Journal of Systematic Palaeontology

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First species of from Sihedang elucidates skeletal development in Early enantiornithines

Han Hu & Jingmai K. O'Connor

To cite this article: Han Hu & Jingmai K. O'Connor (2017) First species of Enantiornithes from Sihedang elucidates skeletal development in enantiornithines, Journal of Systematic Palaeontology, 15:11, 909-926, DOI: 10.1080/14772019.2016.1246111 To link to this article: https://doi.org/10.1080/14772019.2016.1246111

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Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tjsp20 Journal of Systematic Palaeontology, 2017 Vol. 15, No. 11, 909–926, http://dx.doi.org/10.1080/14772019.2016.1246111

First species of Enantiornithes from Sihedang elucidates skeletal development in Early Cretaceous enantiornithines Han Hu a,b* and Jingmai K. O’Connora aKey Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 142 Xizhimenwai Street, Beijing 100044, China; bUniversity of Chinese Academy of Sciences, 19A Yuquan Road, Beijing 100049, China (Received 1 April 2016; accepted 19 September 2016; published online 14 November 2016)

The Sihedang locality of the Lower Cretaceous Yixian Formation is the only recognized ornithuromorph-dominated locality in the Jehol Group of north-eastern China. Here we report on the first enantiornithine from this locality and erect a new taxon Monoenantiornis sihedangia gen. et sp. nov. The holotype and only specimen preserves a rare ontogenetic stage in which the intermedium is ossified but free from the other proximal tarsals and the tibia, consistent with the pattern of ossification that occurs in neornithines. In order to explore the pattern of skeletal development in the enantiornithines, we select several published specimens inferred to represent different ontogenetic stages and document their degree of fusion in five key compound bones and the sterna. This provides a preliminary hypothesis for the sequence in which compound bones form in Early Cretaceous enantiornithines. From this hypothesis, most known specimens can be categorized into four major ontogenetic stages: all the compound bones unfused; synsacrum and pygostyle fused; tarsals fused; tibiotarsus and carpometacarpus formed. http://zoobank.org/urn:lsid:zoobank.org:pub:347485CA-87E6-4834-BEB5-687B6798644E Keywords: Aves; Mesozoic; Enantiornithes; ontogeny; skeletal development

Introduction recognizable, such as Longipterygidae, Bohaiornithidae and Pengornithidae (Zhou 2014). The Early Cretaceous Jehol Biota in north-eastern China Recently, a new locality in the Yixian Formation was contains the most diverse recognized Mesozoic avifauna. discovered at Sihedang near Lingyuan, in western Liaon- Thousands of exceptionally preserved fossils have ing. Initial reports described the Sihedang avifauna as been uncovered from these deposits, accounting for half consisting of a single ornithuromorph taxon, Iteravis the known diversity of Mesozoic so far. The Jehol huchzermeyeri (Zhou et al. 2014). This is unusual Biota occurs in the lower Huajiying Formation (130.7 amongst Early Cretaceous localities, in which enantiorni- Ma), the middle Yixian Formation (125 Ma) and the upper thines typically dominate in both numbers and diversity. (120 Ma) (Swisher et al. 2002;He Four additional ornithuromorphs have been reported from et al. 2004, 2006; Zhou 2014), together recording over the Sihedang locality: a new species of (Liu et al. 10 million years of early avian evolution. Enantiornithes 2014) and three longirostrine taxa: Juehuaornis zhangi (Aves: ) is considered to be the dominant (Wang et al. 2015), Dingavis longimaxilla (O’Connor avian clade in the Cretaceous and the first major avian et al. 2016) and Changzuiornis ahgmi (Huang et al. radiation. The horizon of the Huajiying For- 2016). In addition, the holotype of Xinghaiornis lini, mation represents the second oldest known avian-bearing which was initially described as from the Sihetun locality deposit in the world and contains the earliest record of (Wang et al. 2013), may also be from the Sihedang local- the Enantiornithes. It records the first stage with low ity (O’Connor et al. 2016). The only other known orni- diversity in the evolution of the Jehol Biota, with only thuromorph-dominated locality is the Lower Cretaceous two primitive enantiornithines known: Protopteryx and Changma locality of the Xiagou Formation in Gansu, Eopengornis (Zhang & Zhou 2000; Wang et al. 2014). China. From the discovery of the similar Sihedang locality Enantiornithine diversity is much higher in both the youn- in the Yixian Formation, hypotheses regarding avian fau- ger Yixian and Jiufotang formations, with diverse families nal turnover based on the Changma locality likely need to

*Corresponding author. Email: [email protected]

Ó The Trustees of the Natural History Museum, London 2016. All rights reserved.

Published online 14 Nov 2016 910 H. Hu and J. K. O’Connor be reassessed in light of potential ecological differences and minor metacarpals in Pterygornis, but this is thought (Zhou et al. 2014). to be an autapomorphy since it is absent in all other taxa; Here we describe a new fossil bird representing the first Wang et al. 2016), and the major and minor metacarpals enantiornithine reported from the Sihedang locality. The unfused distally, whereas the alular metacarpal is fused to specimen represents a new taxon, Monoenantiornis sihe- the major metacarpal which is fused distally to the minor dangia gen. et sp. nov. We conducted a cladistic analysis metacarpal in ornithuromorphs; the tibiotarsus is fully to determine its phylogenetic position relative to previ- formed; the distal tarsals are fused to the proximal ends of ously known Cretaceous birds. As the first enantiornithine metatarsals II–IV, which are unfused to each other reported from Sihedang, this new specimen provides criti- (O’Connor & Chiappe 2011). Late Cretaceous taxa show cal information regarding the perceived diversity of this increased fusion in certain regions such as the skull, pelvis avifauna. and tarsometatarsus. However, neither a fully fused tarso- The level of skeleton fusion and reduction in modern metatarsus nor a distally fused carpometacarpus is ever birds is much higher than in other groups, having known to occur in any enantiornithine taxa. evolved to reduce weight and reinforce the body for aerial The new specimen described here records a rarely pre- locomotion: skull elements are almost completely fused served and previously undocumented ontogenetic stage, and some are greatly reduced, such as the maxilla, lacri- and thus contributes to our understanding of the sequence mal and postorbital; several thoracic vertebrae fuse into of fusion in the development of compound bones in Early the notarium; thoracic and sacral vertebrae fuse into the Cretaceous enantiornithines. synsacrum; distal caudal vertebrae fuse into the pygostyle; the pelvic bones are fully fused; the sternum consists of a single element; the distal carpals and metacarpals are Institutional abbreviations fused into the carpometacarpus; the proximal tarsals are fused to the tibia forming the tibiotarsus; and the distal BMNH: Beijing Museum of Natural History, Beijing, tarsals are fused to the metatarsals, forming the tarsometa- China; CNU: Capital Normal University, Beijing, China; tarsus. In the postcranial skeleton of some living domestic DNHM: Dalian Natural History Museum, Dalian, Liaon- fowls, the synsacrum is the first element to begin to fuse, ing, China; GMV: National Geological Museum of China, but fusion in this element occurs for a relatively long Beijing, China; IVPP: Institute of Vertebrate Palaeontol- period. The proximal tarsals begin to fuse nearly at the ogy and Palaeoanthropology, Beijing, China; LPM: same time as the synsacrum. Next, the sternum is fused, Liaoning Palaeontology Museum, Shenyang, Liaoning, followed by the formation of the tibiotarsus and the tarso- China; NIGP: Nanjing Institute of Palaeontology and metatarsus. The elements of the carpometacarpus are the Geology, Nanjing, China; STM: Shandong Tianyu last to begin the fusion process (Hogg 1982). Museum of Nature, Shandong, China. All these compound elements are absent in the earliest and basalmost bird, (Andrzej 2002). Skele- tal fusions occur in basal birds in various combinations: Systematic palaeontology the carpometacarpus is partially fused at the proximal end in the long bony-tailed bird (Zhou & Zhang Class Aves Linnaeus, 1758 2002a); the premaxillae are fused to each other, and the Ornithothoraces Chiappe, 1995 scapula and coracoid are fused into the scapulocoracoid Enantiornithes Walker, 1981 in (Chiappe et al. 1999); the pygostyle, Genus Monoenantiornis gen. nov. synsacrum, tibiotarsus, tarsometatarsus and carpometacar- Type species. Monoenantiornis sihedangia sp. nov. pus (alular metacarpal still free) are all formed in Sapeor- nis (Zhou & Zhang 2002b). Compared to these basal Diagnosis. As for the type and only species. lineages that are limited temporally and taxonomically, Derivation of name. Monoenantiornis is composed of the diverse enantiornithine clade shows a broad, general the Greek prefix ‘mono’ (meaning only) and , trend towards increased skeletal fusion that parallels that indicating that it is the first and only enantiornithine from of the Ornithuromorpha (Chiappe et al. 2007; O’Connor the Sihedang locality at the time of publication. 2009; O’Connor et al. 2014), the lineage that includes modern birds. In adult Early Cretaceous enantiornithines, Monoenantiornis sihedangia sp. nov. both the synsacrum and the pygostyle are fully fused; the (Figs 1–7) body and the trabeculae of the sternum are fully fused; the carpometacarpus is partially fused proximally, with Holotype. IVPP V20289, a nearly complete and articu- the semilunate carpal and potentially carpal X fused with lated subadult individual preserved in a single slab in ven- the major and minor metacarpals but the alular metacarpal tral view, only missing some of the vertebrae, the ilia and free (the alular metacarpal is only fused with the major the ischia (Fig. 1; Table 1). New Early Cretaceous enantiornithine bird from China 911

Figure 1. Monoenantiornis sihedangia gen. et sp. nov., IVPP V20289. A, photograph; B, camera lucida drawing. Abbreviations: ap, ascending process of astragalus; ce, cervical vertebrae; co, coracoid; cv, caudal vertebrae; dr, dorsal rib; dt, distal tarsals; fe, femur; fi, fibula; fu, furcula; hu, humerus; il, ilium; mcI–III, metacarpals I–III; md, manual digits; mtI–IV, metatarsals I–IV; pd, pedal digits; pt, proximal tarsals; pu, pubis; py, pygostyle; r, radius; ra, radiale; sc, scapula; se, semilunate carpal; sk, skull; sr, sternal rib; st, sternum; sy, synsacrum; ti, tibia; tv, thoracic vertebrae; u, ulna; ul, ulnare; up, uncinate process.

Derivation of name. The species name refers to the of the cranial surface; foot with extremely robust digit II Sihedang locality, where the holotype was collected. and delicate digit IV.

Occurrence. Sihedang locality, near Lingyuan, Liaon- Differential diagnosis. ThenewtaxonisreferredtoEnan- ing, China; Lower Cretaceous Yixian Formation. tiornithes and can be easily distinguished from other enan- tiornithine taxa, with the exception of the bohaiornithids. Diagnosis. A medium to large-sized enantiornithine bird The holotype specimen IVPP V20289 is only slightly characterized by the following unique combination of smaller than the bohaiornithids (a factor that could change morphological features: small teeth with unrecurved and with ontogeny), and bears several morphological similarities pointed apices; premaxillary teeth with grooves on the lin- to them. The strong lateral projection of the lateral trabecu- gual side; sternum with a narrowly vaulted rostral margin; lae of sternum is present in both IVPP V20289 and bohaior- lateral trabeculae directed caudolaterally and terminating nithids, but absent in all the other enantiornithines. Besides cranial to the distal end of the xiphoid process; furcular this, IVPP V20289 shares a number of additional morpho- articular surface of scapula large and triangle-shaped; dis- logical features with bohaiornithids including: pygostyle tal half of the lateral margin of the coracoid corpus tapered without abrupt distal constriction; pedal digit II strongly convex; extension of the minor metacarpal much more robust than other digits; and pedal digit IV beyond the distal end of the major metacarpal more than much more delicate than all other non-ungual pedal phalan- 15% the length of the latter (autapomorphy); single and ges (Wang et al. 2014b). However, detailed comparisons low cnemial crest on tibia present along the proximal 30% can distinguish IVPP V20289 from bohaiornithids and other 912 H. Hu and J. K. O’Connor

Table 1. Measurements (in mm) of the holotype of Monoenantiornis sihedangia gen. et sp. nov., IVPP V20289. Abbreviations: l, left; r, right; Ã indicates preserved length; ÃÃ indicates estimated length.

Element Measurement Element Measurement

Skull length 35.1Ã Femur length (r) 38.5 Pygostyle length 17.3Ã Tibia length (r) 45.5 Sternum width 28.8 Fibula length (r) 39.5Ã Sternum, lateral trabecula length (l) 8.0 Metatarsal I length (l) 5.3Ã Scapula length (r) 37.1ÃÃ Metatarsal II length (l) 18.8Ã Coracoid length (r) 24.4 Metatarsal III length (l) 20.4Ã Humerus length (r) 45.1 Metatarsal IV length (l) 18.4Ã Humerus, midshaft width (r) 4.6 Pedal phalanx I–1 length (l) 6.4 Ulna length (r) 45.6 Pedal phalanx I–2 length (r) 9.1 Ulna, midshaft width (r) 4.0 Pedal phalanx II–1 length (l) 5.7 Radius length (l) 43.3 Pedal phalanx II–2 length (l) 7.9 Radius, midshaft width (r) 2.0 Pedal phalanx II–3 length (l) 11.2 Alular metacarpal length (l) 5.0ÃÃ Pedal phalanx III–1 length (l) 7.5 Major metacarpal length (l) 19.2 Pedal phalanx III–2 length (l) 7.2 Minor metacarpal length (l) 20.0 Pedal phalanx III–3 length (l) 6.5 Alular phalanx–1 length (l) 7.1 Pedal phalanx III–4 length (l) 9.9Ã Alular phalanx–2 length (l) 4.2 Pedal phalanx IV–1 length (l) 4.3 Major phalanx–1 length (l) 10.8 Pedal phalanx IV–2 length (l) 3.0 Major phalanx–2 length (l) 11.2 Pedal phalanx IV–3 length (l) 3.4 Major phalanx–3 length (l) 4.0 Pedal phalanx IV–4 length (l) 2.4 Pubis length (l) 35.5Ã Pedal phalanx IV–5 length (l) 6.4Ã enantiornithines easily. The rostral margin of the sternum of in IVPP V20289, 48 mm in Pengornis houi IVPP V15336 IVPP V20289 is narrowly vaulted, rather than broad or (Zhou et al. 2008), 39.8 mm in Parapengornis eurycauda- rounded as in most enantiornithines including bohaiorni- tus IVPP V18687 (Hu et al. 2015) and 39 mm in Bohaior- thids, although it is somewhat similar to (Wang nis guoi LPM B00167 (Hu et al. 2011)), and larger than &Liu2016). Apart from the sternal morphology, the teeth most other previously described Early Cretaceous enan- of IVPP V20289 are smaller than the typical robust teeth of tiornithines, despite its ontogenetic immaturity. the bohaiornithids. The premaxillary teeth preserve grooves on the lingual side, which resemble only those of Sulcavis, Skull and mandibles. The skull of Monoenantiornis but differ from the latter in the morphology of the grooves. IVPP V20289 is exposed partially disarticulated in ventro- The minor metacarpal extends farther distally than the major lateral view (Fig. 2). Most elements are badly crushed, metacarpal, and much farther than in other enantiornithines severely limiting available anatomical information. according to the ratio of surpassing length to the major Although slightly disarticulated from other elements, metacarpal length. IVPP V20289 also preserves some fea- the premaxillae are preserved articulated, with only the tures that are rarely seen in other known enantiornithines, right corpus exposed, suggesting their corpora may be such as the large and triangle-shaped furcular articular sur- partially fused, similar to those of Longusunguis (Wang face of the scapula and the tibial cnemial crest. These char- et al. 2014b). The dorsal and ventral margins of the pre- acters are not considered subject to ontogenetic change at maxillae define an angle of approximately 35. Visible on this fairly late stage in development. the right, a small foramen is present at the base of the frontal process, similar to Archaeopteryx (Rauhut 2014) and unique to other early birds. Two broken teeth are pre- Description served in the right premaxillary, and three are preserved The following description is based on the anatomy of in the left with their lingual surfaces exposed. The apices IVPP V20289, which is preserved primarily in ventral of the premaxillary teeth are pointed and nearly unrec- view. Anatomical terminology primarily follows Baumel urved. They are similar to other enantiornithines in size & Witmer (1993), using the English equivalents of the (0.68 mm in width), and smaller than the robust teeth of Latinized osteological features. This specimen is smaller the similar body-sized bohaiornithids (Wang et al. than Pengornis houi in size, similar to bohaiornithids and 2014b). However, the midcrown length of the teeth is smaller pengornithids (Table 1; length of femur 38.5 mm larger than the crown-base length, which is similar to New Early Cretaceous enantiornithine bird from China 913

dorsolateral margin of the eye socket. A narrow and strap- like bone overlapped by the frontal may represent the right nasal, revealing that the caudal margin was tapered and that the element appears elongate and narrow. The right parietal is exposed in ventral view; it is concave and quadrangular, as in other avian taxa. Only the left quadrate of the new specimen is pre- served. The otic process is long and straight, similar to chaoyangensis (Zhang et al. 2001) and Para- pengornis eurycaudatus (Hu et al. 2015), contrasting with the bowed condition in some other enantiornithines, for example, pani (O’Connor et al. 2011a), Long- irostravis hani (Hou et al. 2004), buhleri (Hou et al. 1999), Pengornis houi (Zhou et al. 2008) and Eopengornis martini (Wang et al. 2014). The orbital pro- cess is abraded. No pneumaticity is present, whereas a caudal foramen is visible in Shenqiornis and Pengornis (O’Connor & Chiappe 2011). The mandibular articulation appears to be formed by two transversely aligned con- dyles, the medial of which is larger in size. The mandibular elements are slightly disarticulated and ventrolaterally exposed. The rostral ends of the dentaries are blunt and unfused. Five teeth are preserved in the right dentary and three in the left. They are similar to the pre- maxillary teeth in size and morphology, although the lin- gual surface is not exposed in any of the dentary teeth. Two robust postdentary elements are symmetrically pre- Figure 2. Skull of Monoenantiornis sihedangia gen. et sp. nov., served, and slightly ventrocaudally displaced away from IVPP V20289. A, photograph; B, camera lucida drawing. Abbre- the dentaries. The rostral portion in each bone slightly viations: de, dentary; fr, frontal; hy, hyoid; ma, maxilla; na, curves dorsally, and the dorsoventral height of each bone nasal; pa, parietal; pm, premaxilla; qu, quadrate; su, surangular; v, vomer. is subequal to that of the dentary. They are supposed to represent the surangular and angular on the right and only the angular on the left, but the preservation is too poor to bohaiornithids. Similar to Sulcavis, the lingual surfaces of determine that. An extremely delicate bone below the sur- the new specimen are flat and bear enamel grooves or angular is identified as one of the hyoid bones. flutes, representing the second occurrence of such a fea- ture reported in birds (O’Connor et al. 2013). The enamel Vertebral column and ribs. The entire vertebral column grooves in Sulcavis radiate from the apex, whereas they is poorly preserved. Approximately seven badly crushed are shallower and orientated parallel to each other in cervical vertebrae are preserved in articulation with the IVPP V20289 (Fig. 3). Only the apex of the second pre- skull. Two thoracic vertebrae are identified near the fur- served left premaxillary tooth is exposed, suggesting that cula, as well as three more exposed through the breaks in it may have recently erupted. At least two tiny teeth are the sternum, and a sixth isolated thoracic preserved near preserved in the right maxilla. The premaxillary ramus of the caudal margin of the sternum. These thoracics all pos- the maxilla is shorter than the jugal ramus, and the broken sess spool-shaped vertebral bodies, with amphyplatan ascending process is overlapped by the frontal. articular surfaces much larger than the vertebral foramen. The frontals are preserved in ventral view, and appear The length-to-width ratio of the cranialmost preserved entirely fused medially. With its fairly poor preservation, thoracic vertebral body is approximately 1.45. Visible in the fusion could be a taphonomic effect. The frontals are the thoracic preserved just below the furcula, the lateral narrow rostrally and expanded caudally, as in other birds surface is deeply excavated by a groove, as in other enan- (O’Connor & Chiappe 2011). The ventrolateral margins tiornithines (Chiappe & Walker 2002). are concave and notably thickened, forming the rounded The ventrally exposed synsacrum is nearly complete; dorsal margin of the orbit. The medial extensions of the the caudal half is crushed and obscured by other elements. ventrolateral prominences end abruptly, medially sepa- We estimate seven vertebrae are present, as in Protopteryx rated by a deep, flat valley. This morphology is widely (Zhang & Zhou 2000), Pengornis (Zhou et al. 2008) and observed in living birds, and inferred to form the Parabohaiornis (Wang et al. 2014b), compared to the 914 H. Hu and J. K. O’Connor

Figure 3. Details of the tooth with grooves in A, Monoenantiornis sihedangia gen. et sp. nov.; B, Sulcavis geeorum, BMNH Ph–000805. typical eight fused sacrals present in (Sereno and appears to taper gently distally, reminiscent of et al. 2002), (Sereno 2000), Longipteryx bohaiornithids, compared to the abrupt distal constriction (Zhang et al. 2001), Vescornis (Zhang et al. 2004), Rapax- present in many other enantiornithines such as Rapaxavis, avis (O’Connor et al. 2011a) and Parapengornis (Hu et al. Shanweiniao, and Halimornis (Chiappe et al. 2014). Fusion between the sacrals is nearly complete, with 2002; O’Connor et al. 2009, 2011a, b; Wang et al. sutures faintly visible. The cranial articular surface of the 2014b). A fragment preserved near the pygostyle is inter- first sacral is very slightly concave and mediolaterally preted as the craniodorsal fork that is typical of the enan- wider than dorsoventrally tall. The entire ventral surface tiornithine pygostyle (Chiappe et al. 2002). bears a longitudinal sulcus. The transverse processes are Approximately four or five robust sternal ribs articulate distally expanded, and the processes in the last sacral are on each side of the sternum. Preservation and overlap with strongly directed caudolaterally, similar to bohaiornithids, thoracic ribs prevents determining the exact number. Sev- whereas they are laterally directed in pengornithids and eral disarticulated long and curved dorsal ribs are preserved longipterygids (Wang et al. 2014). just distal to the sternal ribs. Alongside them, a few shorter Two poorly preserved elements located distal to the elements are preserved. They are expanded at one end and synsacrum are interpreted as caudal vertebrae. Another probably represent unfused uncinate processes. caudal with ventrolaterally directed transverse processes is preserved proximal to the pygostyle. The fully fused Sternum. Although overall poorly preserved, the ster- pygostyle is exposed in left lateral view. It measures num of Monoenantiornis IVPP V20289 reveals a mor- 17.3 mm as preserved, missing the distal end. The phology that is unique amongst enantiornithines (Figs 4, exposed left ventrolateral process is thickest proximally 5). Although somewhat obscured by the sternal margin of New Early Cretaceous enantiornithine bird from China 915

Figure 4. Monoenantiornis sihedangia gen. et sp. nov., IVPP V20289; detailed photographs and line drawings of A, B, sternum; C, D, metacarpals. Scale bars D 5 mm. the coracoids, the rostral margin appears narrowly 2016). Since the distal expansions of the lateral trabeculae vaulted, similar to Cathayornis (Wang & Liu 2016), ossify late during the sternal development (O’Connor whereas it is broad and rounded in most enantiornithines 2009; O’Connor et al. 2015) and the new specimen is a (e.g. Protopteryx Zhang & Zhou 2000), pengornithids subadult individual, distal expansions may potentially (Wang et al. 2014) and longipterygids (O’Connor et al. have been unossified at the time of death. This could 2009). The trabeculae are strongly directed caudolaterally, potentially explain the relative brevity of the lateral pro- approximately defining a 20 angle with the longitudinal cesses in IVPP V20289 compared to other enantiorni- axis of the sternum, which is similar only to bohaiorni- thines. In this specimen, the trabeculae terminate cranial thids amongst enantiornithines (Wang et al. 2014b). The to the caudal margin of the xiphoid process and only form distal ends of the lateral trabeculae lack the expansions 47% of the length of the lateral margin, proportionately typical of other enantiornithines, such as the slight expan- less than in most enantiornithines (e.g. approximately sions in primitive enantiornithines Protopteryx (Zhang & 59% in Rapaxavis, 56% in Longipteryx and 76% in Para- Zhou 2000) and the pengornithids (Wang et al. 2014), or pengornis). The intermediate trabeculae are weakly devel- the large expansions in bohaiornithids (Wang et al. oped as in Longipteryx (Zhang et al. 2001) and 2014b), Longipteryx (Zhang et al. 2001), Rapaxavis Eocathayornis (Zhou 2002), whereas they are more (O’Connor et al. 2011a) and Cathayornis (Wang & Liu strongly developed in most other enantiornithines 916 H. Hu and J. K. O’Connor

Figure 5. Comparative sternal morphology of Monoenantiornis sihedangia gen. et sp. nov., IVPP V20289 and selected enantiornithines. A, Monoenantiornis sihedangia, IVPP V20289, photograph; B, reconstruction of Monoenantiornis sihedangia; C, Longipteryx chaoyan- gensis; D, Parabohaiornis martini; E, Cathayornis yandica; F, Monoenantiornis sihedangia; G, Protopteryx fengningsis; H, Parapen- gornis eurycaudatus; I, Shanweiniao cooperorum; J, Dunhuangia cuii. including the bohaiornithids (Wang et al. 2014b) and (Sanz et al. 1996; Zhang et al. 2004). Although missing, a Longirostravis (Hou et al. 2004); notably these processes hypocleidium is inferred to be present based on the cau- are absent in pengornithids (Wang et al. 2014). The dally elongated morphology of the symphysis. The clavic- median trabeculae form an elongate xiphoid process as in ular rami are straight and slender. The omal articular most enantiornithines, except Protopteryx and the pengor- surface is only preserved on the left, and is obscured by nithids (Wang et al. 2014). A well-ossified keel extends abrasion. along the caudal three-fifths of the sternal ventral midline. It gradually reaches its maximum height in the proximal Fore limb. The nearly complete and articulated fore third of its length, and then maintains a fairly even height limbs are slightly longer than the hind limbs, with an C C distally. intermembral index of 1.05 (humerus ulna major metacarpal / femur C tibia C metatarsal III). Both humeri Pectoral girdle. Both scapulae are largely covered by the are exposed in cranial view, and are subequal to the ulnae coracoids and sternum. The distal half of the right scapu- in length (Table 1). The proximal margin of the right lar corpus is visible through a break in the sternum indi- humeral head is slightly abraded, but the typical enantior- cating that the scapula is straight, weakly tapered distally, nithine profile can be observed (Chiappe & Walker 2002). and shorter than the humerus (Table 1). The elongate The furrow below the proximal margin is more likely to acromion process is exposed on both sides but most be due to preservation, rather than representing a trans- clearly on the right. The furcular articular surface is large verse ligamental groove. The ventral tubercle is well and triangular. The coracoidal tubercle is not developed, developed and projects ventrally, similar to the ornithuro- as in other Early Cretaceous enantiornithines. morph Schizooura (Zhou et al. 2012). The bicipital crest The ventrally exposed coracoids are strut-like. The is weakly developed on the cranial surface. The dorsal acrocoracoid process is rounded and a procoracoid pro- height of the deltopectoral crest is less than the dorsoven- cess is absent, as in most other enantiornithines. Both the tral thickness of the humeral shaft. The crest extends less medial and lateral margins of the corpus are concave than one-third the length of the humerus, with an abrupt proximally but convex distally, making the straight sternal distal margin. The distal margin of the humerus is angled margin mediolaterally expanded, similar to bohaiorni- ventrally and a blunt flexor process present. The dorsal thids. Visible on the left, the supracoracoidal nerve fora- and ventral epicondyles are weakly developed, as in most men pierces the neck, separated from the medial margin Early Cretaceous enantiornithines. by a thin bony bar. The ulna is robust with a midshaft width twice that of The furcula is Y-shaped, with an interclavicular angle the radius, a measurement possibly exaggerated by crush- of approximately 60, similar to that of pengornithids, ing of the ulna. It is bowed proximally as in other enan- Protopteryx and Longipteryx (Zhang & Zhou 2000; Zhang tiornithines (Chiappe & Walker 2002). The distal et al. 2001; Wang et al. 2014), but wider than observed in condyles are well developed, extending onto the cranial other enantiornithines, such as and Vescornis surface, and separated by an intercondylar insisure. In the New Early Cretaceous enantiornithine bird from China 917 preserved aspect, the ulnare and the radiale are roughly than the femur. The pubic symphysis is poorly preserved, subequal in size. Visible on the left, the carpometacarpus but it appears to be expanded and limited to the distal end is entirely unfused. of the pubis. The alular metacarpal is craniocaudally thinner than the major metacarpal and approximately 26% of the proximo- Hind limb. Both hind limbs are complete and articulated, distal length of the latter, as in most basal birds such as only missing the proximal end of the right metatarsus. The Jeholornis, , Cathayornis and Eoenantiornis proximal portions of the femora are overlapped by pelvic (Hou et al. 1999; O’Connor & Sullivan 2014). The major elements. The femoral head is visible on the right, and metacarpal is robust and straight. The minor metacarpal is reveals no pit-shaped fossa for the capital ligament. The craniocaudally much thinner than the major metacarpal, femur is nearly straight and measures 85% of the length but similarly wide in ventral view, as in many enantiorni- of the tibia, similar to most enantiornithines, for example, thines. The slightly bowed metacarpal bears a concave Rapaxavis (81%; O’Connor et al. 2011a), Longirostravis cranial surface, and extends beyond the distal margin of (78%; Hou et al. 2004), Sulcavis (87%; O’Connor et al. the major metacarpal as in other enantiornithines 2013) and Bohaiornis (85%; Hu et al. 2011), but less than (Chiappe & Walker 2002). The ratio of the surpassing the pengornithids (more than 90%; Hu et al. 2015). A length of the minor metacarpal relative to the total length patellar groove is not developed on the distal cranial of the major metacarpal is approximately 16% (left side) surface. in IVPP V20289 (Fig. 4), which is much larger than A small cnemial crest is present on both tibiae, resem- observed in other enantiornithines (e.g. 4% in Rapaxavis, bling that of Soroavisaurus (Chiappe & Walker 2002); 7% in Pengornis,7.5%inBohaiornis and 8% in Longip- this feature is not commonly preserved in Early Creta- teryx)(Fig. 6). ceous enantiornithines. The cnemial crest of IVPP The alular digit terminates level with the distal end of V20289 is developed on the craniolateral border of the the major metacarpal. The alular ungual phalanx is tibia, and extends approximately 30% the length of the roughly subequal to that of the major digit in size, but the tibia. The fibular crest is separated from the proximal end ungual of the major digit is more strongly recurved. Both of the tibia, and extends less than one-third of its total the first and second phalanges of the major digit are slen- length. The fibula is half the length of the tibia and tapers der, with the latter slightly shorter than the former, as in rapidly, making its distal half splint-like. Visible on the most enantiornithines except for Protopteryx (Zhang & left, the astragalus and the calcaneum are preserved in situ Zhou 2000). The left minor digit consists of a single non- and fused to each other, but unfused to the tibia. The inter- ungual phalanx, which is hollow as indicated from medium forms an ascending process that is broad and sub- breakage. triangular like that of Archaeopteryx and nonavian theropod (Mayr et al. 2005). This element is Pelvic girdle. The pelvic elements of the new specimen preserved free from the fused astragalus and calcaneum, are unfused and dorsoventrally crushed; only the pubes capturing a rare stage in the formation of the tibiotarsus are informative. They are robust, rod-like, and shorter (Ossa-Fuentes et al. 2015). A circular pit is centred on the

Figure 6. Comparison of the metacarpals of Monoenantiornis sihedangia gen. et sp. nov., IVPP V20289 and selected enantiornithines. A, IVPP V20289 (right); B, IVPP V20289 (left); C, Sulcavis geeorum; D, Longipteryx chaoyangensis; E, Rapaxavis pani; F, Fortungua- vis xiaotaizicus; G, Pengornis houi; H, Bohaiornis guoi. Scale bars D 5 mm. 918 H. Hu and J. K. O’Connor

ginglymous, and the right metatarsal III preserves a well- developed ligamental pit visible on the medial surface of the trochlea. The hallux is short, with a robust claw slightly longer than the first phalanx. Digit III is the longest digit in the foot, while digits II and IV are nearly equal in length. Digit II is much more robust than the other digits, similar to bohaiornithids amongst enantiornithines (Wang et al. 2014b), but more strongly developed in the new taxon (the width ratio of the proximal phalanx of digit II is 1.5 to that of digit III, and 2.7 to digit IV). The proximal pha- lanx of digit II is shorter than the penultimate phalanx, which is subequal in length to the proximal phalanx in digit III but much wider. Digit IV is significantly more delicate than digits II and III, also similar to the bohaiorni- thids (Wang et al. 2014b). The proximal and penultimate phalanges in digit IV are approximately subequal in length but the distal phalanx is much more delicate; the second and third phalanges are shorter and also approxi- mately subequal in length. The ungual phalanges in digits II and III are subequal in length and slightly longer than that in digit I, whereas the digit IV ungual phalanx is sig- nificantly smaller. The ungual phalanges in digits I and II are significantly taller dorsoventrally at the proximal artic- Figure 7. Detailed photographs and line drawings of the feet of ular surface, and overall more robust than those of digits Monoenantiornis sihedangia, IVPP V20289. A, right foot photo- III and IV. All unguals bear well-developed ligamental graph; B, right foot line drawing; C, left foot photograph; D, left grooves on the lateral surfaces, but lack well-developed foot line drawing. Abbreviations: mtI–IV, metatarsals I–IV. flexor tubercles (only weakly developed in the hallucal D Scale bar 5 mm. claw). medial surface of the medial condyle, similar to Qiliania Plumage. The new specimen poorly preserves remnants (You et al. 2005). The distal tarsals on the left are fused to of body on the skull, neck, and tibiotarsus, and each other, but unfused to the metatarsals. the remiges associated with the fore limbs. Notably, the Metatarsals II–IV are unfused in IVPP V20289 (Fig. 7). body feathers on the head do not extend onto the rostrum, The J-shaped metatarsal I measures 26% of the length of and the crural feathers do not extend beyond the ankle metatarsal III, comparable to most enantiornithines with joint, as in other enantiornithines. the exception of the pengornithids (Hu et al. 2015). The articular surface for the hallucal digit is perpendicular to that of metatarsal II so that the hallux is fully reversed. Discussion The trochlear extension of metatarsal I is nearly as long as the articulation with metatarsal II. Metatarsals II–IV are Histology straight. Metatarsals III and IV appear subequal in length The midshaft portions of the right ulna and a dorsal rib, and slightly longer than metatarsal II, so the trochlea of the distal end of a sternal rib, and the proximal end of the metatarsal II terminates above the trochlea of metatarsals right pubis were sampled for histological analysis. All the III and IV, which as preserved terminate nearly at the samples were embedded, dried, cut and polished follow- same level. This morphology is different from other enan- ing the methodology and terminology of Chinsamy tiornithines (Chiappe & Walker 2002), but due to the poor (2005). The pubis sample turned out to be completely preservation of the proximal portion and slight disarticula- recrystallized and the dorsal rib sample heavily damaged, tion of the metatarsals, it cannot be confirmed as an auta- so that neither sample is informative. pomorphy of Monoenantiornis sihedangia. Metatarsal IV The cortex of the ulna consists nearly entirely of is narrower than metatarsals II and III throughout its woven-textured bone tissue. A very thin inner circumfer- length as in other enantiornithines (Chiappe & Walker ential layer (ICL) is visible, consisting of endosteally 2002). Metatarsal II is considerably more robust than derived avascular lamellar bone (Fig. 8A, B). The osteo- metatarsals III and IV as in bohaiornithids (Wang et al. cyte lacunae in the ICL are flattened, typical of lamellar 2014b). The trochlea of metatarsals II and III are bone. The ICL is not completely continuous around the New Early Cretaceous enantiornithine bird from China 919

Figure 8. Ulna and sternal rib histology of Monoenantiornis sihedangia gen. et sp. nov., IVPP V20289. A, complete section of the right ulna; B, detailed structure of region framed in A; C, complete section of the sternal rib; D, detailed structure of region framed in C. Abbreviation: ICL, inner circumferential layer. medullary surface, which may be due to poor preserva- are nearly fully fused into the synsacrum; the ossified ster- tion. Although no distinctive outer circumferential layer num consists of a single element; and the distal caudal ver- (OCL) is developed, the compacta (excluding the ICL) tebrae are fully fused into the pygostyle. In addition, with can be easily distinguished into two regions: a thick mid- the exception of the sternal margins of the coracoids, which dle region with globular and haphazardly arranged osteo- are slightly porous, the periosteal surfaces in most elements cyte lacunae, and abundant large longitudinal canals; and are well ossified. Based on the combination of these fea- a nearly avascular outer region with flattened osteocyte tures, we consider the specimen to be a subadult and not a lacunae organized in parallel. No secondary osteons or juvenile. At this ontogenetic stage, although some features lines of arrested growth (LAG) are visible. are prone to change (e.g. sternum), others already show sta- The sternal rib section is thin and crushed, different ble adult morphology (e.g. pedal morphology) and can be from the ulna section in that it is nearly avascular with no used to justify the erection of a new taxon. LAGs or visible stratification of any kind (Fig. 8C, D). The compacta is woven-textured with globular osteocyte lacunae lacking organization. A single canal is present in Taxonomy the middle of the bone wall. IVPP V20289 can be readily assigned to the Enantiornithes based on the presence of several enantiornithine synapo- morphies including: lateral margin of coracoid convex; Ontogenetic status proximal margin of the humeral head concave in its central IVPP V20289 is considered to be a subadult individual portion, rising ventrally and dorsally; minor metacarpal based on histology (the absence of any LAGs and the pro- extending farther distally than the major metacarpal; meta- portionately thin ICL) and the incomplete fusion of some tarsal IV significantly thinner than metatarsals II and III compound bones, such as the carpometacarpus (the semi- (Chiappe & Walker 2002). Although development was lunate carpal unfused to the metacarpals), tibiotarsus incomplete at the time of death, IVPP V20289 preserves (proximal tarsals are unfused to the tibia with free inter- two clear autapomorphies that indicate it represents a new medium), and tarsometatarsus (distal tarsals unfused to taxon, Monoenantiornis sihedangia gen et. sp. nov.: the the metatarsals, and metatarsals unfused with each other premaxillary teeth bear lingual grooves that differ morpho- at their most proximal ends). logically from the only other avian in which this feature Apart from these unfused elements, the new specimen occurs (Sulcavis)(Fig. 3) and the minor metacarpal extends does not represent a young juvenile as indicated by the twice as far as in any other enantiornithine distally beyond presence of fusion in other compound elements: the sacrals the major metacarpal (Fig. 6). These autapomorphic 920 H. Hu and J. K. O’Connor

Figure 9. Strict consensus tree showing the phylogenetic position of Monoenantiornis sihedangia gen. et sp. nov. Consistency index: 0.343; retention index: 0.665. Absolute Calculated Bremer support values are indicated at each node. New Early Cretaceous enantiornithine bird from China 921 features are not considered subject to ontogenetic change at fused, which has been described in a few other Early Cre- the fairly late stage in development captured by this speci- taceous enantiornithine specimens including Longusun- men. Furthermore, IVPP V20289 also preserves features guis IVPP V17964 (Wang et al. 2014b). These two rarely observed in other known Early Cretaceous enantior- specimens share similar degrees of skeletal fusion, not nithines, such as the large and triangle-shaped furcular limited to the fusion of the premaxillary corpora: the syn- articular surface of scapula and the tibial cnemial crest sacrum and the pygostyle are both nearly fully fused, (Fig. 1), that support the justification of new taxon. while the carpometacarpus is entirely unfused and the In order to test taxonomic hypotheses based on morpho- tibiotarsus and the tarsometatarsus are partially fused or logical comparisons, we submitted the new specimen to unfused. If inferences regarding the fusion of the premax- phylogenetic analysis using a modified version of the illary corpus in Monoenantiornis IVPP V20289 and Lon- Wang et al.(2015) data set with TNT (Goloboff et al. gusunguis IVPP V17964 are correct, it would appear that 2008) (Supplemental material S1, S2). We implemented a the premaxillae fuse with or shortly after fusion occurs in heuristic search conducting 1000 replications of tree vertebral elements (synsacrum and pygostyle), and before bisection reconnection (TBR) branch swapping, saving 10 the complete formation of compound limb bones (carpo- trees per replication, which returned 250 most parsimoni- metacarpus, tibiotarsus and tarsometatarsus). This is simi- ous trees (MPTs) of 1070 steps. Another round of TBR lar to the pattern observed in Neornithes in which the branch swapping returned 384 MPTs of 1070 steps. compound limb bones are the last to ossify (Hogg 1982). The results of the strict consensus tree (Fig. 9) nearly Furthermore, the holotype of Monoenantiornis sihedan- concur with those of Wang et al.(2015) with regards to gia captures an ontogenetic stage in the formation of the basal birds and the Ornithuromorpha, except for the rela- tibiotarsus that is rarely preserved in fossil birds. The tive positions of several confuciusornithids (Confuciusor- ascending process was previously considered to be a pro- nis dui and Jinzhouornis are resolved as a clade here). jection of the astragalus in non-avian dinosaurs (Ostrom Enantiornithes is well resolved, but weakly supported 1991) and Mesozoic birds (Mayr et al. 2005), since it is as indicated by the low absolute Bremer support values. always preserved as part of this element. In Monoenan- As in several previous phylogenetic analyses (Zhou et al. tiornis IVPP V20289, the astragalus is fused with the cal- 2008;Huet al. 2014; Wang et al. 2016), Protopteryx and caneum but the ascending process remains free. This the Pengornithidae are resolved as basal enantiornithines, supports the results of recent embryological studies in liv- but Iberomesornis is resolved in the basalmost position in ing birds that indicate the ascending process originates this analysis, similar to the result in Wang et al.(2016). from an independent ossification centre, the intermedium The monophyletic Longipterygidae and Bohaiornithidae (Ossa-Fuentes et al. 2015). are supported here as in some previous analyses (Wang Although the abundant juvenile and subadult specimens et al. 2014b, 2016; Zhang et al. 2014). The Longipterygi- of Early Cretaceous enantiornithines from the Jehol biota dae are in a relatively basal position, only more derived contain a wealth of ontogenetic information, the timing than Iberomesornis, Protopteryx and Pengornithidae. and sequence of the formation of compound bones remain Monoenantiornis sihedangia is resolved more derived largely unexplored with the exception of the sternum than Longipterygidae, but basal to the Bohaiornithidae (O’Connor et al. 2015). Clarification of the pattern of skel- and other enantiornithines. This node is supported by sev- etal development and the sequence of fusion that occurs in eral synapomorphies: outermost trabeculae terminating the formation of compound bones will not only help to cranial to caudal end of sternum (character 112: 0); rostral quantify the unique super-precocial ontogeny of the Enan- margin of sternum more vaulted (character 114: 0); and tiornithes, but also allow accurate estimates of ontogenetic laterally directed outermost trabecula of sternum (charac- age in specimens when destructive histological techniques ter 246: 1). These results correspond well to conclusions are not possible or not permitted. Using the new informa- based on morphological observations. tion provided by IVPP V20289, together with that of sev- eral previously published specimens, we form a preliminary hypothesis regarding the sequence of fusion Implications for skeletal development in the between elements that occurs during the post-hatching Enantiornithes skeletal development of Early Cretaceous enantiornithines. The sequence in which skeletal elements fuse is difficult From the earliest known post-hatching ontogenetic con- to determine in fossil birds since it requires the excellent dition with incomplete ossification of the periosteal surfa- preservation of all compound bones in specimens that ces in long bones and no skeletal fusion present, to the record the full ontogenetic spectrum. In the formation of adult condition with the maximum degree of fusion compound bones, some ontogenetic stages are quite observed amongst Early Cretaceous Jehol enantiorni- ephemeral and thus very rarely preserved. The holotype thines, three general stages are identified in the formation of Monoenantiornis sihedangia records such an ontoge- of compound bones, which can be defined by the degree netic stage, previously undocumented in an enantiorni- of fusion in the participating elements (Supplemental thine. The premaxillary corpora are considered medially material S3; Fig. 10). Although a large number of Early 922 H. Hu and J. K. O’Connor

Figure 10. Occurrences of fusion in compound bones preserved in select specimens of Early Cretaceous enantiornithines representing different ontogenetic stages. New Early Cretaceous enantiornithine bird from China 923

Cretaceous enantiornithines have been discovered, only ambiguously in Protopteryx IVPP V11665 and Eopengor- some of them preserve most or all compound bones pro- nis STM 24–1; stage 1 or stage 2a). The synsacrum is viding information regarding skeletal fusion. Since histo- entirely fused in Parapengornis IVPP V18632 and Proto- logical analysis is destructive to the specimen, only a few pteryx IVPP V11665, but appears incompletely fused in of them have been permitted to be sampled histologically. Eopengornis STM 24–1; the pygostyle is fused, and the Therefore, we cannot completely verify our hypothesis semilunate is unfused to the major metacarpal in Parapen- with specific age data gained through histology. Histologi- gornis IVPP V18687 and IVPP V18632, Protopteryx cal analyses on well-preserved specimens are required for IVPP V11665 and Eopengornis STM 24–1. Given the a more detailed understanding of early avian skeletal pygostyle is partially fused in the basal condition, it fusion than can be presented here. However, the available appears that this element fully forms slightly before the histological information so far is consistent with our synsacrum, which rapidly ossifies to provide rigidity to hypothesis (Supplemental material S3, Fig. 10). the body in flight, important for super-precociality. The astragalus and the calcaneum are neither fused to each Stage 0. The earliest post-hatching condition of enantior- other, nor to the tibia (intermedium not visible) in Para- nithines is comparable to the basal condition observed in pengornis IVPP V18687 and IVPP V18632, and it is diffi- Archaeopteryx, in which all the compound bones are cult to determine if they fused to each other in unfused, including the pygostyle (incipiently fused), synsa- Protopteryx IVPP V11665 and Eopengornis STM 24–1 crum, tibiotarsus, tarsometatarsus and the carpometacarpus, due to poor preservation; the distal tarsals are not pre- but differs from this basal taxon in that carpals and tarsals served, and the metatarsals are unfused to each other prox- are not even ossified or only show incipient ossification. imally in Parapengornis IVPP V18687 and IVPP This stage is exemplified by the juvenile individuals V18632, while the distal tarsals are ambiguously fused GMV–2156, GMV–2158, GMV–2159, NIGP–130723 into one element, but unfused to the tibia, in Protopteryx (Chiappe et al. 2007), STM 34–1, STM 34–2, STM 34–7 IVPP V11665 and Eopengornis STM 24–1. The sternum (Zheng et al. 2012). The pygostyles (preserved in GMV– in Parapengornis IVPP V18687 is almost fully ossified, 2156, GMV–2159, NIGP–130723, STM 34–1, STM 34–2, but the two bilaterally symmetrical sternal plates are STM 34–7) have undergone some degree of fusion, but are incompletely fused medially and slightly separated along morphologically very different from the fully fused adult their rostromedial margins forming a small cleft also pygostyle, being proportionately more elongate, slender observed in subadult specimens of Jeholornis (Zhou & and simple in outline. Sutures between individual caudal Zhang 2003) and Confuciusornis (Chiappe et al. 1999). vertebrae are obviously visible. With the exception of the Histological analysis of the femur of Parapengornis pygostyle, all the other preserved compound bones are IVPP V18687 indicates immaturity: an ICL, middle entirely unfused: the sacrals remain free, whereas in neo- region, OCL, and LAG are all absent, which are typical rnithines fusion begins first in the synsacrum (preserved in features of adult Jehol enantiornithines (Hu et al. 2015). GMV–2156, GMV–2158, GMV–2159, NIGP–130723, This indicates this specimen was probably less than one STM 34–1, STM 34–2, STM 34–7); the semilunate is year of age at the time of death. unfused to the major metacarpal (preserved in GMV–2156, The histology of Eopengornis martini STM 24–1 GMV–2158, GMV–2159, NIGP–130723, STM 34–7); the (ambiguous stage 1 or 2a) shows that the recent deposition astragalus and the calcaneum are neither fused to each of bone tissue in the femur and the humerus had slowed, other, nor to the tibia to form the tibiotarsus, or completely although the ulna was still growing at a relatively fast not ossified in this stage (partially preserved in GMV– rate. A LAG is only present in the humerus, an OCL is 2156, GMV–2159, STM 34–1, STM 34–7); the distal tar- present both in the humerus and the femur, and the ICL is sals are often missing, but the metatarsals are entirely formed in the humerus, femur and ulna (Wang et al. unfused to each other (preserved in GMV–2156, GMV– 2014). The stratifications of the ICL and OCL in the femur 2158, GMV–2159, STM 34–1, STM 34–7). The sternum is indicate Eopengornis martini STM 24–1 is more mature incompletely ossified, consisting of a small fan-shaped than Parapengornis IVPP V18687, consistent with the body with a xiphoid process already bearing an incipient partial fusion of the tarsometatarsus in STM 24–1. How- keel (preserved in GMV–2158, GMV–2159, NIGP– ever, poor preservation of the ankle prevents a detailed 130723, STM 34–1, STM 34–2, STM 34–7) (Zheng et al. comparison of STM 24–1 with other specimens. 2012). The morphology of the sternum in pengornithids at this stage is unknown (O’Connor et al. 2015). Stage 2a. The tarsals are the next elements to fuse. Based Stage 1. The synsacrum is nearly or fully fused, with on Monoenantiornis IVPP V20289, we infer the astraga- sutures still visible between the intervening vertebrae in lus and the calcaneum fuse to each other after fusions of some specimens, and the pygostyle is fused, while other the synsacrum and pygostyle, and for a brief moment the compound limb bones remain entirely unfused (e.g. Para- ascending process remains free before becoming fused to pengornis IVPP V18687 and IVPP V18632, and the other proximal tarsals. The distal tarsals are also fused 924 H. Hu and J. K. O’Connor to each other to form a cap, but unfused to the proximal Cretaceous enantiornithines indicates the synsacrum and part of the metatarsals. Though badly preserved, the ster- the pygostyle are the first elements to fully fuse, similar to num including the keel appears to be fully fused and living birds (Hogg 1982), in which the sternum is also nearly ossified entirely, with the potential exception of the incompletely ossified. The tarsals are the next to fuse, distal expansions of the lateral trabeculae. with the astragalus and the calcaneum first fusing to each The ulna histology of Monoenantiornis IVPP V20289 other before fusion occurs with the intermedium (ascend- developed a very thin ICL, and no OCL or LAG was pres- ing process). The sternum completes ossification before ent. Although comparison is limited by differences in the tarsals fuse to the tibia forming a tibiotarsus. The tar- available sampling elements, IVPP V20289 is histologi- sometatarsus and the carpometacarpus are the last ele- cally similar to Eopengornis martini STM 24–1. They are ments to fuse in this sequence. also very similar in terms of skeletal fusion with STM 24– Based on specimens that encompass a phylogenetic 1 potentially being slightly more mature, highlighting the spectrum of taxa (e.g. Bohaiornithidae, Pengornithidae), brevity of the ontogenetic period in which the interme- this very general hypothesis represents a launching point dium is free. for further enquiry into the skeletal ontogenetic sequences of the Enantiornithes. We recognize that lineage-specific Stage 2b. The proximal tarsals are fused with the ascend- trends in skeletal development occur (Zheng et al. 2012; ing process, but unfused to the tibia. The distal tarsal cap O’Connor et al. 2015) but, unfortunately, at this time no is fused to the metatarsals, which are unfused to each complete ontogenetic series are known for any individual other throughout their length. The carpometacarpus taxon. Although limited, available histological data remains entirely unfused (e.g. Bohaiornis LPM B00167, largely concurs with the presented hypothesis. However, Sulcavis BMNH ph 000805, Parabohaiornis IVPP the condition observed in Enantiornithes indet. STM 29–8 V18691 and IVPP V18690, and Longusunguis IVPP clearly indicates differences between taxa (O’Connor V17964). The sternum is fully ossified. et al. 2014). Lineage-specific trends in the sternum also Stage 3. All compound elements are fused in this stage. remain unresolved. Although we know the keel appears in The proximal tarsals are fused to the tibia forming a true stage 1 in derived enantiornithines, in primitive taxa such tibiotarsus. The metatarsals sometimes show some degree as the pengornithids it is presumed that the keel must have of proximal fusion. The semilunate carpal is fused to the formed very late (stage 3) although there is still currently major metacarpal in this stage, forming a carpometacarpus no direct evidence to support this (O’Connor et al. 2015). with the alular metacarpal free. There is a carpal X pre- Additional histological information and investigation of a served in the juvenile specimen GMV–2158, suggesting greater number of enantiornithine specimens will the semilunate is potentially fused to the carpal X before undoubtedly lead to clarifications that hone this hypothe- the formation of a carpometacarpus. Unfortunately, carpal sis, which represents a start for early bird skeletal devel- X is rarely preserved so it cannot be determined at what opment study. stage this fusion occurs. Several adult specimens have been reported preserving stage 3, including Zhouornis CNUVB 0903, Pengornis IVPP V15336, Pterygornis IVPP V20729 Acknowledgements and Fortunguavis IVPP V18631 (Wang et al. 2014a). The presence of a well-developed ICL and a mid-corti- We thank Dahan Li and Yutong Li (IVPP) for preparing cal LAG suggests that Zhouornis CNUVB 0903 is a sexu- the specimen, Jie Zhang and Wei Gao (IVPP) for taking ally mature individual that has already experienced the the photographs, and Shukang Zhang for assistance with full extent of its rapid growth phase (Zhang et al. 2013) the histological preparation. This project was supported and only slow growth and the deposition of a few more by the National Basic Research Program of China 973 peripheral LAGs would be expected (O’Connor et al. Program (2012CB821906) and the National Natural Sci- 2014). This is consistent with the fusion of all compound ence Foundation of China (91514302). bones in Zhouornis CNUVB 0903, and supports the deter- mination of this specimen as stage 3. Only the indetermi- nant enantiornithine STM 29–8 shows more advanced Supplemental data histology with several LAGs located in the OCL (O’Connor et al. 2014). However, the carpometacarpus, Supplemental material for this article can be accessed tibiotarsus and tarsometatarsus are all incompletely here: http://dx.doi.org/10.1080/14772019.2016.1246111. formed in STM 29–8, indicating that at least in this enan- tiornithine lineage, ontogeny is even more prolonged. This may be related to terminal body size. ORCID This initial study of the ontogenetic sequence of fusion events in the formation of compound bones in Early Han Hu http://orcid.org/0000-0001-5926-7306 New Early Cretaceous enantiornithine bird from China 925

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