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Yuanjiawaornis viriosus, gen. et sp. nov., a large enantiornithine bird from the Lower Cretaceous of western Liaoning, China
Cretaceous Research 55 (2015) 210e219
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Yuanjiawaornis viriosus, gen. et sp. nov., a large enantiornithine bird from the Lower Cretaceous of western Liaoning, China Dongyu Hu a, b, *, Ying Liu a, Jinhua Li a, Xing Xu a, b, c, Lianhai Hou a, c a
Paleontological Institute of Shenyang Normal University, 253 North Huanghe Street, Shenyang 110034, China Key Laboratory for Evolution of Past Life in Northeast Asia, Ministry of Land and Resources (Shenyang Normal University), Shenyang 110034, China c Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 142 Xiwai Street, Beijing 100044, China b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 18 March 2013 Accepted in revised form 28 February 2015 Available online
Here we describe a new enantiornithine bird, Yuanjiawaornis viriosus gen. et sp. nov., based on a nearly complete, mostly articulated postcranial skeleton from the Lower Cretaceous Jiufotang Formation (120 Ma) of western Liaoning Province, northeastern China. It is similar in size to large bohaiornithids among the known Early Cretaceous enantiornithines; only Pengornis houi is larger. The semilunate carpal is incompletely fused to the metacarpals, suggesting that the holotype specimen was not fully mature at the time of death. The new specimen is distinguishable from other known enantiornithines by a unique combination of features including large body size, forelimb and hind limb subequal in length, a longitudinally grooved ventral surface of the synsacrum, robust and long transverse processes of the caudalmost sacral vertebra, a craniodorsally tapered acromion process of the scapula, a straight lateral margin of the coracoid, medially curved clavicular rami with tapered omal tips, a sternum that is oval in outline with slightly expanded distally caudolateral processes, a humeral head with a flat proximal surface, and a humerus with a deltopectoral crest that gradually decreases in height distally. A comparative analysis of some sacral features of basal birds including this taxon suggests that enantiornithines might have a uniquely shaped synsacrum, although more data is needed to confirm that hypothesis. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Enantiornithes Yuanjiawaornis viriosus Lower Cretaceous Liaoning China
1. Introduction Most known Early Cretaceous enantiornithine birds are small e about the size of a living sparrow or starling. They are much smaller than contemporaneous basal birds such as Confuciusornis sanctus (Hou et al., 1995) and ornithuromorph birds such as Yixianornis grabaui (Zhou and Zhang, 2001). The discovery of the largest known Early Cretaceous enantiornithine Pengornis houi (Zhou et al., 2008), greatly increased the upper bound of the size range of Early Cretaceous enantiornithines, and indicates a greater overlap in body size range among the three major categories of Early Cretaceous birds: basal birds, Enantiornithes, and Ornithuromorpha. Since the description of Pengornis, several large and medium sized enantiornithines have been reported from the Jehol deposits:
* Corresponding author. Paleontological Institute of Shenyang Normal University, 253 North Huanghe Street, Shenyang 110034, China. E-mail addresses: [email protected] (D. Hu), [email protected] (Y. Liu), [email protected] (J. Li), [email protected] (X. Xu), houlianhai@ synu.edu.cn (L. Hou). http://dx.doi.org/10.1016/j.cretres.2015.02.013 0195-6671/© 2015 Elsevier Ltd. All rights reserved.
Shenqiornis mengi (Wang et al., 2010), Bohaiornis guoi (Hu et al., 2011), Sulcavis geeorum (O'Connor et al., 2013), Zhouornis hani (Zhang et al., 2013), Parabohaiornis martini (Wang et al., 2014) and Longusunguis kurochkini (Wang et al., 2014), and those species comprise the Family Bohaiornithidae (Wang et al., 2014). Adding to this diversity, we report a new Early Cretaceous enantiornithine bird based on a specimen collected during the 2005 field season from the lacustrine beds of Dapingfang Town, Chaoyang County, western Liaoning Province. The new specimen is approximately the same size as Zhouornis hani among the bohaiornithids and only slightly smaller than Pengornis houi. We believe this specimen represents a new taxon (described below) and has implications for a greater understanding of enantiornithine morphology. Anatomical abbreviations: Ac, acromion process; cav, caudal vertebra; cmc, carpometacarpus; dv, dorsal vertebra; fe, femur; fl, the length of humerus þ ulna þ carpometacarpus; fu, furcula; ga, gastralia; gl, glenoid facet; hl, the length of femur þ tibiotarsus þ tarsometatarsus; hu, humerus; lco, left coracoid; lfe, left femur; lfi, left fibula; lhu, left humerus; lil, left ilium; lis, left ischium; lmc-III, left minor metacarpal; lpu, left pubis; lr, left radius; lra, left radiale; lsc; left scapula; lti, left
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tibiotarsus; ltm, left tarsometatarsus; lu, left ulna; mph, manual phalanx; mt-II-IV, the second to forth metatarsals; ns, neural spine; pa, parapophysis; pph, pedal phalanx; py, pygostyle; rco, right coracoid; rfe, right femur; rfi, right fibula; rhu, right humerus; ri, rib; ril, right ilium; ris, right ischium; rmc-I-III, right alular, major and minor metacarpals; rmtI, right first metatarsal; rr, right radius; rra, right radiale; rpu, right pubis; rsc, right scapula; rtm, right tarsometatarsus; rti, right tibiotarsus; ru, right ulna; rul, right ulnare; ns, neural spine; st, sternum; sy, synsacrum; ti, tibiotarsus; tmt, tarsometatarsus; tp, transverse process; ul, ulna; un, ungual; I, alular digit; i, hallux digit. Institutional Abbreviations: BMNHC, Beijing Natural History Museum, China; CNU, Capital Normal University, Beijing, China; IVPP, Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, China; PMOL, Paleontological Museum of Liaoning, China.
2. Systematic palaeontology Aves Linnaeus, 1758 Enantiornithes Walker, 1981 Yuanjiawaornis, gen. nov. Derivation of name: Yuanjiawao, name of type locality and strata, and Greek, ornis, bird. Type species: Yuanjiawaornis viriosus, type by monotypy. Diagnosis: Yuanjiawaornis differs from other enantiornithines including Pengornis and bohaiornithids by a unique combination of the following characters: large size (but smaller than Pengornis); forelimb and hind limb subequal in length (forelimb much longer than hind limb in Pengornis); ventral surface of synsacrum grooved longitudinally (ridged in bohaiornithids Bohaiornis and Parabohaiornis); transverse processes of caudal-most sacral vertebra robust and long (transverse processes of penultimate sacral vertebra robust and long in bohaiornithids Zhouornis, Parabohaiornis, and Longusunguis); acromion process tapered craniodorsally (acromion process nearly parallels to the shaft of scapular in all bohaiornithids except for Longusunguis); lateral margin of coracoid straight (strongly convex in Pengornis and bohaiornithids Shenqiornis, Sulcavis, and Longusunguis); clavicular rami medially curved and omal tips tapered (clavicular rami straight and omal tips expanded laterally in bohaiornithids); sternum oval in outline with caudolateral processes slightly expanded distally (caudolateral processes strongly expanded distally in most bohaiornithids, and craniolateral margin of sternum angular in Zhouornis); humeral head flat (convex in Pengornis and concave in all bohaiornithids except for Zhouornis) and deltopectoral crest gradually decreased in height distally (abruptly decreased distally in Shenqiornis, Sulcavis, and Longusunguis). Yuanjiawaornis viriosus sp. nov. Figs. 1e8, Table 1 Derivation of name: Latin, viriosus, vigorous. Type specimen: PMOL (Paleontological Museum of Liaoning) AB00032, a nearly complete and mostly articulated postcranial skeleton, missing the skull, cervical and cranial thoracic vertebrae, and most of the manual and pedal digits. Stratigraphic horizon and type locality: The Yuanjiawa Beds of Jiufotang Formation (120 Ma), Lower Cretaceous (Duan et al., 2006); Yuanjiawa Village, Dapingfang Town, Chaoyang County, Liaoning Province, China (Hu et al., 2010). Diagnosis: As for the genus. Description and comparisons: Axial skeleton: Seven thoracic vertebrae are present in articulation (Fig. 3). They are amphicoelous and bear prominent groove-like
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lateral excavations, as in most other enantiornithines (Chiappe and Walker, 2002). The parapophysis is centrally located on each centrum, as in other enantiornithines (Wang et al., 2014). The prezygapophysis extends cranially beyond the cranial margin of the centrum, and the postzygapophysis extends caudally to the level of the caudal margin of the centrum. In Shenqiornis (Wang et al., 2010) and Longusunguis (Wang et al., 2014), the postzygapophysis is longer than the prezygapophysis, extending caudally beyond the caudal margin of the centrum. The tips of the neural spines are craniocaudally expanded and contact one another as in Longusunguis (Wang et al., 2014) and the Late Cretaceous El Brete specimens from Argentina (Chiappe and Walker, 2002). Seven sacral vertebrae are present as in Pengornis (Zhou et al., 2008), Parabohaiornis (Wang et al., 2014), and the referred specimen of Zhouornis BMNHC Ph 756 (Zhang et al., 2014), and the vertebrae are fully co-ossified into a synsacrum (Fig. 4). The cranial articular surface of the synsacrum is round and distinctly concave; it is slightly broader than the caudal articular surface, but significantly wider than other middle centra as in Bohaiornis (Hu et al., 2011), Parabohaiornis (Wang et al., 2014), and the referred specimen of Zhouornis BMNHC Ph 756 (Zhang et al., 2014). However, in Bohaiornis and Parabohaiornis, the central synsacrum is more compressed transversely, forming a prominent ventral keel. A sharp groove runs longitudinally along the whole ventral surface of the synsacrum in the holotype. A similar groove is also reported in the synsacrum of Rapaxavis (O'Connor et al., 2010) and the referred specimen of Zhouornis BMNHC Ph 756 (Zhang et al., 2014), but the groove is shallow and limited in the distal two-thirds of the synsacrum in those taxa. The transverse processes of the most caudal sacral vertebra are the longest and most robust. The transverse processes are more delicate than those of the sixth sacral vertebra in Parabohaiornis (Wang et al., 2014), Longusunguis (Wang et al., 2014), and the referred specimen of Zhouornis BMNHC Ph 756 (Zhang et al., 2014). Six free caudal vertebrae are discernible, and they are amphicoelous with long, caudolaterally directed transverse processes. A caudal vertebra exposed in dorsal view and inferred to be from the cranial part of the tail bears a tall spinous process and its prezygapophyses are longer than the postzygapophyses. The pygostyle appears to be compressed mediolaterally and tapered caudally in lateral view. A ridge that is formed by the fused transverse processes, runs along the lateral surface decreasing in height distally, as in other enantiornithines such as Bohaiornis (Hu et al., 2011) and Sulcavis (O'Connor et al., 2013). The pygostyle is significantly shorter than metatarsal III as in most other enantiornithines, but contrasts with the state in Longusunguis where the opposite is true (Wang et al., 2014). At least five pairs of thoracic ribs are preserved, but they do not have uncinate processes (Figs. 1e2). At least three pairs of gastral ribs are also present. Thoracic girdle: Both scapulae are exposed in lateral view (Fig. 5). The acromion process of the left scapula is broken from the shaft and preserved in dorsal view, and the distal half of the shaft is missing. The distal end of the right scapula is concealed by ribs. The exposed shafts of the scapulae are straight. The acromion process tapers craniodorsally as in Enantiornis (Walker and Dyke, 2010) and Longusunguis (Wang et al., 2014), rather being nearly parallel to the shaft in Bohaiornis (Hu et al., 2011), Sulcavis (O'Connor et al., 2013), Shenqiornis (Wang et al., 2010), Zhouornis (Zhang et al., 2013), and Parabohaiornis (Wang et al., 2014). The acromion process is approximately as long as the glenoid facet, and its mediolateral width greatly exceeds its dorsoventral depth. The coracoid is strutlike and relatively short, with a length/maximum width ratio of 2.0, as in most Early Cretaceous enantiornithines including Pengornis and Bohaiornis (Fig. 5). The small acrocoracoid process, flat humeral glenoid and convex scapular facet are nearly aligned along an
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Fig. 1. Photograph of holotype specimen of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). Scale bar: 2 cm.
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Fig. 2. Line drawing of holotype specimen of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). The anatomical abbreviations are explained in the text. Scale bar: 2 cm.
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Fig. 3. Close-up photograph and line drawing of the dorsal vertebrae of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). The anatomical abbreviations are explained in the text. Scale bar: 0.5 cm.
Fig. 4. Close-up photograph of the synsacrum of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). The anatomical abbreviations are explained in the text. Scale bar: 0.5 cm.
omalesternal axis, as in other enantiornithines (Chiappe and Walker, 2002). Although the left and right coracoids are partly covered by the left and right scapulae, most of the dorsal surfaces of both coracoids are exposed. The lateral margin of the sternal half of the coracoid is nearly straight, in contrast to the strongly convex margin seen in many other enantiornithines such as Eoenantiornis (Zhou et al., 2005), Pengornis (Zhou et al., 2008), Shenqiornis (Wang et al., 2010), Sulcavis (O'Connor et al., 2013), and Longusunguis (Wang et al., 2014), and the slightly convex margin present in Bohaiornis (Hu et al., 2011) and Parabohaiornis (Wang et al., 2014). The medial margin of the sternal half of the coracoid also is nearly straight, in contrast to the convex margin seen in Sulcavis (O'Connor et al., 2013) and Parabohaiornis (Wang et al., 2014). A broad shallow fossa is present on the dorsal surface of the coracoid. No supracoracoid foramen is visible, but it is possible that this structure is covered by the scapula. The furcula is Y-shaped, with an interclavicular angle of about 45 and a long hypocleideum (Fig. 5). The interclavicular angle in similar enantiornithines, such as Bohaiornis, Sulcavis and Parabohaiornis is about 60 (Hu et al., 2011; O'Connor et al., 2013; Wang et al., 2014). The clavicular rami are medially curved; the lateral margin of the ramus is strongly convex and the medial margin is slightly concave. In contrast, the clavicular rami are straight in most other enantiornithines including Bohaiornis, Sulcavis, and Zhouornis (Hu et al., 2011; O'Connor et al., 2013; Wang et al., 2014). The dorsolateral surface of the clavicular ramus is strongly excavated so that the dorsal surface is much narrower than the ventral surface. However, in Bohaiornis (Hu et al., 2011) and Zhouornis (Zhang et al., 2014), the dorsal surface deepens towards the omal tip so that the dorsal surface is much wider than the ventral surface in the omal half. The thinner dorsal margin
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Fig. 5. Close-up photograph and line drawing of the pectoral girdle of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). The anatomical abbreviations are explained in the text. Scale bar: 1 cm.
continues along the hypocleidium, giving the hypocleidium a Tshaped cross section. The omal end has a bulbous dorsal expansion and bears a concave articular facet for the acromion process of the scapula on its dorsal surface. However, in Bohaiornis (Hu et al., 2011), Zhouornis (Zhang et al., 2013), Parabohaiornis, and Longusunguis (Wang et al., 2014), the omal end is blunt and laterally expanded. Sternum: The sternum is preserved in dorsal view (Fig. 5). It has a rounded rostral margin; the transverse dimension exceeds the longitudinal dimension from the rostral margin to the base of the xiphoid process. The shape of the sternum is similar in Longipteryx (Zhang et al., 2001) and Eocathayornis (Zhou, 2002), but in Eoenantiornis (Zhou et al., 2005) and Bohaiornis (Hu et al., 2011) the sternum is subcircular. The sternum of Zhouornis bears angular craniolateral margins (Zhang et al., 2013) rather than the rounded rostral margin present here. The caudal margin of the sternum along the midline forms a strap-shaped xiphoid process. The minimum width of the xiphoid process exceeds that of the caudolateral processes, whereas the xiphoid and caudolateral processes are subequal in width in most other enantiornithines including Longipteryx (Zhang et al., 2001), Eocathayornis (Zhou,
2002), Bohaiornis (Hu et al., 2011), and Parabohaiornis (Wang et al., 2014). The caudolateral processes extend almost as far caudally as the xiphoid process. Their distal ends are only slightly mediolaterally expanded as in Longipteryx (Zhang et al., 2001), in contrast to the more obvious expansion in many other enantiornithines including Cathayornis (Zhou and Hou, 2002), Bohaiornis (Hu et al., 2011), Zhouornis (Zhang et al., 2013), and Parabohaiornis (Wang et al., 2014). The xiphoid process forms a smaller angle with the caudolateral process than in Parabohaiornis (Wang et al., 2014). The medial processes are well-developed compared to most enantiornithines, similar to Eoenantiornis (Zhou et al., 2005), and they are oriented slightly medially and taper. Forelimb: As in most known enantiornithines other than Longipteryx (Zhang et al., 2001) and Pengornis (Zhou et al., 2008) which have much longer forelimbs than hind limbs, the forelimb (humerus þ ulna þ carpometacarpus) and hind limb (femur þ tibiotarsus þ tarsometatarsus) are subequal in length (see Table 1). Both left and right humeri are exposed in caudal view. The proximal surface of the humeral head is relatively flat as in Otogornis (Hou, 1994) and Zhouornis (Zhang et al., 2013) (Fig. 6), rather than prominently convex as in Pengornis (Zhou et al., 2008) or
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Fig. 6. Close-up photographs of the forelimb of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). A, right humerus; B, left ulna and radius; C, right ulna. Arrow indicates the groove which separates the dorsal cotyla from the olecranon. The anatomical abbreviations are explained in the text. Scale bar: 1 cm.
concave as in many other enantiornithines such as Cathayornis (Zhou and Hou, 2002), most bohaiornithids (Hu et al., 2011), and the specimens from the Upper Cretaceous of the El Brete in Argentina (Chiappe and Walker, 2002). The deltopectoral crest extends along the proximal third of the humerus and is
approximately half the width of the shaft. The deltopectoral crest gently recedes distally as in most other enantiornithines rather than ending abruptly as in Shenqiornis (Wang et al., 2010), Sulcavis (O'Connor et al., 2013), and Longusunguis (Wang et al., 2014). The ventral tubercle is considerably elongated and strongly curved
Fig. 7. Close-up photographs and line drawing of the pelvic girdle of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). A, left pelvic girdle; B and C, right pelvic girdle. Arrows indicate the supratrochanteric process on the dorsal edge of the ilium above the acetabulum and the groove along the ventrolateral surface of the ischium. The anatomical abbreviations are explained in the text. Scale bar: 1 cm.
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Fig. 8. Close-up photograph of the left tarsometatarsus of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). The arrow indicates the articular facet of metatarsal I. The anatomical abbreviations are explained in the text. Scale bar: 1 cm.
medially. It is separated from the humeral head by a wide and shallow capital incision. The distal end of the humerus is compressed craniocaudally and slightly curved laterally. The distal margin of the humerus is angled ventrally as in other enantiornithines. The flexor process and olecranon fossa are well-developed. The ulna is slightly longer than the humerus, with a caudally convex proximal half and a straight distal half (Fig. 6). The dorsal cotyla is separated from the olecranon by a groove. The radius is relatively straight and is about half as wide as the ulna. It appears to bear a shallow groove along the interosseous surface, as in some other enantiornithines (Chiappe and Walker, 2002). The ulnare and radiale are too poorly preserved to yield clear morphological information. The manus is also poorly preserved, but the right metacarpals are nearly complete. They are separated from each other, and the distal end of the major metacarpal is overlaid by the right humerus. The metacarpals are not proximally co-ossified with each other or with the semilunate carpal, as these elements are physically separated from each other on each manus (Figs. 1e2, 6), suggesting that the specimen is not fully mature. The alular metacarpal is rectangular. The major metacarpal is of approximately constant diameter throughout its length and is relatively straight. The minor metacarpal tapers distally and curves. Only the right alular digit, which bears a robust and curved ungual, is completely preserved among the manual digits. The first phalanx tapers distally and curves. Table 1 Measurements (mm) of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOLAB00032). Forelimb length, humerus þ ulna þ carpometacarpus; hind limb length, femur þ tibiotarsus þ tarsometatarsus; *, estimated length. Pygostyle length Scapula length Furcula length Coracoid length Basal width Sternum length Max width Forelimb length Humerus length Ulna length Mid-shaft width Radius length Mid-shaft width Metacarpal length Manual phalanx length Ilium length Pubis length Ischium length Hind limb length Femur length Tibia length Fibula length Metatarsus length Pedal phalanx length
22.5 >38 32 28 14 23 (sternal plate) 34 (total) 30 126.5 51 53 3.5 49 2.5 5.5, 21.5*, 22.5(I, II, III) 11, 4.5 (I-1, I-2) 29 36 20 120.5 43 50.5 20.5 6.5, 24.5, 27, 25 (IeIV) 7, 9 (I-1, I-2) 9 (ungual of II, III or IV)
Pelvic girdle: The cranial and caudal ends of the left ilium are missing (Fig. 7). The right ilium is completely preserved, but it is overlain by a thick sheet of what seems to be preserved soft tissue (Fig. 4). The preacetabular portion of the ilium is lobe-shaped cranially, and apparently is longer than the postacetabular portion, which is triangular and tapers caudally. The ilium has a prominent supratrochanteric process above the acetabulum, and the pubic pedicel is much more strongly expanded than the ischiadic pedicel. The anti-trochanter is well-developed and relatively prominent in the vicinity of the junction between the ilium and ischium. The pubis is about 125% of the ilium's length, and it is slender and strongly curved caudally. The proximal portion of the pubis has a subcircular cross-section, whereas the distal portion is compressed dorsoventrally. The pubic foot is small. The left ischium is missing the caudal end (Fig. 7), and the right ischium is completely preserved. The ischium is about two-thirds the length of the pubis, and is mediolaterally compressed. The proximal part of the ischium is broad, and the distal part tapers and curves caudally. A large process extends dorsally to contact the ventral margin of the postacetabular ilium, demarcating an ilioischiadic fenestra as in other enantiornithines such as Longipteryx (Zhang et al., 2001), Sinornis (Sereno et al., 2002), Qiliania (Ji et al., 2011), and specimen PVL4032-3 from the Upper Cretaceous of the El Brete in Argentina (Chiappe and Walker, 2002). A distinct groove is present along the ventrolateral surface of the distal half of the right ischium as seen in the ischium of Bohaiornis (Hu et al., 2011), but in Yuanjiawaornis this groove extends further proximally (Fig. 7). Hind limb: The femur is slightly bowed cranially. The proximal end of the femur forms a distinct head and neck (Figs. 1e2, 4). The distal end of the femur is poorly preserved yielding no additional morphological information. The tibiotarsus measures slightly less than 120% of the femoral length, and bears a prominent fibular crest (Figs. 1e2). The proximal tarsals are completely fused to the distal end of the tibia in caudal view. The fibula is short, about 30% of the tibiotarsus length, proximally robust and rapidly tapering as in Bohaiornis (Hu et al., 2011) and Longusunguis (Wang et al., 2014). However, the fibula extends distally to approach the tarsal joint in Pengornis (Zhou et al., 2008) and Zhouornis (Zhang et al., 2013). Metatarsal I is P-shaped in medial view, and its long axis is not twisted medially or laterally in cranial view as in Soroavisaurus (Chiappe, 1993) and Neuquenornis (Chiappe and Calvo, 1994). Metatarsal I is compressed craniolaterally and pointed proximally, likely abutting on the medioplantar surface of metatarsal II, as indicated by a distinctive articular facet proximal to the distal articulation of metatarsal II (Fig. 8). Metatarsals IIeIV are proximally fused together, and are compressed mediolaterally just proximal to their distal ends. Metatarsal II is clearly the widest of the metatarsals, while metatarsal IV is the narrowest and metatarsal III the longest. Metatarsal II is longer than metatarsal IV, whereas both are subequal in length in Zhouornis (Zhang et al., 2013). The medial rim of the metatarsal III trochlea projects further plantarly than the lateral rim, as in Soroavisaurus (Chiappe, 1993) and Neuquenornis (Chiappe and Calvo, 1994). The trochlea of
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metatarsal IV is nonginglymous, reduced to a single condyle. Among the pedal digits, only the right hallux is completely preserved. The hallucal ungual appears to be robust and strongly curved. Another preserved ungual, which appears to belong to a pedal digit other than the hallux, is more slender and less curved than the hallucal ungual. 3. Discussion The sacral vertebrae are co-ossified into a synsacrum and the proximal tarsals are fused to the tibia, suggesting that PMOLAB00032 is relatively mature. However, the semilunate carpal is incompletely fused to the metacarpals, suggesting that the individual was not fully mature. These features combined suggest that the holotype specimen is a sub-adult. Yuanjiawaornis displays the following enantiornithine synapomorphies: parapophyses located in central position of dorsal vertebrae; coracoid with convex articular facet for scapula and broad dorsal fossa; Y-shaped furcula with long hypocleideum; sternum with parabolic anterior margin and paired caudolateral processes; radius with longitudinal groove along interosseous surface; metatarsal II transversely wider than metatarsal III, which is in turn wider than metatarsal IV (Chiappe, 2002; Chiappe and Walker, 2002). These features strongly support the identification of Yuanjiawaornis as an enantiornithine. The robust and strongly curved hallux claw and the long unguals of the other pedal digits suggest that Yuanjiawaornis was likely arboreal, like most Early Cretaceous enantiornithine birds (Zhou and Zhang, 2006a). Among the known enantiornithines, Yuanjiawaornis is most similar in size and in limb segment proportions to the known bohaiornithids Shenqiornis (Wang et al., 2010), Bohaiornis (Hu et al., 2011), Sulcavis (O'Connor et al., 2013), Zhouornis (Zhang et al., 2013), Parabohaiornis (Wang et al., 2014), and Longusunguis (Wang et al., 2014). Several unique morphological characters are combined to distinguish the bohaiornithids from other enantiornithines (Wang et al., 2014): robust rostrum with large and subconical teeth; pygostyle gently tapered distally; omal tips of furcula expanded laterally; short and robust tarsometatarsus; and long pedal unguals. Yuanjiawaornis has a similar pygostyle with the bohaiornithids, whereas the omal tips of its furcula taper in dorsal view as in other enantiornithines Eoenantiornis and Pengornis, rather than laterally expand as in the bohaiornithids. Yuanjiawaornis is also clearly different from the bohaiornithids in having the following character states: ventral surface of synsacrum longitudinally grooved (ridged in Bohaiornis and Parabohaiornis); transverse processes of the most caudal sacral vertebra relatively robust and long (transverse processes of penultimate sacral vertebra relatively robust and long in Zhouornis, Parabohaiornis, and Longusunguis); acromion process tapered craniodorsally (nearly parallels to the shaft of scapula in all bohaiornithids except for Longusunguis, which has a similar scapula with Yuanjiawaornis); lateral margin of coracoid straight (strongly convex in Shenqiornis, Sulcavis, and Longusunguis); clavicular ramus medially curved (straight in all bohaiornithids except for Longusunguis, in which both clavicular rami are not exposed); sternum shorter longitudinally than transversely, with slightly expanded distally caudolateral processes (distal end of caudolateral process strongly expanded into an asymmetrical triangle in Bohaiornis, Zhouornis, and Parabohaiornis); proximal surface of humeral head flat (concave in all bohaiornthids except for Zhouornis, which has a flat proximal surface of humeral head as in Yuanjiaornis); and deltopectoral crest gently recedes distally (abruptly ends distally in Shenqiornis, Sulcavis and Longusunguis). Yuanjiawaornis differs from Pengornis mostly in its limb proportions (Table 2). The femur of Yuanjiawaornis is slightly shorter than that of Pengornis, but the tibiotarsus and
tarsometatarsus are subequal in length between both. In Pengornis, the ulna, as well as the humerus, is much longer than the tibiotarsus, whereas the three elements are subequal in length in Yuanjiawaornis. Additionally, the fibula of Pengornis extends distally to meet the proximal tarsals as in Zhouornis (Zhang et al., 2013), whereas the bone is less than half the length of the tibiotarsus in Yuanjiawaornis. The observed differences in proportions are unable to be explained from individual variation and different ontogenetic stages within species, and they most likely represent interspecific variation. Therefore, this combination of the features (above), along with the holotype's large size, subequal forelimb and hind limb lengths, further distinguishes Yuanjiawaornis from all other enantiornithines. The discovery of Yuanjiawaornis, in combination with new data from other enantiornithines, sheds light on the sacral morphology of enantiornithines. The sacrum of most known basal birds, such as confuciusornithids and sapeornithids (Zhang et al., 2008; Provini et al., 2009), and ornithuromorphans such as Archaeorhynchus (Zhou and Zhang, 2006b), Gansus (You et al., 2006), Apsaravis (Clarke and Norell, 2002), and Ichthyornis (Clarke, 2004) all seem to share one morphological feature: the middle sacral vertebrae are considerably wider than the anterior and posterior ones, implying a strengthened sacrum. This feature is also seen in some deinonychosaurs, although to a less degree (Xu et al., 2000; Xu et al., 2002), suggesting that this is a primitive feature for Aves. Among known Early Cretaceous enantiornithines, the recently reported Rapaxavis (O'Connor et al., 2010), Bohaiornis (Hu et al., 2011), Parabohaiornis (Wang et al., 2014), and the referred specimen of Zhouornis BMNHC Ph 756 (Zhang et al., 2014) have a completely preserved and ventrally exposed sacrum, as in Yuanjiawaornis. These Early Cretaceous enantiornithines appear to have a reduced sacrum with the middle sacral vertebrae transversely thinner than the cranial and caudal articular ends of the synsacrum. In Rapaxavis, the cranial one-third of the sacral centra are distinctly thinner than the cranial articular surface. The caudal two-thirds appears to be strongly compressed dorsoventrally and seems to be slightly widened. Examination of the holotype, however, suggests this dorsoventral compression and the groove on the caudal two-thirds of the ventral surface may be a result of postmortem crushing. Among known Late Cretaceous enantiornithines, only Elbretornis has a nearly complete synsacrum, although the cranial centrum is partly damaged (Walker and Dyke, 2010). The middle centra of the synsacrum appear to be narrow and the cranial articular surface seems to be broader than the middle centra as in the Early Cretaceous enantiornithines. Zhyraornis kashkarovi (Nessov, 1984), Zh. logunovi (Nessov, 1992) and Lenesornis maltshevskyi (Nessov, 1986) are Late Cretaceous enantiornithines identified only on the basis of isolated and incompletely preserved synsacra (Kurochkin, 2000). Narrow middle centra and a broader cranial centrum are also present in the synsacrum of Lenesornis (Nessov, 1986). These features support the identification of Zhyraornis and Lenesornis as enantiornithines. However, further discoveries of new specimens are necessary to clarify whether or not the morphological structures seen in the synsacral centra of many enantiornithines is a diagnostic Table 2 Comparative measurements (mm) of selected enantiornithine birds. Taxon
hu
ul
cmc
fe
ti
tmt
fl/hl
Yuanjiawaornis viriosus 51(r) 53(r) 24*(r) 43(r) 50.5(l) 27(l) 1.06 (PMOL AB00032) Bohaiornis guoi 47(l) 48(l) 22.3(l) 39(r) 46(r) 22.5(r) 1.09 (PMOL AB00167) 64.3(l) 70.7(l) 34.3(r) 48(r) 50.4(r) 26.5(r) 1.36 Pengornis houi (IVPP V15336) See text for abbreviations. *, estimated length; l and r, left and right sides.
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for the clade or for a less inclusive group within that clade. The fact that the cranial and caudal articular surfaces of the synsacrum are wider than the other centra in the enantiornithines likely results from a combination of reduction of the main part of the sacrum and retention of a large surface for articulation with the dorsal and caudal vertebra. Enantiornithines have a relatively large bony tail that consists of expanded and elongated free caudal vertebrae and pygostyle. Therefore, a large caudal articular surface of the synsacrum is necessary to increase the functional load of the tail vertebrae and the feathers they bore (Zelenkov and Averianov, 2011). 4. Conclusion During the last two decades, over ten enantiornithine taxa have been reported from the Lower Cretaceous deposits of western Liaoning in northeastern China, and the description of Yuanjiawaornis viriosus increases the taxonomic and morphological diversity known in the Lower Cretaceous Jiufotang Formation of this area. This new species provides additional morphological information about enantiornithines, and further suggests that enantiornithines might have a uniquely shaped synsacrum among birds. Acknowledgments We thank the field crew of PMOL for collecting and preparing this specimen, Sullivan C., O'Connor J. K., Falk A. and Stidham T. for their helpful suggestions on earlier draft, E. Jagt-Yazykova for their careful edits, and the reviewers for their review and helpful comments. This research was supported by the National Natural Science Foundation of China (41172026, 41120124002), and Natural Science Foundation (201102199) and Education Bureau Foundation (LR2012038) of Liaoning Province. X. Xu's work was also supported by the Special Funds for the Major State Basic Research Projects of China. References Chiappe, L.M., 1993. Enantiornithine (Aves) tarsometatarsi from the Cretaceous Lecho Formation of northwestern Argentina. American Museum Novitates 3083, 1e27. Chiappe, L.M., 2002. Early bird phylogeny: problems and solutions. In: Chiappe, L.M., Witmer, L.M. (Eds.), Mesozoic Birds: Above the Heads of Dinosaurs. University of California Press, Berkeley, California, pp. 448e472. Chiappe, L.M., Calvo, J.O., 1994. Neuquenornis volans, a new Late Cretaceous bird (Enantiornithes: Avisauridae) from Patagonia, Argentina. Journal of Vertebrate Paleontology 14, 230e246. Chiappe, L.M., Walker, C.A., 2002. Skeletal morphology and systematics of the Cretaceous Euenantiornithes (Ornithothoraces: Enantiornithes). In: Chiappe, L.M., Witmer, L.M. (Eds.), Mesozoic Birds: Above the Heads of Dinosaurs. University of California Press, Berkeley, California, pp. 240e267. Clarke, J.A., 2004. Morphology, phylogenetic taxonomy, and systematics of Ichthyornis and Apatornis (Avialae: Ornithurae). Bulletin of the American Museum of Natural History 286, 1e179. Clarke, J.A., Norell, M.A., 2002. The morphology and phylogenetic position of Apsaravis ukhaana from the Late Cretaceous of Mongolia. American Museum Novitates 3387, 1e46. Duan, Y., Zhang, L., Li, L., Cheng, S., 2006. Division and correlation of unique fossil-bearing beds of Jiufotang Formation in Dapingfang-Meileyingzi Basin of western Liaoning. Global Geology 25, 113e119 [Chinese with English abstract]. Hou, L., 1994. A Late Mesozoic bird from Inner Mongolia. Vertebrata PalAsiatica 32, 258e266 [Chinese with English abstract]. Hou, L., Zhou, Z., Gu, Y., Zhang, H., 1995. Confuciusornis sanctus, a new Late Jurassic sauriurine bird from China. Chinese Science Bulletin 40, 1545e1551. Hu, D., Li, L., Hou, L., Xu, X., 2010. A new sapeornithid bird from China and its implication for early avian evolution. Acta Geologica Sinica 84, 472e482. Hu, D., Li, L., Hou, L., Xu, X., 2011. A new enantiornithine bird from the Lower Cretaceous of western Liaoning, China. Journal of Vertebrate Paleontology 31, 154e161.
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Cretaceous Research journal homepage: www.elsevier.com/locate/CretRes
Yuanjiawaornis viriosus, gen. et sp. nov., a large enantiornithine bird from the Lower Cretaceous of western Liaoning, China Dongyu Hu a, b, *, Ying Liu a, Jinhua Li a, Xing Xu a, b, c, Lianhai Hou a, c a
Paleontological Institute of Shenyang Normal University, 253 North Huanghe Street, Shenyang 110034, China Key Laboratory for Evolution of Past Life in Northeast Asia, Ministry of Land and Resources (Shenyang Normal University), Shenyang 110034, China c Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 142 Xiwai Street, Beijing 100044, China b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 18 March 2013 Accepted in revised form 28 February 2015 Available online
Here we describe a new enantiornithine bird, Yuanjiawaornis viriosus gen. et sp. nov., based on a nearly complete, mostly articulated postcranial skeleton from the Lower Cretaceous Jiufotang Formation (120 Ma) of western Liaoning Province, northeastern China. It is similar in size to large bohaiornithids among the known Early Cretaceous enantiornithines; only Pengornis houi is larger. The semilunate carpal is incompletely fused to the metacarpals, suggesting that the holotype specimen was not fully mature at the time of death. The new specimen is distinguishable from other known enantiornithines by a unique combination of features including large body size, forelimb and hind limb subequal in length, a longitudinally grooved ventral surface of the synsacrum, robust and long transverse processes of the caudalmost sacral vertebra, a craniodorsally tapered acromion process of the scapula, a straight lateral margin of the coracoid, medially curved clavicular rami with tapered omal tips, a sternum that is oval in outline with slightly expanded distally caudolateral processes, a humeral head with a flat proximal surface, and a humerus with a deltopectoral crest that gradually decreases in height distally. A comparative analysis of some sacral features of basal birds including this taxon suggests that enantiornithines might have a uniquely shaped synsacrum, although more data is needed to confirm that hypothesis. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Enantiornithes Yuanjiawaornis viriosus Lower Cretaceous Liaoning China
1. Introduction Most known Early Cretaceous enantiornithine birds are small e about the size of a living sparrow or starling. They are much smaller than contemporaneous basal birds such as Confuciusornis sanctus (Hou et al., 1995) and ornithuromorph birds such as Yixianornis grabaui (Zhou and Zhang, 2001). The discovery of the largest known Early Cretaceous enantiornithine Pengornis houi (Zhou et al., 2008), greatly increased the upper bound of the size range of Early Cretaceous enantiornithines, and indicates a greater overlap in body size range among the three major categories of Early Cretaceous birds: basal birds, Enantiornithes, and Ornithuromorpha. Since the description of Pengornis, several large and medium sized enantiornithines have been reported from the Jehol deposits:
* Corresponding author. Paleontological Institute of Shenyang Normal University, 253 North Huanghe Street, Shenyang 110034, China. E-mail addresses: [email protected] (D. Hu), [email protected] (Y. Liu), [email protected] (J. Li), [email protected] (X. Xu), houlianhai@ synu.edu.cn (L. Hou). http://dx.doi.org/10.1016/j.cretres.2015.02.013 0195-6671/© 2015 Elsevier Ltd. All rights reserved.
Shenqiornis mengi (Wang et al., 2010), Bohaiornis guoi (Hu et al., 2011), Sulcavis geeorum (O'Connor et al., 2013), Zhouornis hani (Zhang et al., 2013), Parabohaiornis martini (Wang et al., 2014) and Longusunguis kurochkini (Wang et al., 2014), and those species comprise the Family Bohaiornithidae (Wang et al., 2014). Adding to this diversity, we report a new Early Cretaceous enantiornithine bird based on a specimen collected during the 2005 field season from the lacustrine beds of Dapingfang Town, Chaoyang County, western Liaoning Province. The new specimen is approximately the same size as Zhouornis hani among the bohaiornithids and only slightly smaller than Pengornis houi. We believe this specimen represents a new taxon (described below) and has implications for a greater understanding of enantiornithine morphology. Anatomical abbreviations: Ac, acromion process; cav, caudal vertebra; cmc, carpometacarpus; dv, dorsal vertebra; fe, femur; fl, the length of humerus þ ulna þ carpometacarpus; fu, furcula; ga, gastralia; gl, glenoid facet; hl, the length of femur þ tibiotarsus þ tarsometatarsus; hu, humerus; lco, left coracoid; lfe, left femur; lfi, left fibula; lhu, left humerus; lil, left ilium; lis, left ischium; lmc-III, left minor metacarpal; lpu, left pubis; lr, left radius; lra, left radiale; lsc; left scapula; lti, left
D. Hu et al. / Cretaceous Research 55 (2015) 210e219
tibiotarsus; ltm, left tarsometatarsus; lu, left ulna; mph, manual phalanx; mt-II-IV, the second to forth metatarsals; ns, neural spine; pa, parapophysis; pph, pedal phalanx; py, pygostyle; rco, right coracoid; rfe, right femur; rfi, right fibula; rhu, right humerus; ri, rib; ril, right ilium; ris, right ischium; rmc-I-III, right alular, major and minor metacarpals; rmtI, right first metatarsal; rr, right radius; rra, right radiale; rpu, right pubis; rsc, right scapula; rtm, right tarsometatarsus; rti, right tibiotarsus; ru, right ulna; rul, right ulnare; ns, neural spine; st, sternum; sy, synsacrum; ti, tibiotarsus; tmt, tarsometatarsus; tp, transverse process; ul, ulna; un, ungual; I, alular digit; i, hallux digit. Institutional Abbreviations: BMNHC, Beijing Natural History Museum, China; CNU, Capital Normal University, Beijing, China; IVPP, Institute of Vertebrate Paleontology and Paleoanthropology, Beijing, China; PMOL, Paleontological Museum of Liaoning, China.
2. Systematic palaeontology Aves Linnaeus, 1758 Enantiornithes Walker, 1981 Yuanjiawaornis, gen. nov. Derivation of name: Yuanjiawao, name of type locality and strata, and Greek, ornis, bird. Type species: Yuanjiawaornis viriosus, type by monotypy. Diagnosis: Yuanjiawaornis differs from other enantiornithines including Pengornis and bohaiornithids by a unique combination of the following characters: large size (but smaller than Pengornis); forelimb and hind limb subequal in length (forelimb much longer than hind limb in Pengornis); ventral surface of synsacrum grooved longitudinally (ridged in bohaiornithids Bohaiornis and Parabohaiornis); transverse processes of caudal-most sacral vertebra robust and long (transverse processes of penultimate sacral vertebra robust and long in bohaiornithids Zhouornis, Parabohaiornis, and Longusunguis); acromion process tapered craniodorsally (acromion process nearly parallels to the shaft of scapular in all bohaiornithids except for Longusunguis); lateral margin of coracoid straight (strongly convex in Pengornis and bohaiornithids Shenqiornis, Sulcavis, and Longusunguis); clavicular rami medially curved and omal tips tapered (clavicular rami straight and omal tips expanded laterally in bohaiornithids); sternum oval in outline with caudolateral processes slightly expanded distally (caudolateral processes strongly expanded distally in most bohaiornithids, and craniolateral margin of sternum angular in Zhouornis); humeral head flat (convex in Pengornis and concave in all bohaiornithids except for Zhouornis) and deltopectoral crest gradually decreased in height distally (abruptly decreased distally in Shenqiornis, Sulcavis, and Longusunguis). Yuanjiawaornis viriosus sp. nov. Figs. 1e8, Table 1 Derivation of name: Latin, viriosus, vigorous. Type specimen: PMOL (Paleontological Museum of Liaoning) AB00032, a nearly complete and mostly articulated postcranial skeleton, missing the skull, cervical and cranial thoracic vertebrae, and most of the manual and pedal digits. Stratigraphic horizon and type locality: The Yuanjiawa Beds of Jiufotang Formation (120 Ma), Lower Cretaceous (Duan et al., 2006); Yuanjiawa Village, Dapingfang Town, Chaoyang County, Liaoning Province, China (Hu et al., 2010). Diagnosis: As for the genus. Description and comparisons: Axial skeleton: Seven thoracic vertebrae are present in articulation (Fig. 3). They are amphicoelous and bear prominent groove-like
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lateral excavations, as in most other enantiornithines (Chiappe and Walker, 2002). The parapophysis is centrally located on each centrum, as in other enantiornithines (Wang et al., 2014). The prezygapophysis extends cranially beyond the cranial margin of the centrum, and the postzygapophysis extends caudally to the level of the caudal margin of the centrum. In Shenqiornis (Wang et al., 2010) and Longusunguis (Wang et al., 2014), the postzygapophysis is longer than the prezygapophysis, extending caudally beyond the caudal margin of the centrum. The tips of the neural spines are craniocaudally expanded and contact one another as in Longusunguis (Wang et al., 2014) and the Late Cretaceous El Brete specimens from Argentina (Chiappe and Walker, 2002). Seven sacral vertebrae are present as in Pengornis (Zhou et al., 2008), Parabohaiornis (Wang et al., 2014), and the referred specimen of Zhouornis BMNHC Ph 756 (Zhang et al., 2014), and the vertebrae are fully co-ossified into a synsacrum (Fig. 4). The cranial articular surface of the synsacrum is round and distinctly concave; it is slightly broader than the caudal articular surface, but significantly wider than other middle centra as in Bohaiornis (Hu et al., 2011), Parabohaiornis (Wang et al., 2014), and the referred specimen of Zhouornis BMNHC Ph 756 (Zhang et al., 2014). However, in Bohaiornis and Parabohaiornis, the central synsacrum is more compressed transversely, forming a prominent ventral keel. A sharp groove runs longitudinally along the whole ventral surface of the synsacrum in the holotype. A similar groove is also reported in the synsacrum of Rapaxavis (O'Connor et al., 2010) and the referred specimen of Zhouornis BMNHC Ph 756 (Zhang et al., 2014), but the groove is shallow and limited in the distal two-thirds of the synsacrum in those taxa. The transverse processes of the most caudal sacral vertebra are the longest and most robust. The transverse processes are more delicate than those of the sixth sacral vertebra in Parabohaiornis (Wang et al., 2014), Longusunguis (Wang et al., 2014), and the referred specimen of Zhouornis BMNHC Ph 756 (Zhang et al., 2014). Six free caudal vertebrae are discernible, and they are amphicoelous with long, caudolaterally directed transverse processes. A caudal vertebra exposed in dorsal view and inferred to be from the cranial part of the tail bears a tall spinous process and its prezygapophyses are longer than the postzygapophyses. The pygostyle appears to be compressed mediolaterally and tapered caudally in lateral view. A ridge that is formed by the fused transverse processes, runs along the lateral surface decreasing in height distally, as in other enantiornithines such as Bohaiornis (Hu et al., 2011) and Sulcavis (O'Connor et al., 2013). The pygostyle is significantly shorter than metatarsal III as in most other enantiornithines, but contrasts with the state in Longusunguis where the opposite is true (Wang et al., 2014). At least five pairs of thoracic ribs are preserved, but they do not have uncinate processes (Figs. 1e2). At least three pairs of gastral ribs are also present. Thoracic girdle: Both scapulae are exposed in lateral view (Fig. 5). The acromion process of the left scapula is broken from the shaft and preserved in dorsal view, and the distal half of the shaft is missing. The distal end of the right scapula is concealed by ribs. The exposed shafts of the scapulae are straight. The acromion process tapers craniodorsally as in Enantiornis (Walker and Dyke, 2010) and Longusunguis (Wang et al., 2014), rather being nearly parallel to the shaft in Bohaiornis (Hu et al., 2011), Sulcavis (O'Connor et al., 2013), Shenqiornis (Wang et al., 2010), Zhouornis (Zhang et al., 2013), and Parabohaiornis (Wang et al., 2014). The acromion process is approximately as long as the glenoid facet, and its mediolateral width greatly exceeds its dorsoventral depth. The coracoid is strutlike and relatively short, with a length/maximum width ratio of 2.0, as in most Early Cretaceous enantiornithines including Pengornis and Bohaiornis (Fig. 5). The small acrocoracoid process, flat humeral glenoid and convex scapular facet are nearly aligned along an
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Fig. 1. Photograph of holotype specimen of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). Scale bar: 2 cm.
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Fig. 2. Line drawing of holotype specimen of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). The anatomical abbreviations are explained in the text. Scale bar: 2 cm.
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Fig. 3. Close-up photograph and line drawing of the dorsal vertebrae of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). The anatomical abbreviations are explained in the text. Scale bar: 0.5 cm.
Fig. 4. Close-up photograph of the synsacrum of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). The anatomical abbreviations are explained in the text. Scale bar: 0.5 cm.
omalesternal axis, as in other enantiornithines (Chiappe and Walker, 2002). Although the left and right coracoids are partly covered by the left and right scapulae, most of the dorsal surfaces of both coracoids are exposed. The lateral margin of the sternal half of the coracoid is nearly straight, in contrast to the strongly convex margin seen in many other enantiornithines such as Eoenantiornis (Zhou et al., 2005), Pengornis (Zhou et al., 2008), Shenqiornis (Wang et al., 2010), Sulcavis (O'Connor et al., 2013), and Longusunguis (Wang et al., 2014), and the slightly convex margin present in Bohaiornis (Hu et al., 2011) and Parabohaiornis (Wang et al., 2014). The medial margin of the sternal half of the coracoid also is nearly straight, in contrast to the convex margin seen in Sulcavis (O'Connor et al., 2013) and Parabohaiornis (Wang et al., 2014). A broad shallow fossa is present on the dorsal surface of the coracoid. No supracoracoid foramen is visible, but it is possible that this structure is covered by the scapula. The furcula is Y-shaped, with an interclavicular angle of about 45 and a long hypocleideum (Fig. 5). The interclavicular angle in similar enantiornithines, such as Bohaiornis, Sulcavis and Parabohaiornis is about 60 (Hu et al., 2011; O'Connor et al., 2013; Wang et al., 2014). The clavicular rami are medially curved; the lateral margin of the ramus is strongly convex and the medial margin is slightly concave. In contrast, the clavicular rami are straight in most other enantiornithines including Bohaiornis, Sulcavis, and Zhouornis (Hu et al., 2011; O'Connor et al., 2013; Wang et al., 2014). The dorsolateral surface of the clavicular ramus is strongly excavated so that the dorsal surface is much narrower than the ventral surface. However, in Bohaiornis (Hu et al., 2011) and Zhouornis (Zhang et al., 2014), the dorsal surface deepens towards the omal tip so that the dorsal surface is much wider than the ventral surface in the omal half. The thinner dorsal margin
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Fig. 5. Close-up photograph and line drawing of the pectoral girdle of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). The anatomical abbreviations are explained in the text. Scale bar: 1 cm.
continues along the hypocleidium, giving the hypocleidium a Tshaped cross section. The omal end has a bulbous dorsal expansion and bears a concave articular facet for the acromion process of the scapula on its dorsal surface. However, in Bohaiornis (Hu et al., 2011), Zhouornis (Zhang et al., 2013), Parabohaiornis, and Longusunguis (Wang et al., 2014), the omal end is blunt and laterally expanded. Sternum: The sternum is preserved in dorsal view (Fig. 5). It has a rounded rostral margin; the transverse dimension exceeds the longitudinal dimension from the rostral margin to the base of the xiphoid process. The shape of the sternum is similar in Longipteryx (Zhang et al., 2001) and Eocathayornis (Zhou, 2002), but in Eoenantiornis (Zhou et al., 2005) and Bohaiornis (Hu et al., 2011) the sternum is subcircular. The sternum of Zhouornis bears angular craniolateral margins (Zhang et al., 2013) rather than the rounded rostral margin present here. The caudal margin of the sternum along the midline forms a strap-shaped xiphoid process. The minimum width of the xiphoid process exceeds that of the caudolateral processes, whereas the xiphoid and caudolateral processes are subequal in width in most other enantiornithines including Longipteryx (Zhang et al., 2001), Eocathayornis (Zhou,
2002), Bohaiornis (Hu et al., 2011), and Parabohaiornis (Wang et al., 2014). The caudolateral processes extend almost as far caudally as the xiphoid process. Their distal ends are only slightly mediolaterally expanded as in Longipteryx (Zhang et al., 2001), in contrast to the more obvious expansion in many other enantiornithines including Cathayornis (Zhou and Hou, 2002), Bohaiornis (Hu et al., 2011), Zhouornis (Zhang et al., 2013), and Parabohaiornis (Wang et al., 2014). The xiphoid process forms a smaller angle with the caudolateral process than in Parabohaiornis (Wang et al., 2014). The medial processes are well-developed compared to most enantiornithines, similar to Eoenantiornis (Zhou et al., 2005), and they are oriented slightly medially and taper. Forelimb: As in most known enantiornithines other than Longipteryx (Zhang et al., 2001) and Pengornis (Zhou et al., 2008) which have much longer forelimbs than hind limbs, the forelimb (humerus þ ulna þ carpometacarpus) and hind limb (femur þ tibiotarsus þ tarsometatarsus) are subequal in length (see Table 1). Both left and right humeri are exposed in caudal view. The proximal surface of the humeral head is relatively flat as in Otogornis (Hou, 1994) and Zhouornis (Zhang et al., 2013) (Fig. 6), rather than prominently convex as in Pengornis (Zhou et al., 2008) or
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Fig. 6. Close-up photographs of the forelimb of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). A, right humerus; B, left ulna and radius; C, right ulna. Arrow indicates the groove which separates the dorsal cotyla from the olecranon. The anatomical abbreviations are explained in the text. Scale bar: 1 cm.
concave as in many other enantiornithines such as Cathayornis (Zhou and Hou, 2002), most bohaiornithids (Hu et al., 2011), and the specimens from the Upper Cretaceous of the El Brete in Argentina (Chiappe and Walker, 2002). The deltopectoral crest extends along the proximal third of the humerus and is
approximately half the width of the shaft. The deltopectoral crest gently recedes distally as in most other enantiornithines rather than ending abruptly as in Shenqiornis (Wang et al., 2010), Sulcavis (O'Connor et al., 2013), and Longusunguis (Wang et al., 2014). The ventral tubercle is considerably elongated and strongly curved
Fig. 7. Close-up photographs and line drawing of the pelvic girdle of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). A, left pelvic girdle; B and C, right pelvic girdle. Arrows indicate the supratrochanteric process on the dorsal edge of the ilium above the acetabulum and the groove along the ventrolateral surface of the ischium. The anatomical abbreviations are explained in the text. Scale bar: 1 cm.
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Fig. 8. Close-up photograph of the left tarsometatarsus of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOL-AB00032). The arrow indicates the articular facet of metatarsal I. The anatomical abbreviations are explained in the text. Scale bar: 1 cm.
medially. It is separated from the humeral head by a wide and shallow capital incision. The distal end of the humerus is compressed craniocaudally and slightly curved laterally. The distal margin of the humerus is angled ventrally as in other enantiornithines. The flexor process and olecranon fossa are well-developed. The ulna is slightly longer than the humerus, with a caudally convex proximal half and a straight distal half (Fig. 6). The dorsal cotyla is separated from the olecranon by a groove. The radius is relatively straight and is about half as wide as the ulna. It appears to bear a shallow groove along the interosseous surface, as in some other enantiornithines (Chiappe and Walker, 2002). The ulnare and radiale are too poorly preserved to yield clear morphological information. The manus is also poorly preserved, but the right metacarpals are nearly complete. They are separated from each other, and the distal end of the major metacarpal is overlaid by the right humerus. The metacarpals are not proximally co-ossified with each other or with the semilunate carpal, as these elements are physically separated from each other on each manus (Figs. 1e2, 6), suggesting that the specimen is not fully mature. The alular metacarpal is rectangular. The major metacarpal is of approximately constant diameter throughout its length and is relatively straight. The minor metacarpal tapers distally and curves. Only the right alular digit, which bears a robust and curved ungual, is completely preserved among the manual digits. The first phalanx tapers distally and curves. Table 1 Measurements (mm) of Yuanjiawaornis viriosus, gen. et sp. nov. (PMOLAB00032). Forelimb length, humerus þ ulna þ carpometacarpus; hind limb length, femur þ tibiotarsus þ tarsometatarsus; *, estimated length. Pygostyle length Scapula length Furcula length Coracoid length Basal width Sternum length Max width Forelimb length Humerus length Ulna length Mid-shaft width Radius length Mid-shaft width Metacarpal length Manual phalanx length Ilium length Pubis length Ischium length Hind limb length Femur length Tibia length Fibula length Metatarsus length Pedal phalanx length
22.5 >38 32 28 14 23 (sternal plate) 34 (total) 30 126.5 51 53 3.5 49 2.5 5.5, 21.5*, 22.5(I, II, III) 11, 4.5 (I-1, I-2) 29 36 20 120.5 43 50.5 20.5 6.5, 24.5, 27, 25 (IeIV) 7, 9 (I-1, I-2) 9 (ungual of II, III or IV)
Pelvic girdle: The cranial and caudal ends of the left ilium are missing (Fig. 7). The right ilium is completely preserved, but it is overlain by a thick sheet of what seems to be preserved soft tissue (Fig. 4). The preacetabular portion of the ilium is lobe-shaped cranially, and apparently is longer than the postacetabular portion, which is triangular and tapers caudally. The ilium has a prominent supratrochanteric process above the acetabulum, and the pubic pedicel is much more strongly expanded than the ischiadic pedicel. The anti-trochanter is well-developed and relatively prominent in the vicinity of the junction between the ilium and ischium. The pubis is about 125% of the ilium's length, and it is slender and strongly curved caudally. The proximal portion of the pubis has a subcircular cross-section, whereas the distal portion is compressed dorsoventrally. The pubic foot is small. The left ischium is missing the caudal end (Fig. 7), and the right ischium is completely preserved. The ischium is about two-thirds the length of the pubis, and is mediolaterally compressed. The proximal part of the ischium is broad, and the distal part tapers and curves caudally. A large process extends dorsally to contact the ventral margin of the postacetabular ilium, demarcating an ilioischiadic fenestra as in other enantiornithines such as Longipteryx (Zhang et al., 2001), Sinornis (Sereno et al., 2002), Qiliania (Ji et al., 2011), and specimen PVL4032-3 from the Upper Cretaceous of the El Brete in Argentina (Chiappe and Walker, 2002). A distinct groove is present along the ventrolateral surface of the distal half of the right ischium as seen in the ischium of Bohaiornis (Hu et al., 2011), but in Yuanjiawaornis this groove extends further proximally (Fig. 7). Hind limb: The femur is slightly bowed cranially. The proximal end of the femur forms a distinct head and neck (Figs. 1e2, 4). The distal end of the femur is poorly preserved yielding no additional morphological information. The tibiotarsus measures slightly less than 120% of the femoral length, and bears a prominent fibular crest (Figs. 1e2). The proximal tarsals are completely fused to the distal end of the tibia in caudal view. The fibula is short, about 30% of the tibiotarsus length, proximally robust and rapidly tapering as in Bohaiornis (Hu et al., 2011) and Longusunguis (Wang et al., 2014). However, the fibula extends distally to approach the tarsal joint in Pengornis (Zhou et al., 2008) and Zhouornis (Zhang et al., 2013). Metatarsal I is P-shaped in medial view, and its long axis is not twisted medially or laterally in cranial view as in Soroavisaurus (Chiappe, 1993) and Neuquenornis (Chiappe and Calvo, 1994). Metatarsal I is compressed craniolaterally and pointed proximally, likely abutting on the medioplantar surface of metatarsal II, as indicated by a distinctive articular facet proximal to the distal articulation of metatarsal II (Fig. 8). Metatarsals IIeIV are proximally fused together, and are compressed mediolaterally just proximal to their distal ends. Metatarsal II is clearly the widest of the metatarsals, while metatarsal IV is the narrowest and metatarsal III the longest. Metatarsal II is longer than metatarsal IV, whereas both are subequal in length in Zhouornis (Zhang et al., 2013). The medial rim of the metatarsal III trochlea projects further plantarly than the lateral rim, as in Soroavisaurus (Chiappe, 1993) and Neuquenornis (Chiappe and Calvo, 1994). The trochlea of
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metatarsal IV is nonginglymous, reduced to a single condyle. Among the pedal digits, only the right hallux is completely preserved. The hallucal ungual appears to be robust and strongly curved. Another preserved ungual, which appears to belong to a pedal digit other than the hallux, is more slender and less curved than the hallucal ungual. 3. Discussion The sacral vertebrae are co-ossified into a synsacrum and the proximal tarsals are fused to the tibia, suggesting that PMOLAB00032 is relatively mature. However, the semilunate carpal is incompletely fused to the metacarpals, suggesting that the individual was not fully mature. These features combined suggest that the holotype specimen is a sub-adult. Yuanjiawaornis displays the following enantiornithine synapomorphies: parapophyses located in central position of dorsal vertebrae; coracoid with convex articular facet for scapula and broad dorsal fossa; Y-shaped furcula with long hypocleideum; sternum with parabolic anterior margin and paired caudolateral processes; radius with longitudinal groove along interosseous surface; metatarsal II transversely wider than metatarsal III, which is in turn wider than metatarsal IV (Chiappe, 2002; Chiappe and Walker, 2002). These features strongly support the identification of Yuanjiawaornis as an enantiornithine. The robust and strongly curved hallux claw and the long unguals of the other pedal digits suggest that Yuanjiawaornis was likely arboreal, like most Early Cretaceous enantiornithine birds (Zhou and Zhang, 2006a). Among the known enantiornithines, Yuanjiawaornis is most similar in size and in limb segment proportions to the known bohaiornithids Shenqiornis (Wang et al., 2010), Bohaiornis (Hu et al., 2011), Sulcavis (O'Connor et al., 2013), Zhouornis (Zhang et al., 2013), Parabohaiornis (Wang et al., 2014), and Longusunguis (Wang et al., 2014). Several unique morphological characters are combined to distinguish the bohaiornithids from other enantiornithines (Wang et al., 2014): robust rostrum with large and subconical teeth; pygostyle gently tapered distally; omal tips of furcula expanded laterally; short and robust tarsometatarsus; and long pedal unguals. Yuanjiawaornis has a similar pygostyle with the bohaiornithids, whereas the omal tips of its furcula taper in dorsal view as in other enantiornithines Eoenantiornis and Pengornis, rather than laterally expand as in the bohaiornithids. Yuanjiawaornis is also clearly different from the bohaiornithids in having the following character states: ventral surface of synsacrum longitudinally grooved (ridged in Bohaiornis and Parabohaiornis); transverse processes of the most caudal sacral vertebra relatively robust and long (transverse processes of penultimate sacral vertebra relatively robust and long in Zhouornis, Parabohaiornis, and Longusunguis); acromion process tapered craniodorsally (nearly parallels to the shaft of scapula in all bohaiornithids except for Longusunguis, which has a similar scapula with Yuanjiawaornis); lateral margin of coracoid straight (strongly convex in Shenqiornis, Sulcavis, and Longusunguis); clavicular ramus medially curved (straight in all bohaiornithids except for Longusunguis, in which both clavicular rami are not exposed); sternum shorter longitudinally than transversely, with slightly expanded distally caudolateral processes (distal end of caudolateral process strongly expanded into an asymmetrical triangle in Bohaiornis, Zhouornis, and Parabohaiornis); proximal surface of humeral head flat (concave in all bohaiornthids except for Zhouornis, which has a flat proximal surface of humeral head as in Yuanjiaornis); and deltopectoral crest gently recedes distally (abruptly ends distally in Shenqiornis, Sulcavis and Longusunguis). Yuanjiawaornis differs from Pengornis mostly in its limb proportions (Table 2). The femur of Yuanjiawaornis is slightly shorter than that of Pengornis, but the tibiotarsus and
tarsometatarsus are subequal in length between both. In Pengornis, the ulna, as well as the humerus, is much longer than the tibiotarsus, whereas the three elements are subequal in length in Yuanjiawaornis. Additionally, the fibula of Pengornis extends distally to meet the proximal tarsals as in Zhouornis (Zhang et al., 2013), whereas the bone is less than half the length of the tibiotarsus in Yuanjiawaornis. The observed differences in proportions are unable to be explained from individual variation and different ontogenetic stages within species, and they most likely represent interspecific variation. Therefore, this combination of the features (above), along with the holotype's large size, subequal forelimb and hind limb lengths, further distinguishes Yuanjiawaornis from all other enantiornithines. The discovery of Yuanjiawaornis, in combination with new data from other enantiornithines, sheds light on the sacral morphology of enantiornithines. The sacrum of most known basal birds, such as confuciusornithids and sapeornithids (Zhang et al., 2008; Provini et al., 2009), and ornithuromorphans such as Archaeorhynchus (Zhou and Zhang, 2006b), Gansus (You et al., 2006), Apsaravis (Clarke and Norell, 2002), and Ichthyornis (Clarke, 2004) all seem to share one morphological feature: the middle sacral vertebrae are considerably wider than the anterior and posterior ones, implying a strengthened sacrum. This feature is also seen in some deinonychosaurs, although to a less degree (Xu et al., 2000; Xu et al., 2002), suggesting that this is a primitive feature for Aves. Among known Early Cretaceous enantiornithines, the recently reported Rapaxavis (O'Connor et al., 2010), Bohaiornis (Hu et al., 2011), Parabohaiornis (Wang et al., 2014), and the referred specimen of Zhouornis BMNHC Ph 756 (Zhang et al., 2014) have a completely preserved and ventrally exposed sacrum, as in Yuanjiawaornis. These Early Cretaceous enantiornithines appear to have a reduced sacrum with the middle sacral vertebrae transversely thinner than the cranial and caudal articular ends of the synsacrum. In Rapaxavis, the cranial one-third of the sacral centra are distinctly thinner than the cranial articular surface. The caudal two-thirds appears to be strongly compressed dorsoventrally and seems to be slightly widened. Examination of the holotype, however, suggests this dorsoventral compression and the groove on the caudal two-thirds of the ventral surface may be a result of postmortem crushing. Among known Late Cretaceous enantiornithines, only Elbretornis has a nearly complete synsacrum, although the cranial centrum is partly damaged (Walker and Dyke, 2010). The middle centra of the synsacrum appear to be narrow and the cranial articular surface seems to be broader than the middle centra as in the Early Cretaceous enantiornithines. Zhyraornis kashkarovi (Nessov, 1984), Zh. logunovi (Nessov, 1992) and Lenesornis maltshevskyi (Nessov, 1986) are Late Cretaceous enantiornithines identified only on the basis of isolated and incompletely preserved synsacra (Kurochkin, 2000). Narrow middle centra and a broader cranial centrum are also present in the synsacrum of Lenesornis (Nessov, 1986). These features support the identification of Zhyraornis and Lenesornis as enantiornithines. However, further discoveries of new specimens are necessary to clarify whether or not the morphological structures seen in the synsacral centra of many enantiornithines is a diagnostic Table 2 Comparative measurements (mm) of selected enantiornithine birds. Taxon
hu
ul
cmc
fe
ti
tmt
fl/hl
Yuanjiawaornis viriosus 51(r) 53(r) 24*(r) 43(r) 50.5(l) 27(l) 1.06 (PMOL AB00032) Bohaiornis guoi 47(l) 48(l) 22.3(l) 39(r) 46(r) 22.5(r) 1.09 (PMOL AB00167) 64.3(l) 70.7(l) 34.3(r) 48(r) 50.4(r) 26.5(r) 1.36 Pengornis houi (IVPP V15336) See text for abbreviations. *, estimated length; l and r, left and right sides.
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for the clade or for a less inclusive group within that clade. The fact that the cranial and caudal articular surfaces of the synsacrum are wider than the other centra in the enantiornithines likely results from a combination of reduction of the main part of the sacrum and retention of a large surface for articulation with the dorsal and caudal vertebra. Enantiornithines have a relatively large bony tail that consists of expanded and elongated free caudal vertebrae and pygostyle. Therefore, a large caudal articular surface of the synsacrum is necessary to increase the functional load of the tail vertebrae and the feathers they bore (Zelenkov and Averianov, 2011). 4. Conclusion During the last two decades, over ten enantiornithine taxa have been reported from the Lower Cretaceous deposits of western Liaoning in northeastern China, and the description of Yuanjiawaornis viriosus increases the taxonomic and morphological diversity known in the Lower Cretaceous Jiufotang Formation of this area. This new species provides additional morphological information about enantiornithines, and further suggests that enantiornithines might have a uniquely shaped synsacrum among birds. Acknowledgments We thank the field crew of PMOL for collecting and preparing this specimen, Sullivan C., O'Connor J. K., Falk A. and Stidham T. for their helpful suggestions on earlier draft, E. Jagt-Yazykova for their careful edits, and the reviewers for their review and helpful comments. This research was supported by the National Natural Science Foundation of China (41172026, 41120124002), and Natural Science Foundation (201102199) and Education Bureau Foundation (LR2012038) of Liaoning Province. X. Xu's work was also supported by the Special Funds for the Major State Basic Research Projects of China. References Chiappe, L.M., 1993. Enantiornithine (Aves) tarsometatarsi from the Cretaceous Lecho Formation of northwestern Argentina. American Museum Novitates 3083, 1e27. Chiappe, L.M., 2002. Early bird phylogeny: problems and solutions. In: Chiappe, L.M., Witmer, L.M. (Eds.), Mesozoic Birds: Above the Heads of Dinosaurs. University of California Press, Berkeley, California, pp. 448e472. Chiappe, L.M., Calvo, J.O., 1994. Neuquenornis volans, a new Late Cretaceous bird (Enantiornithes: Avisauridae) from Patagonia, Argentina. Journal of Vertebrate Paleontology 14, 230e246. Chiappe, L.M., Walker, C.A., 2002. Skeletal morphology and systematics of the Cretaceous Euenantiornithes (Ornithothoraces: Enantiornithes). In: Chiappe, L.M., Witmer, L.M. (Eds.), Mesozoic Birds: Above the Heads of Dinosaurs. University of California Press, Berkeley, California, pp. 240e267. Clarke, J.A., 2004. Morphology, phylogenetic taxonomy, and systematics of Ichthyornis and Apatornis (Avialae: Ornithurae). Bulletin of the American Museum of Natural History 286, 1e179. Clarke, J.A., Norell, M.A., 2002. The morphology and phylogenetic position of Apsaravis ukhaana from the Late Cretaceous of Mongolia. American Museum Novitates 3387, 1e46. Duan, Y., Zhang, L., Li, L., Cheng, S., 2006. Division and correlation of unique fossil-bearing beds of Jiufotang Formation in Dapingfang-Meileyingzi Basin of western Liaoning. Global Geology 25, 113e119 [Chinese with English abstract]. Hou, L., 1994. A Late Mesozoic bird from Inner Mongolia. Vertebrata PalAsiatica 32, 258e266 [Chinese with English abstract]. Hou, L., Zhou, Z., Gu, Y., Zhang, H., 1995. Confuciusornis sanctus, a new Late Jurassic sauriurine bird from China. Chinese Science Bulletin 40, 1545e1551. Hu, D., Li, L., Hou, L., Xu, X., 2010. A new sapeornithid bird from China and its implication for early avian evolution. Acta Geologica Sinica 84, 472e482. Hu, D., Li, L., Hou, L., Xu, X., 2011. A new enantiornithine bird from the Lower Cretaceous of western Liaoning, China. Journal of Vertebrate Paleontology 31, 154e161.
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