formation in Gansu Province. Also [1]. Traditionally, Cretaceous avifaunas are dominated by similar to the Xiagou avifauna, the fauna at Sihedang is Enantiornithes, the sister taxon to Ornithuromorpha and largely dominated by a single taxon (described here). often considered the first major avian radiation [2]. However, Differences in faunal dominance may suggest the Sihedang this successful clade succumbed with other non-neornithine records a unique ecological habitat. This may also explain dinosaurs at the end of the Cretaceous; the underlying causes the dominance of Gansus in the younger Xiagou Formation of their extinction and whether their demise was sudden or locality and suggests that previous hypotheses regarding gradual are unclear. Until now, known localities in the Jehol the shift in dominance between Enantiornithes and Orni- Biota have either been dominated by enantiornithines (not thuromorpha need to be reassessed in terms of potential any one taxa) or Confuciusornis, a beaked basal pygostylian ecological biases due to limited sampling. Furthermore, the bird apparently endemic to the Jehol and the single most recognition of an ornithuromorph dominated locality in the abundant taxon in the avifauna [3, 4]. In contrast, the only Sihedang significantly weakens the signal of such an other avian bearing Early Cretaceous deposits in China, the inferred trend. Compared to most Jehol birds, the new slightly younger Xiagou Formation in Gansu Province, is specimen is relatively better preserved in three dimensions dominated by ornithuromorph specimens largely assignable revealing morphological details of the skeleton, as well as to a single taxon, Gansus yumenensis [5, 6]. Because the preserves feather impressions including a rectricial mor- Xiagou Formation is younger than the Yixian formation, it phology previously unknown among Mesozoic birds. has been suggested that the Xiagou records the shift from enantiornithine to ornithuromorph dominance [7]. Keywords Early Cretaceous Á Sihedang Á The Yixian Formation (125 Ma) records the second Ornithuromorpha Á Aves Á Tail feathers phase of the Jehol Biota and the first appearance datum (FAD) of Ornithuromorpha. Enantiornithes first appears in the slightly older Huajiying Formation (alternatively referred to as the Dabeigou Formation in some early lit- S. Zhou Á J. K. O’Connor (&) Á M. Wang erature), the first phase of the Jehol Biota (130.7 Ma) [8]. Key Laboratory of Vertebrate Evolution and Human Origins The younger Jiufotang Formation (120 Ma) preserves a of Chinese Academy of Sciences, Institute of Vertebrate greater diversity of ornithuromorph taxa compared to the Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China Yixian Formation, although still less than that recognized e-mail: [email protected] for Enantiornithes [1]. The new locality, Sihedang, belongs 123 Chin. Sci. Bull. to the Yixian Formation; located near Lingyuan, western 3 Description Liaoning, this locality has already produced hundreds of turtles and more recently approximately 20 orni- 3.1 Skull thuromorphs, as well as one caudipteryid (Maniraptora: Oviraptorosauria); however, not a single enantiornithine Although the skull is largely complete, preserved in left has yet to be collected (Zhou Z. pers. comm.). Most of the lateral view, overlap of the thin bones from both sides of new ornithuromorphs appear to represent a single new the skull make it difficult to identify some structures and taxon, which we describe here. We investigate this new interpret their details, especially in the caudal region specimen through phylogenetic analysis and discuss the (Fig. 2). The premaxilla appears toothless; the lateral sur- implications of this new locality in regards to earlier face is marked by small but well-defined nutrient foramina. interpretations concerning avifaunal shifts in the The shallow premaxillary corpus is elongate, three times Cretaceous. longer than it is dorsoventrally high, although it is still fairly rostrally restricted contributing to only the rostral third of the facial margin. The rostral margin is gently 2 Systematic paleontology rounded, and the nasal and maxillary processes are nearly parallel. The nasal (frontal) processes are elongate; they are Aves Linnaeus 1758 unfused along most of their length, and the left process is Ornithothoraces Chiappe 1995 missing the caudal half. The distal eighth of the right Ornithuromorpha Chiappe 2002 process is broken and slightly displaced, but we infer they Iteravis huchzermeyeri gen. et sp. nov. would have articulated with the frontals. Just ventral to the distal quarter of this process, a short, broad sheet of bone Holotype IVPP V18958, a nearly complete, articulated ventral may represent the left nasal. The straight maxilla is specimen with feather impressions preserved in a single slightly displaced dorsally; although this element is not slab in dorsolateral view (Fig. 1). well preserved, several teeth are visible intercalating with the dentary teeth. We infer the last maxillary tooth was Locality and horizon Sihedang locality, near Lingyuan, level with the rostral margin of the antorbital fossa. The western Liaoning Province, China; Lower Cretaceous premaxillary ramus of the maxilla is approximately twice Yixian Formation [9]. the length of the jugal ramus, forming the ventral margin of Etymology The name Iteravis (Latin iter—meaning elongate nares. The nasal process is incomplete, but the journey, avis—meaning bird) huchzermeyeri meaning well preserved rostral margin indicates that it would have Huchzermeyer’s journey bird is in honor of the late formed the caudal margin of the external nares. A large archosaur biologist, Dr. Fritz Huchzermeyer, and his end- sheet of bone visible through the external nares appears to less quest for knowledge. be the palatal shelf of the maxilla or the palatine. The exposed ‘dorsal’ surface is concave and appears to be Diagnosis An ornithuromorph bird (predentary bone continuous with the premaxillary ramus of the maxilla present, delicate U-shaped furcula, first phalanx of the supporting the former interpretation. Between the concave major digit expanded, short plow-shaped pygostyle) with palatal shelf and the lateral surface of the premaxillary the unique combination of the following features: pre- ramus, there is located a shallow and caudally tapered maxillary corpus elongate and toothless; maxilla with groove that we infer is for the articulation of the premax- numerous teeth; rostrum 50 % of skull length; ethmoid illa. The region of the antorbital fenestra is not clear, and bone lining rostral half of the orbit; tubercle on caudal the lacrimal bone cannot be clearly identified; however, it margin of minor digit phalanx; pubes with dorsally appears the antorbital fenestra was short, similar to that of expanded distal boot; and narrow ischium with concave Confuciusornis. A very broad and sheet-like bone located ventral margin and weak dorsal process at midpoint. in the rostral third of the orbit and apparently rostrally in Ontogenetic remarks The well ossified periosteal sur- contact with the frontal appears to be an ethmoid bone faces of all the preserved elements and the complete fusion forming a rostrally enclosed interorbital septum. Alterna- of the tibiotarsus and tarsometatarsus indicate that growth tively, this may represent the lacrimal, in which case it was nearly complete, thus the specimen does not represent would represent a very strange hypertrophied and autapo- a juvenile; however, apparent incomplete fusion of the morphic morphology. A trend toward decreasing lacrimal pygostyle, proximal carpometacarpus, and caudal midline size in more derived ornithuromorphs (absent in Neorni- of the sternum indicate that IVPP V18958 was not fully thes) supports interpretations of this bone as the ethmoid. mature. We consider this specimen to represent a near adult The lateral surface bears a slight ridge that extends cau- subadult. dodorsal–cranioventrally (Fig. 2). The jugal is not well 123 Chin. Sci. Bull. preserved, partially obscured by scleral ossicles; it appears The thoracic vertebrae are poorly preserved, obscured to be fairly thin, slightly bowed, and tapered rostrally. The by overlap with other elements (Fig. 1). They are slightly dentary clearly preserves numerous teeth located in indi- shorter than the cervicals, with broad fossae excavating vidual sockets, not a communal row as in Hesperornithi- their lateral surfaces as in other ornithuromorphs [11], and formes. At least ten tightly packed, recurved teeth were amphyplatan articular surfaces. The synsacrum is almost present in the region of the dentary ventral to the pre- entirely covered by other elements. Only the proximal and maxillary ramus of the maxilla. The teeth appear to be distal ends of the synsacrum are visible, revealing a flat fairly high crowned, slightly constricted at the base, and ventral surface and a weakly concave distal articular sur- not strongly compressed mediolaterally. The mandibular face. Although the transverse processes of the proximal symphysis is not formed and a predentary bone is present, sacral vertebrae are laterally oriented, those of the cau- as in other ornithuromorphs [10]. Foramina mark the ros- dalmost vertebra are caudolaterally oriented. tral portion of the dentary ventral to the premaxilla; cau- Five to six free caudal vertebrae are preserved; the dally where teeth are present, foramina are absent proximal and distal vertebrae are interrupted by the over- suggesting a horny sheath (beak) may have been present lying ischium (Fig. 1). The caudals are all small and deli- only on the cranial third of the rostrum. The first preserved cate. The second and third free caudals have long, laterally tooth in the left dentary is level with the rostral margin of directed transverse processes that exceed the width of the the external nares. The T-shaped quadrate is preserved but centrum. The haemel arches appear to be quadrangular and it is not in situ and it is unclear which surface is exposed; plate like. The pygostyle is nearly completely co-ossified. we interpret the bone in lateral view with the quadrate body This element is short and plow-shaped and the length of the directed caudally, which in the preserved view is imper- pygostyle is less than that of the preserved free caudals, as forate and lacks excavation. The ventrally directed ramus in other ornithuromorph birds. Proximally, the pygostyle is would be the lateral mandibular condyle and the dorsal very wide, 50 % the maximum preserved length. The ramus the orbital process. Alternatively, this ‘dorsal ramus’ proximal half of the ventral margin forms a distinct ridge, could be part of the pterygoid. Proximally, the dentary is which may suggest that, in three dimensions, the pygostyle straight; it slopes ventrally just proximal to the articulation was heavily excavated, as in living birds. with the surangular so that if it was forked caudally and a Visible on the left, the vertebral ribs are mostly covered dorsal process was present, it would have been very small. by the sternum; three sternal ribs and one probable uncinate Partial fusion obscures contacts between the postdentary process can also be observed. Several gastralia are pre- bones. The surangular is much shorter than the dentary, and served near the pubes indicative of a small, vestigial gastral the caudal margin appears to be deeply concave. The basket like that in other Early Cretaceous ornithuromorphs; angular appears large, extending dorsally to form the these bones are short, delicate, and rod-like. mandibular articulation. 3.3 Pectoral girdle 3.2 Axial skeleton Only the blades of both scapulae can be observed (Fig. 1); The vertebral column is not well preserved (Fig. 1); the these are curved and tapered distally, as in other orni- axis and atlas cannot be identified. Thirteen articulated thuromorphs. Both coracoids are exposed in ventral view. vertebrae are preserved primarily in ventral view leading The coracoid is strut-like. The length to width ratio is about up to the point at which the series is covered by the pec- 1.4, which is subequal to Yanornis, but much larger than toral girdle. Due to the articulation of the vertebrae, the Archaeorhynchus (1.2), and less than Yixianornis (1.65), morphology of the articular surfaces is unclear; however, Hongshanornis (2.0) and Jianchangornis (1.9). Proximally, their elongate morphology may suggest they were hetero- the acrocoracoid appears to be straight. In three dimen- coelic. The cranial cervical vertebrae are more elongate sions, the ventral surface of the neck of the coracoid is than the caudal ones, their length approximately twice their strongly convex so that the dorsoventral thickness of the width, while the caudal six preserved vertebrae are much coracoid is greatest just below the acrocoracoid; and the shorter, with nearly equal length and width. The cervicals neck quickly flattens toward the sternal margin being have well-developed costal processes that are shorter than nearly flat by the level of the procoracoid. This process is their associated vertebrae and tapered caudally. The tenth short, blunt craniomedially projecting, lacking the medial preserved vertebra has massive carotid processes and the expansion present in Yixianornis. The supracoracoidal two that follow are deeply excavated laterally by pleuro- nerve foramen perforates the medial margin of the neck of cels. No articulated thoracic ribs reveal the position of the the coracoid at the level of the procoracoid process. Dis- cervicothoracic transition, although the tenth preserved tally, the sternal margin is straight with a well-developed cervical has the last clearly visible costal process. sternolateral process, as in other Jehol ornithuromorphs 123 Chin. Sci. Bull.

Fig. 1 Photograph (a) and line drawing (b) of the holotype specimen of Iteravis huchzermeyeri gen. et sp. nov. (IVPP V18958). Scale bar = 1 cm. ca, caudal vertebra; co, coracoid; cv, cervical vertebra; fe, femur; fi, fibula; fu, furcula; gs, gastralia; hu, humerus; il, ilium; is, ischium; md, manual digits; mcI, alular metacarpal; mcII, major metacarpal; mcIII, minor metacarpal; pd, pedal digits; pu, pubis; py, pygostyle; r, radius; sc, scapula; sk, skull; st, sternum; sys, synsacrum; ti, tibia; tmt, tarsometatarsus; tr, thoracic rib; u, ulna; ul, ulnare

123 Chin. Sci. Bull.

(Yanornis, Yixianornis), lacking the cranial hook present in margin of the sternum; distally they are slightly expanded but Gansus. The furcula is U-shaped, lacking a hypocleidium, lack the large fan-shaped distal expansions present in some with an interclavicular angle of approximately 60°, similar taxa (e.g., Yixianornis, Songlingornis). The intermediate to most other Cretaceous ornithuromorphs. The clavicular trabeculae are broken, but a fragment of the left intermediate rami are long and the omal tips are tapered, strongly trabeculae is visible overlying the right tibiotarsus (Fig. 3); it resembling Yanornis and Piscivoravis, and not expanded appears this process was thin and medially curved, enclosing into well-developed articular surfaces for the scapula, as in a large lachriform fenestra, similar to Yixianornis, Yanornis, Archaeorhynchus, or epicledial processes, as in Yixianor- Songlingornis, and Gansus. The xiphial region is broadly nis. The furcula appears to be slightly bowed triangular; the caudal margin of each half of the sternum is dorsoventrally. convex so that the midline bears a short cleft—potentially The sternum is craniocaudally elongate, with a deep keel this is an ontogenetic artifact. extending its entire rostrocaudal length (Figs. 1, 3). The rostral margin is developed into shallow coracoidal sulci, 3.4 Forelimbs which define an acute angle of slightly less than 90° so that the rostral margin is strongly arched, similar to Yixianornis The forelimb is slightly longer than the hindlimb with an in- [11, 12] (Fig. 3). Distinct craniolateral processes are absent, termembral index (humerus ? radius ? carpometacarpus/ although the dorsal surface of the craniolateral margin of the femur ? tibiotarsus ? tarsometatarsus) of 1.016 (Table 1). coracoidal sulcus projects more strongly than the ventral Both forelimbs are complete, but the right humerus is nearly margin, visible on the left; costal facets cannot be observed. entirely covered by the sternum and the left is obscured by Distal to the costal margin, the sternum has a rostrocaudally overlap with the antebrachium. The humerus appears to be long, narrow lateral process (zyphoid process [11]), also slightly shorter than the ulna. The left humerus is preserved in present in Yixianornis [11] and Longicrusavis [13]. The cranial view, and both the proximal and distal ends are poorly narrow rectangular morphology of this process most preserved. The humeral head is domed proximally and resembles that in Longicrusavis. Distally, the lateral tra- reaches further than the proximal margin of the deltopectoral beculae are proportionately short and robust as in most other crest; a well-developed ventral tubercle appears to be present. ornithuromorphs (with the exception of Archaeorhynchus The deltopectoral crest extends the proximal one-third of the and Jiuquanornis), but extend slightly beyond the caudal humerus. Distally, the articular surface is abraded and only the

Fig. 2 Photo of the skull of the holotype of Iteravis huchzermeyeri gen. et sp. nov. (IVPP V18958). an, angular; de, dentary; eb, ethmoid bone; m, maxilla; n, nasal; pm, premaxilla; prd, predentary; qu, quadrate; scl, scleral ossicle; sur, surangular; t, tooth 123 Chin. Sci. Bull.

Fig. 3 Detail photograph (a) and line drawing (b) of the sternum of Iteravis huchzermeyeri gen. et sp. nov (IVPP V18958) and comparison of the sternum of Early Cretaceous ornithuromorphs. c Hongshanornis longicresta, d Longicrusavis houi, e Iteravis huchzermeyeri, f Archaeorhynchus spathula, g Yanornis martini, h Yixianornis grabaui, i Gansus yumenensis. Scale bar = 1 cm. lp, lateral process; it, intermediate trabecula; lt. lateral process; other abbreviations as in Fig. 1 round bulbous dorsal condyle is preserved. A well-developed and U-shaped, well developed into distinct dorsal and ventral flexor process is absent. The left ulna is primarily in dorsal rami that are subequal in length. aspect; it is slightly longer than the radius and appears to be Both hands are preserved in dorsal view (Fig. 1). The nearly straight similar to Gansus, not strongly bowed proxi- carpometacarpus is not completely fused proximally; the mally as in most other Early Cretaceous birds. The proximal major and minor metacarpals appear incompletely fused, and distal ends of the ulna reveal limited anatomical infor- and a hint of the suture between the alular and major mation; the exposed surface of the proximal end of the right metacarpals is still visible. The alular metacarpal is short ulna is deeply concave, probably the ventral cotyla, and a and narrow, slightly more than half the width of the major distinct olecranon process is not visible (Fig. 3). Both ends of metacarpal, with a small extensor process present so that the ulna are rather blunt and slightly expanded relative to the the proximal end is much taller than the distal end. The midpoint the shaft. No remige papillae are visible. The radius articulation with the alular digit appears ginglymous. The is straight and expanded at the distal end apparently forming a major metacarpal is robust and straight; an intermetacarpal tuberculum aponeurosis ventralis separated from the radial- process is absent. The distal end is expanded ventrally, carpal articulation by a tendinal groove. The mid-shaft width crossing the narrow intermetacarpal space to fuse with the of the radius is greater than half that of the ulna, with a minor metacarpal. The straight, narrow minor metacarpal is lachriform cross section. The ulnare is larger than the radiale, shorter than the major metacarpal, with lesser proximal and

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Table 1 Measurements of some skeletal elements of Iteravis huchzermeyeri gen. et sp. nov. (IVPP V 18958) Elements Measurements Elements Measurements

Skull l 46 Minor digit I l 6 Skull h 20 Pubis l 41 Skull l/h 2.3 Pygostyle l Scapula l 35 Femur l 35 Coracoid l 21 Tibiotarsus l 59 W 15 Tarsometatarsus l 31 Humerus l 52 Pedal digit I-1 l 8 Ulna l 53 Pedal digit I-2 l 3 Radius l 49a Pedal digit II-1 l 11a Carpometacarpus l 22 Pedal digit II-2 l 11.5 Alular Metacarpal l 4 Pedal digit II-3 l 4.5 Alular Metacarpal w 2 Pedal digit III-1 l 12 Major Metacarpal l 22 Pedal digit III-2 l 10 Major Metacarpal w 2 Pedal digit III-3 l 8 Minor Metacarpal l 18 Pedal digit III-4 l 4 Minor Metacarpal w 1 Pedal digit IV-1 l 10 Alular digit I l 9.5 Pedal digit IV-2 l 8 Alular digit II l 4 Pedal digit IV-3 l 8 Major digit I l 11.5 Pedal digit IV-4 l 7 Major digit II l 11 Pedal digit IV-5 l 3.5 Major digit III l 3 Forelimb/Hindlimb 127/125 = 1.016 Femur/Tibiotarsus 0.59 Estimated value; l, length; w, width; h, height a Preserved length distal extent, and less than half the width of the major 3.5 Pelvic girdle metacarpal. The distal end is slightly expanded and curved toward the major metacarpal, helping to enclose the narrow The left side of pelvic girdle is preserved in lateral view, and intermetacarpal space. The alular digit is short, not distally the pelvic bones appear well fused at the level of the fully surpassing the distal end of the major metacarpal. The first perforated acetabulum (Fig. 1). The cranial margin of the phalanx is approximately three times longer than the alular ilium is broadly rounded, and the lateral margin between the metacarpal; the ungual phalanx is weakly recurved and proximocranial corner and the acetabulum is concave, larger than that of the major digit. The first phalanx of the defining a weak ventral hook as present in some other orni- major digit is dorsoventrally compressed and caudally thuromorphs (e.g., Schizooura). The preacetabular wing of expanded, as in other ornithuromorph birds, with a well- the ilium is twice as broad as the postacetabular wing; the two developed cranial pila; the second phalanx is of nearly alae are approximately equal in length similar to Gansus but equal length but is much more slender. The minor digit unlike more basal birds in which the preacetabular wing is retains only the first phalanx, the morphology of which is significantly longer than the postacetabular wing (e.g., Ya- an autapomorphy of this species. It is short, approximately nornis). A large but heavily abraded laterally directed anti- half the length of the first phalanx of the major digit. trochanter is present on the caudodorsal margin of the Proximally, it is more than three times its distal width; the acetabulum. A dorsal antitrochanter on the dorsal margin of proximal third appears expanded due to a tubercle on the the ilium was either poorly developed or absent. The proxi- caudal margin. The distal two-thirds of the phalanx are mal 4/5 of the postacetabular wing is strap-like; the distal fifth narrow and the distal end is tapered. The proximal end of the dorsal margin constricts ventrally and tapers to the appears to have formed a wedge-like articulation with the distal end. The ischium is fused to the ilium proximally, but minor metacarpal and the proximocaudal surface of the not distally so that an ilioschiadic foramen is absent. The first phalanx of the major digit, where the caudal surface is ischium is much shorter than the pubis and the triangular not strongly expanded. dorsal process that characterizes some Jehol ornithuromorphs

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(e.g., Yixianornis, Chaoyangia, Gansus) is only weakly and the two condyles appear to slightly taper toward each developed at approximately the midpoint of the bone, similar other. The fibula is just over half the length of the tibiotarsus. to Yanornis. The ischium is broad proximally and sharply Its proximal end is fat and robust, but the shaft tapers quickly, tapered along its distal half; in lateral view, the ventral margin and the distal half of the fibula is thin and delicate. is concave (straighter in Changmaornis) and the bone has a The left tarsometatarsus is preserved in lateral view, while bent appearance, resembling Schizooura [14]. The lateral the right is in dorsomedial view. The tarsometatarsus is surface bears a longitudinal ridge-like muscle scar also completely fused, as in other ornithuromorphs. Metatarsal V present in Yixianornis and Gansus. Proximally, this low ridge is absent. In lateral view, the proximoplantar surface does not is centered on the lateral surface; distally, it becomes con- appear expanded relative to the metatarsal shafts, suggesting tinuous with the dorsal margin where the ischial blade a hypotarsus was absent. The caudal margin of the proximal deflects ventrally. The pubes are more than 50 % longer than articular surface projects beyond the cranial margin so that the ischia and caudally directed. The shaft lacks any lateral the articular surface appears angled similar to some enant- compression and no obturator process is present. The distal iornithines (e.g., Soroavisaurus australis). The proximal ends of the pubes are not preserved in contact, but a medially articular surface of the tarsometatarsus is wider in cross oriented facet clearly visible on the right pubis indicates the section than the combined width of the fused metatarsals so symphysis would have extended for approximately the distal that the tarsometatarsus rapidly narrows below the articular 1/3 of the total length of the pubis, greater than Yixianornis surface. As in other ornithuromorphs, the proximal end of and Gansus but less than Piscivoravis; the distal ends of the metatarsal III is plantarly displaced with respect to metatar- pubes are expanded dorsally forming a distinct pubic boot sals II and IV forming an extensor sulcus that excavates the absent in other ornithuromorphs. proximal third of the dorsal surface; distally, the cranial surface is flat. A distinct tubercle for the attachment of the m. 3.6 Pelvic limb tibialis cranialis muscle is not clearly visible. A proximal vascular foramen perforates the tarsometatarsus between The left femur is preserved in caudolateral view and the right metatarsals III and IV. Metatarsal III is the longest; metatarsal is visible in caudomedial view overlapped by the femur, IV extends farther than the proximal margin of the metatarsal however neither preserves much anatomical information III trochlea, and metatarsal II is the shortest, not extending to (Fig. 1). The femur is much shorter than the tibiotarsus with a the proximal margin of the metatarsal IV trochlea. A distal ratio of approximately 0.60. The femoral head is separated by vascular foramen perforates the tarsometatarsus between a slight neck visible on the left. The trochanteric crest of the metatarsals III and IV. Very tight intermetacarpal incisures femur extends beyond the proximal margin of the femoral extend beyond the proximal margin of the trochlea. The head and curves medially so that its lateral surface is convex. trochlea of metatarsal IV appears enlarged relative to III and Distally, the left femur reveals a single large bulbous lateral II with an angled distal articular surface. The metatarsal II condyle; the fibular trochlea cannot be observed. The cranial trochlea appears to be displaced plantarly with respect to the surface of the right distal femur reveals a well-developed other trochlea. In lateral view, the proximal half of metatarsal patellar sulcus. The tibiotarsus is completely fused and is IV is dorsoplantarly thicker than the caudal half; evidence slightly shorter than twice the length of the tarsometatarsus. A suggests the cross section of the tarsometatarsus was trian- single cnemial crest is clearly visible on the cranial surface, gular with a caudally located apex, which may be interpreted although another laterally positioned crest may also have as a weak lateral plantar crest indicating the proximal half of been present; the craniocaudally expanded portion of the the element was slightly plantarly excavated. The medial cnemial crest is short, limited to the proximal 10 % of the surface of metatarsal II is not clear. The first metatarsal is tibiotarsus. It projects proximally beyond the articular surface small, straight in caudal view, laterally compressed, tapered for approximately 1/3 its length; the cranial surface is convex. proximally, and expanded distally. In medial view, metatarsal Visible on the left tibiotarsus, the cranial cnemial crest dis- I has a curved appearance. Metatarsal I articulates on the tally forms a low ridge that extends to the distal margin of the plantar surface just above the proximal margin of the meta- fibular crest. The fibular crest extends for less than one quarter tarsal II trochlea so that the hallux was fully reversed. the total length of the bone. The combined width of the The pedal digits are long and slender, resembling those of condyles is expanded relative to the width of the shaft. The Gansus, with a pedal phalangeal formula of 2-3-4-5-x; the condyles are large and bulbous, and widely separated by a phalanges have well-formed distal ginglymous trochleae and shallow intercondylar incisure; the extensor sulcus is well distinct pits for the attachment of the collateral ligaments. developed but an ossified supratendinal bridge was absent. The proximal phalanges are longer than the distal ones with The medial condyle is wider than the lateral condyle, as in the exception of the second digit, where the proximal pha- basal birds but opposite the condition observed in some lanx is slightly shorter than the penultimate phalanx. The advanced ornithuromorphs (e.g. Apasavis, Longicursavis); unguals are subequal in size, short, and lacking curvature, as 123 Chin. Sci. Bull. in other Early Cretaceous ornithuromorphs. They have impression, it is difficult to determine whether the ‘‘fork’’ straight to weakly convex dorsal margins and a step-like was composed of multiple rectrices medially separated by a ventral margin, constricted just beyond the flexor tubercle, notch (e.g., Schizooura)[14] and thus a true fork-tail [19], located approximately mid-ungual. The hallux is formed by or if the ‘‘fork’’ was only composed of a pair of short two phalanges; the first is short (approximately twice the rectrices; elongate paired rectrices are fairly common, preserved length of metatarsal I) and slender (half the width being present in Confuciusornis and some enantiornithines of the other pedal phalanges), followed by a claw that (e.g., Protopteryx)[20]. The area surrounding the pygo- appears to be slightly more recurved than that of the other style preserves a large amount of organic carbon—this may pedal digits. Digit II is more robust than the hallux but is be the preserved bulbi rectricium, inferred to be present in delicate compared to digits III and IV; the penultimate ornithuromorphs [11]. This carbonized mass is surrounded phalanx is longer than the first and more slender, and the by a fainter impression that appears to demarcate the out- ungual is the largest in the foot, being approximately equal in line of the soft tissue body; this is in turn lined by short width and height and thus not mediolaterally compressed. body covert feathers along the dorsal margin. Feathers The first phalanx of the third digit is the longest in the foot; potentially lined the ventral margin as well (as in living the non-ungual phalanges decrease in length each by 20 % birds); although not clearly preserved, we suggest they distally. Digit IV is as robust as digit III (often more delicate would have been smaller and shorter than the dorsal co- in contemporaneous taxa) and only slightly shorter than digit verts. The short rectricial feathers protrude from the caudal III so that the foot is asymmetrical, the opposite to the con- margin of the soft body impression, separated at a 50° dition observed in Gansus yumenensis (the length of the digit angle (Fig. 4). If the impression on each side is interpreted III is slightly shorter than the digit IV). The phalanges of the as a single feather as we suggest here, the rectrix feathers fourth digit become increasingly delicate and slender dis- would be approximately comparable to the primary remige tally; the first two phalanges are approximately equal in feathers in mediolateral width. The two feathers are equal length, as are the distal two. The ungual phalanges all bear a in length and mirror images of each other—the medial half pronounced flexor process on the midpoint of the ventral of each feather (or fork of the tail) is tapered along the surface and deep grooves on the lateral surface. The flexor distal 30 % while the lateral edge is straight. This supports process is most developed in the hallucal claw. our interpretation that the length of the feathers is not an artifact of preservation. If our interpretation is correct and 3.7 Gastroliths the tail in Iteravis is formed by two short rectrices pro- truding from the simple covert feathers, this would be the Six gastroliths are preserved near the pelvic girdle in IVPP first documentation of an ornamental tail morphology V18958 (Figs. 1, 3). The stones are large and polished but among Cretaceous ornithuromorphs. not very round or regular, varying in size, morphology, and chemical composition; however, the stones are consistently large, measuring approximately 4–5 mm in diameter. 4 Discussion Although not in situ, the size, number, and morphology of the stones are consistent with their interpretation as gizzard 4.1 Phylogenetic analysis stones [15, 16]. These stones resemble aggregates pre- served in association with some specimens of Gansus (J. In order to determine the relationship of Iteravis relative to O’C. pers. obs.). However, these stones differ from those other ornithuromorphs, we added IVPP V18958 to a large preserved in other Jehol ornithuromorphs Archaeorhynchus cladistic analysis targeted at Mesozoic birds [21]. Using the and Hongshanornis, which are proportionately smaller and TNT software [22], we conducted a heuristic search using more numerous [15, 17]. tree bisection and reconnection (TBR) retaining the single shortest tree out of every 1,000 trees. The first round of 3.8 Soft tissue and integument TBR produced a single tree 847 steps long (Fig. 5a); a second round of TBR produced 9,760 trees one step Feathers are preserved as carbonized traces or imprints shorter. The strict consensus tree (Fig. 5b) is largely con- associated with the wing and tail regions (Figs. 1a, 4). The gruent with previous analyses [23–25], and Ornithotho- feathers appear to be in situ [18]. The primaries are pre- races is resolved without the need to remove taxa (reduced served only as faint impressions with a maximum pre- consensus); some recent analyses have seen a collapse of served length of 10 cm. The specimen seems to have a this clade due to the discovery of very basal orni- short fork-like tail, a morphology that is otherwise thuromorphs that blur the morphological distinction unknown among Early Cretaceous birds. However, because between ornithuromorphs and enantiornithines and are the tail is only preserved as a somewhat incomplete resolved in both clades in different trees of equal length 123 Chin. Sci. Bull.

Fig. 4 Detail photograph and line drawing of the tail of Iteravis huchzermeyeri gen. et sp. nov (IVPP V18958). br, bulb rectricium (organic residue of); cf, covert feathers; rec, rectrix; st, soft tissue body impression; other abbreviations as in Fig. 1. Scale bar = 5mm

(e.g., Chaoyangia, Zhongjianornis). Ornithuromorpha represents the FAD of Ornithuromorpha, strongly suggests forms a basal polytomy that includes Patagopteryx, Ar- a much earlier origination for this clade. The holotype of chaeorhynchus, Schizooura, Piscivoravis, Jianchangornis, Iteravis comes from the new Sihedang locality of the Yixian Chaoyangia, and the clade that includes all more derived Formation that has so far only yielded ornithuromorph taxa. This latter clade is formed by a dichotomy between a birds, and appears dominated by this clade (Zhou Z. pers. Hongshanornithidae ? Songlingornithidae clade and a comm.). Other localities of the Jehol Biota are dominated polytomy between Iteravis, Gansus, Apsaravis, Ambiortus, by Enantiornithes, although not representing a single taxon, Ichthyornis, Limenavis, Enaliornis, Hesperornithiformes, and preserve a more diverse avifauna including basal and Neornithes. This indicates that the new taxon is a fairly pygostylians and sometimes long-tail birds [1]. With the derived ornithuromorph; notably, it is the only Jehol taxon exception of North American transcontinental seaway in this derived polytomy, suggesting Iteravis is the most deposits, Cretaceous localities producing bird fossils are derived ornithuromorph so far uncovered from the Jehol. typically dominated by Enantiornithes. In the Early Creta- ceous, there are only two exceptions; the new Sihedang 4.2 The rise of Ornithuromorpha locality of the Yixian Formation and the Changma locality of the Xiagou Formation [7]. This has lead to interpretations Based on the new specimen IVPP V18958, we erect the that the enantiornithines dominated the Cretaceous and that taxon Iteravis huchzermeyeri gen. et sp. nov., the most the extinction of this clade and other primitive birds helped derived Jehol ornithuromorph uncovered to date, as con- to facilitate the Tertiary radiation of modern birds. Studies firmed by phylogenetic analysis. The fact this specimen have shown that enantiornithines survived up to the KT comes from the Yixian Formation (*125 Ma), which boundary [26]. However, as with other clades of dinosaurs,

123 Chin. Sci. Bull.

Fig. 5 Result of the phylogenetic analysis of Iteravis huchzermeyeri gen. et sp. a The result of the first round of TBR. a single tree with 847 steps long. b Strict consensus cladogram of the 9760 most parsimonious trees (Length 846). CI 0.384, RI 0.662 the enantiornithine record in the latest Cretaceous may Outside the deposits of the Jehol in Northeastern China, suggest that this clade was already in decline prior to the the only other Early Cretaceous avian fossil bearing deposits end Cretaceous event in at least some ecosystems [27]. are of the Xiagou Formation in Gansu Province, Northern

123 Chin. Sci. Bull.

Central China. Although several ornithothoracine species Sihetun near Beipiao) has been interpreted as leks, groups have been described [6, 28–30], these are all known from of males formed during breeding season to attract mates isolated specimens and the great majority of the material [33, 34]. Similarly, the large number of Iteravis from the from this deposit is referable to the ornithuromorph Gansus Sihedang locality may present evidence for some form of yumenensis [5, 7]. This led authors to suggest that the Xia- social behavior such as a breeding colony or migration gou Formation captures an early stage in the shift from the stopover point—many aquatic birds are migratory [35]. Cretaceous dominance of enantiornithines to the rise of The large number of a single species preserved together Ornithuromorpha. However, more accurate dating tech- strongly suggests social behavior for this taxon. Regard- niques now indicate the Xiagou Formation is early Aptian in less, the discovery of this 125 Ma ornithuromorph domi- age (124–120 Ma) [31] and overlaps with the younger Ji- nated locality implies that the success of the ufotang Formation of the Jehol Group. enantiornithines in the Cretaceous may not have neces- The Sihedang locality samples the oldest ornithuromorph sarily been as pervasive as previously inferred. bearing Formation (the Yixian) yet is also dominated by ornithuromorph birds, which apparently represent a single 4.3 Tail feathers taxon, I. huchzermeyeri. There are numerous possible rea- sons for this skewed taxonomic distribution that do not The rectrices preserved in the holotype of Iteravis huch- involve broad evolutionary trends. Ecological differences zermeyeri provide the first potential evidence of a Creta- between specific localities could produce a fauna more ceous ornithuromorph with ornamental tail morphology. heavily dominated by one clade or another. Early Creta- These feathers are much shorter than those preserved in the ceous enantiornithines and ornithuromorphs appear to tail of any other Jehol ornithuromorph bird, which typically occupy different niches, the former being arboreal and the have ‘‘rounded tails’’ formed by six to ten tail feathers, latter—including Iteravis—being largely cursorial with which exceed half the body in length, and form a large aquatic specializations. All Jehol enantiornithines have aerodynamic surface [11, 36]. Although the feathers in large recurved pedal unguals and a relatively long hallux, IVPP V18958—and potentially the entire tail—could be indicative of a foot better adapted for perching, whereas incomplete, the integrity of the soft body impression of the ornithuromorphs have a proportionately longer tarsometa- tail area and the mirror image morphology of the two sides tarsus, shorter and smaller hallux, pedal unguals that of the tail suggest that the length of these feathers is a true decrease in length distally, and small, straight pedal claws, feature. Ornamental tail feathers are common in enantior- features indicative of a foot better adapted for the ground nithines and present in Confuciusornis [37, 38]. However, [23]. Furthermore, Jehol ornithuromorphs typically possess in these birds, the paired tail feathers are elongate, a well-developed proximally projecting cranial cnemial exceeding body length. The shorter rectrices in IVPP crest (also present in Gansus), in living birds associated with V18958 would have generated less drag but also have aquatic environments, and Gansus preserves evidence that formed a much less striking ornament compared to the its toes were webbed like that of extant aquatic and semi- racket plumes in confuciusornithiforms and enantiornith- aquatic birds [7]. The Sihedang locality has also produced a ines [39]. The specimen preserves a dark organic stain large number of aquatic turtles, supporting the inference that concentrated around the pygostyle (Fig. 4) suggesting that this quarry may record a very specific niche occupied by the bulbi rectricium was present. This is consistent with the Iteravis. Enantiornithines are dominant at most localities in derived phylogenetic placement of Iteravis relative to other the Jehol both in diversity and numbers, but this may simply Jehol ornithuromorphs (Fig. 5), which typically preserve a reflect localities that capture the more typical fauna of the rounded tail morphology that would have been aerody- forested (arboreal) paleoenvironment of the Jehol [32]. namically costly without the associated musculature to Gansus and Iteravis are the only taxa known to domi- control its shape. For example, the ability to spread the tail nant Early Cretaceous localities. The two species are during landing and slow flight would greatly increase resolved in a polytomy of taxa more derived than all other maneuverability; however, if the tail could not be folded included Jehol ornithuromorphs. Similarities in gastrolith during normal flight, it would incur a large amount of drag morphology with Gansus, which are larger and less and become detrimental. Therefore, it has been suggested numerous than those found in other Jehol birds, may sug- that the bulbi rectricium co-evolved with the derived short gest that Iteravis may have occupied a niche comparable to and plow-shaped pygostyle and fan-shaped tail observed in that of Gansus and or had a similar lifestyle that facilitated ornithuromorphs [11]. Based on the phylogenetic distri- their preserved dominance in isolated localities. bution of known tail morphologies, we suggest that Iteravis Alternatively, the unusual taxonomic distribution could probably evolved from an ancestor who possessed the bulbi be due to social behavior. The large number of Confuciu- rectricium and a large, fan-shaped array of rectrices, which sornis specimens collected from other localities (e.g., were independently reduced both in length and number in 123 Chin. Sci. Bull. the Iteravis lineage. The tail morphology preserved in 17. 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