Here we report on three new species of ornithuromorph birds from the Lower Cretaceous Xiagou Formation in the Changma Basin of Gansu Province, northwestern China: Yumenornis huangi gen. et sp. nov., Changmaornis houi gen. et sp. nov., and Jiuquanornis niui gen. et sp. nov.. The last of these is based on a previously published but unnamed specimen: GSGM-05-CM-021. Although incomplete, the specimens can be clearly distinguished from each other and from Gansus yumenensis Hou and Liu, 1984. Phylogenetic analysis resolves the three new taxa as basal ornithuromorphs. This study reveals previously unrecognized ornithuromorph diversity in the Changma avifauna, which is largely dominated by Gansus but with at least three other ornithuromorphs. Body mass estimates demonstrate that enantiornithines were much smaller than ornithuromorphs in the Changma avifauna. In addition, Changma enantiornithines preserve long and recurved pedal unguals, suggesting an arboreal lifestyle; in contrast, Changma ornithuromorphs tend to show terrestrial or even aquatic adaptions. Similar differences in body mass and ecology are also observed in the Jehol avifauna in northeastern China, suggesting niche partitioning between these two clades developed early in their evolutionary history.

Funding: This research was supported by the Hundred Talents Project of the Chinese Academy of Sciences, the National Natural Science Foundation of China (40672007,41072019), and the Department of Land and Resources of Gansu Province to LDQ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Copyright: © 2013 Wang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Here we describe two new ornithuromorph specimens from the Xiagou Formation in the Changma Basin. Based on comparison with GSGM-05-CM-021 [ 5 , 10 ], we also erect a new species for this specimen. We describe the morphology of the new specimens and discuss the significance of these taxa in understanding the Changma avifauna.

The second unnamed ornithuromorph specimen, GSGM-05-CM-021, consists of an isolated sternum, furcula, and sternal ribs [ 5 ]. Its sternum is distinct from that of Gansus, representing a basal non-ornithurine member of Ornithuromorpha similar to Archaeorhynchus from the Jiufotang Formation of Liaoning Province in northeastern China [ 5 , 10 ]. Despite this growing diversity, all other taxa are represented by isolated specimens and Gansus is by far the dominant taxon in the Changma avifauna.

In the last decade, nearly one hundred fossil birds have been discovered from the Lower Cretaceous Xiagou Formation in the Changma Basin of Gansu Province in northwestern China. Most of these are referred to Gansus yumenensis, the first Mesozoic fossil bird from China [ 1 - 4 ], although additional diversity has slowly accumulated; a second unnamed ornithuromorph bird [ 5 ], the enantiornithine Qiliania graffini [ 6 ], and three other unnamed enantiornithine specimens [ 7 - 9 ] have also been described.

The electronic edition of this article conforms to the requirements of the amended International Code of Zoological Nomenclature, and hence the new names contained herein are available under that Code from the electronic edition of this article. This published work and the nomenclatural acts it contains have been registered in ZooBank, the online registration system for the ICZN. The ZooBank LSIDs (Life Science Identifiers) can be resolved and the associated information viewed through any standard web browser by appending the LSID to the prefix "http://zoobank.org/". The LSID for this publication is: urn:lsid:zoobank.org:pub:DC6A3D74-B8B7-41BA-A6BF-7BD48D6CD3C7. The electronic edition of this work was published in a journal with an ISSN, and has been archived and is available from the following digital repositories: PubMed Central, LOCKSS.

A phylogenetic analysis was performed using the O’Connor and Zhou [ 12 ] dataset, with the addition of Yumenornis, Changmaornis, and Jiuquanornis [ 5 ] ( File S1 ). Neornithes was represented by Anas platyrhynchos and Gallus gallus; Dromaeosauridae was scored as the outgroup. The dataset consists of 245 characters (31 ordered; all characters weighted equally) evaluated for 63 taxa; the matrix was analyzed with TNT [ 13 ], applying a heuristic search retaining the single shortest tree from every 1000, followed by an additional round of tree bisection reconnection (TBR) branch swapping.

The two new specimens, GSGM-06-CM-013 and GSGM-08-CM-002, and the previously described GSGM-05-CM-021 (Gansu Geological Museum) were discovered in the Xiagou Formation near Changma in Gansu Province of northwestern China. Precise locality information is available to qualified researchers upon request. The issuing authority is the Gansu Geological Museum, represented by Da-Qing Li (co-author). All necessary permits were obtained for the described study, which complied with all relevant regulations.

Anatomical nomenclature primarily follows Baumel and Witmer [ 11 ]. English equivalents are used for osteological terminology while Latin is maintained for muscles. All measurements were taken with calipers to the nearest 0.1 mm.

Results

Systematic Paleontology Aves Linnaeus, 1758 [15] Pygostylia Chiappe, 2002 [16] Ornithothoraces Chiappe, 1995 [17] Ornithuromorpha Chiappe, 2002[16] Yumenornis huangi gen. et sp. nov. urn:lsid:zoobank.org:act:EEC6E8A1-318F-491B-BD62-EFF58C4DBFC0

Etymology The generic name “Yumen” is derived from the name of the city near the fossil locality. The specific name is dedicated to Mr. Zhao-Chu Huang of the Institute of Vertebrate Paleontology and Paleoanthropology (IVPP) for his long-lasting support to several generations of IVPP staff.

Diagnosis Yumenornis huangi is distinguished from other known ornithuromorphs by the following unique combination of characters: sternum with angular rostral margin (~90°), lateral (zyphoid) processes, and robust, distally expanded lateral trabeculae; radius with deep distal fossa; ratio of length of manus relative to humerus 1.1. Yumenornis huangi can be separated from Gansus by the following morphological differences: the rostral margin of the sternum is sharper than that of Gansus (90° vs. 140° in Gansus); the lateral trabeculae are short and caudally expanded, contrasting with the unexpanded trabeculae in Gansus.

Etymology The generic name “Changma” is derived from the name of the town where the fossil locality belongs to. The specific name is in honor of Professor Lian-Hai Hou, who named Gansus yumenensis.

Diagnosis Changmaornis houi is distinguished from other known ornithuromorphs by the following unique combination of characters: synsacrum composed of at least 11 sacral vertebrae with elongate distal transverse processes; ischium with dorsal process; distal half of the pubis compressed mediolaterally; metatarsal I J-shaped; distal margin of metatarsal II trochlea does not reach the proximal margin of the metatarsal III trochlea; pedal digit III longest in foot; ratio of pedal digit III to tibiotarsus 0.82; robust and blunt pedal unguals with poorly developed flexor tubercles. Changmaornis houi can be distinguished from Gansus by the following morphological differences: pedal digit III is the longest and shorter than tarsometatarsus, while in Gansus pedal digit IV is the longest and longer than tarsometatarsus; pedal unguals lack well-developed flexor tubercles, contrasting with the pointed flexor tubercles in Gansus.

Description A relatively complete thoracic vertebra is preserved in articulation with another completely damaged thoracic (Figure 5). The spinous process is rectangular, with a distinct ridge forming the dorsal margin. The vertebral centrum is laterally excavated by a deep, broad fossa, similar to those of other basal ornithuromorphs (e.g. Gansus, Yixianornis, Yanornis, and Hongshanornis longicresta [25]). The length of the centrum is nearly twice its width. The articular surfaces appear to be amphicoelous. The proximal half of an isolated thoracic rib is preserved. It bears a round costal tubercle on the proximal end. The synsacrum is preserved in ventral view, crushed so that the cranial and caudal ends are unclear. The two cranialmost sacral vertebrae bear laterodorsally directed costal processes. The synsacrum is formed by at least 11 completely fused vertebrae based on the number of preserved transverse processes (Figure 5B). In most ornithuromorphs, the synsacrum is composed of at least nine vertebrae; Yixianornis and Yanornis both have nine fused sacral vertebrae [19,20], while the more derived Gansus [2], Apsaravis [24], and Ichthyornis [26] possess 10 fused sacrals. The basalmost ornithuromorph, Archaeorhynchus spathula, possesses only seven to eight fused sacral vertebrae [10,12,27], although this may potentially be ontogenetic given that all known specimens are subadult [10]. In enantiornithines, the synsacrum is composed of seven or eight vertebrae [12,28]. The transverse processes of the sacral vertebrae are much longer than those of Gansus [2]; in the first few vertebrae they are laterocaudally directed, becoming more caudally directed and elongate in the last four synsacral vertebrae, similar to Yanornis [19]. Of the two ilia, only the proximal half of the right side and a fragment of the left are preserved, although these do not provide many anatomical details; the lateral margins appear to be deeply concave in ventral view (Figure 5). The right ischium and pubis are not preserved in articulation and are missing their proximal ends. The dorsal process of the ischium is large and obtusely triangular, as in Gansus and other ornithuromorphs, but is more proximally located than in Yixianornis. The distal end of the ischium tapers to its terminus, as in Gansus and Yixianornis. The pubis is medially curved and mediolaterally compressed along its distal half, contrary to the uncompressed pubis in Gansus. The distal end of the pubis does not expand ventrally although a dorsal expansion may have been present. The distal end of the right tibiotarsus is preserved in medial view, in articulation with the completely preserved right tarsometatarsus and pedal phalanges (Figure 5). A medial epicondyle is developed on the medial surface of the distal tibiotarsus. Two tubercles are developed on the cranial surface of the distal end of the tibiotarsus. One is subrounded, located midway between the medial and lateral condyles, and bounded by a shallow fossa. The other is developed proximal to the medial condyle, forming a cranially projecting, proximodistally elongate ridge. The shape and position of the two tubercles resemble the paired ridges present in Apsaravis, which are interpreted as comparable to the tubercles for attachment of the extensor retinaculum in Neornithes [24]. However, three tubercles are present cranially on the distal end of the tibiotarsus in Gansus (GSGM-05-CM-014): the distalmost tubercle is subtriangular; the next tubercle is smaller, and located proximal and lateral to the first; the proximalmost one is medially located, forming an elongate ridge similar to the second one just described for Changmaornis. As in Gansus, the tarsometatarsus is straight and completely fused (Figure 5). The dorsal surface of the proximal end is somewhat crushed; a large prominence without grooves or ridges projects weakly on the plantar surface of the proximal end, interpreted as a primitive hypotarsus, similar to that in Gansus and other basal ornithuromorphs (e.g. Yixianornis and Yanornis) [20,29]. The proximodorsal surface bears a deep dorsal infracotylar fossa, and the tubercle for the attachment of the m. tibialis cranialis is located on the mediodistal margin of this fossa [11]. Metatarsal IV is buried in the matrix; only metatarsals I, II, and III are visible. The short metatarsal I is nearly “J”-shaped in medial view, articulating with the medial surface of metatarsal II proximal to the trochlea, similar to the condition in Gansus. A small collateral ligament pit is present on the medial surface of the trochlea of metatarsal I. Metatarsal II does not extend distally to the base of the metatarsal III trochlea, and is displaced plantarly; the proximal position of metatarsal II trochlea strongly resembles that in Gansus. The trochlear surface of metatarsal II is partially ginglymous, while metatarsal III is fully ginglymous. Both metatarsals bear a pit for the collateral ligament on the medial surface of the trochlea. The pedal phalanges are well preserved (Figure 5). Digit I is completely reversed, as in Gansus. The first phalanx in each digit is proportionately shorter than that of Gansus (CAGS-IG-04-CM-008 and GSGM-05-CM-014; Table 2). The nonungual phalanges of digits II-IV are also shorter than those in Gansus (Table 1; Figure 6C). Digit III is the longest, as in most ornithuromorphs (e.g. Schizooura, Yanornis, and Yixianornis; Figure 6) including neornithines [10,19,20,23,25], although the digit is shorter than the tarsometatarsus; the ratio of the length of digit III (including the ungual) relative to the tarsometatarsus is approximately 0.82, similar to that of Schizooura (0.80, IVPP V16861; Figure 6B) [30]. This clearly distinguishes this specimen from Gansus (CAGS-IG-04-CM-008), in which digit IV is the longest and the ratio of the length of digit III (including the ungual) to the tarsometatarsus is nearly 1.21. Measurement Specimen CAGS-IG-04-CM-008 GSGM-05-CM-014 GSGM-08-CM-002 Tarsometatarsus length 31.5 40 36.9 Pedal phalanx I-1 length 8.1 7.3 7.4 Pedal phalanx I-2 length 3.7 4.1 3.9 Pedal phalanx II-1 length 13.7 15.1 10 Pedal phalanx II-2 length 10.4 12.9 9.9 Pedal phalanx II-3 length 4.4 4.6 4.8 Pedal phalanx III-1 length 13.6 13.5 11.4 Pedal phalanx III-2 length 8.5 12.2 7.4 Pedal phalanx III-3 length 7.1 9.0 7.3 Pedal phalanx III-4 length 4.3 4.6 4.2 Pedal phalanx IV-1 length 11.5e 12.0 8.5 Pedal phalanx IV-2 length 8.3 9.7 6.3 Pedal phalanx IV-3 length 7.5 8.7 4.9 Pedal phalanx IV-4 length 7.2 9.3 4.9 Pedal phalanx IV-5 length 3.5 3.7 3.6 Table 2. Measurements (mm) of hind limbs of Gansus yumenensis (CAGS-IG-04-CM-008, GSGM-05-CM-014) and Changma houi gen. et sp. nov. (GSGM-08-CM-002). CSV Download CSV PPT PowerPoint slide

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larger image TIFF original image Download: Figure 6. Comparison of pedes of Changmaornis houi (A) and other Early Cretaceous ornithuromorphs. B, Schizooura lii; C, Gansus yumenensis; D, Yixianornis grabaui; E, Yanornis martini. https://doi.org/10.1371/journal.pone.0077693.g006 The unguals are all small but robust (Figure 5); ungual IV is the shortest, and II and III are the longest. Relatively deep extensor grooves (compared to those in Gansus) run the entire length of the medial and lateral surfaces of all the unguals, resembling Yixianornis (Figure 6D), rather than restricted to the distal portion as in Gansus (CAGS-IG-04-CM-008). Flexor tubercles are nearly absent; the proximal ends have plantarly projected, weak and rounded tubercles that can barely be distinguished from the proximoventral corner of the articular cotyla. Jiuquanornis niui gen. et sp. nov. urn:lsid:zoobank.org:act:DF96E3B8-4A15-403D-85BC-EE46517858E6

Etymology The generic name “Jiuquan” is derived from the name of the city near the fossil locality. The specific name is dedicated to Professor Shao-Wu Niu, for his contribution to geological research in the Changma Basin.

Diagnosis Jiuquanornis niui is distinguished from other known ornithuromorphs by the following unique combination of characters: U-shaped furcula without a hypocleidium; short imperforate body of sternum; small lateral processes on sternum; lateral trabeculae distally expanded medially; elongate intermediate trabeculae, equal to lateral trabeculae in distal extent; V-shaped xiphoid formed by short, fused medial trabeculae [5]. The sternum of Jiuquanornis niui can be clearly differentiated from that of Gansus by the long lateral and intermediate caudal trabeculae, V-shaped xiphoid, and absence of caudal fenestrae.

Comments Jiuquanornis niui was first described as an unnamed ornithuromorph by You et al. [5]. Where comparison allows, the specimen is morphologically distinct from all other described ornithuromorphs, and thus we erect a new taxon. The sternum of Jiuquanornis strongly resembles that of Archaeorhynchus: both have long lateral and intermediate caudal trabeculae separated by deep incisures, which distinctly separate them from other basal ornithuromorphs; the trabeculae extend well past the caudal midline margin in both taxa. However, the two taxa differ from each other in the following features of the sternum: the rostral margin in Jiuquanornis defines an angle of approximately 100°, constituting a sharp craniomedial apex [5], while the rostral margin in Archaeorhynchus is more rounded, defining a greater angle of nearly 110°; the craniolateral processes in Jiuquanornis are smaller and more pointed than those of Archaeorhynchus; Jiuquanornis possesses a tapered, V-shaped xiphoid process, while the xiphial region in Archaeorhynchus is very short, lacking a distinct process (Figure 3F) [10]. The furcula of Jiuquanornis is similar to that of Archaeorhynchus and other basal ornithuromorphs (e.g. Gansus, Jianchangornis, and Yanornis); it is U-shaped with a low interclavicular angle of approximately 36°, and lacks a hypocleidium (Figure 7).