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A Reappraisal of Boluochia Zhengi (Aves: Enantiornithes) and a Discussion of Intraclade Diversity in the Jehol Avifauna, China Jingmai K

A Reappraisal of Boluochia Zhengi (Aves: Enantiornithes) and a Discussion of Intraclade Diversity in the Jehol Avifauna, China Jingmai K

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Journal of Systematic Palaeontology Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/tjsp20 A reappraisal of Boluochia zhengi (Aves: ) and a discussion of intraclade diversity in the Jehol avifauna, China Jingmai K. O’Connor a , Zhonghe Zhou a & Fucheng Zhang a a Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Palaeontology and Palaeoanthropology, Beijing, China Available online: 16 Dec 2010

To cite this article: Jingmai K. O’Connor, Zhonghe Zhou & Fucheng Zhang (2011): A reappraisal of Boluochia zhengi (Aves: Enantiornithes) and a discussion of intraclade diversity in the Jehol avifauna, China, Journal of Systematic Palaeontology, 9:1, 51-63 To link to this article: http://dx.doi.org/10.1080/14772019.2010.512614

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A reappraisal of Boluochia zhengi (Aves: Enantiornithes) and a discussion of intraclade diversity in the Jehol avifauna, China Jingmai K. O’Connor∗, Zhonghe Zhou and Fucheng Zhang Key Laboratory of Evolutionary Systematics of Vertebrates, Institute of Vertebrate Palaeontology and Palaeoanthropology, Beijing, China (Received 14 April 2010; accepted 6 July 2010)

A careful reappraisal of the only known specimen of the poorly understood enantiornithine Boluochia zhengi reveals numerous morphological similarities that suggest this taxon is closely related to the well-known chaoyangensis, and so is assignable to the most diverse recognized clade of Early enantiornithines, the Longipterygidae. This new study of the holotype of B. zhengi reveals new longipterygid synapomorphies and expands our knowledge of the temporal and geographical ranges and diversity of the clade. We suggest that the trophic specialization that characterizes longipterygids may have been a major factor contributing to the success of this clade. Keywords: Enantiornithes; ; Longipterygidae; Boluochia; Longipteryx; Jehol

Introduction eries of new avian taxa have, however, benefited from the surge of palaeontological activity in the Jehol region; the Since the first discoveries of enantiornithine in the collecting process is much more methodical and meticu- Jehol Group of northeastern China in the early 1990s (Zhou lous. Because newly discovered tend to be more et al. 1992), a steady flow of new forms have been discov- complete and better prepared than earlier finds, they have ered (Sereno & Rao 1992; Zhang et al. 2003; Zhou & Zhang the potential to reveal more anatomical information (Zhou 2006). This wealth of fossils has revealed more information et al. 2008). Although the discovery of new forms is about enantiornithine skeletal and integumentary morphol- not unexpected, the paucity of new specimens that can ogy than those known from any other geological unit in the be referred to already known taxa is surprising; unlike world, and specimens that substantially change our under- more basal birds, such as sanctus and, to standing of this diverse clade continue to be discovered a lesser degree, chaoyangensis and (Zhou et al. 2008; Wang et al. 2010). The majority of prima, most Jehol ornithothoracine birds are not known these birds come from the younger two formations in the from multiple specimens (Zhou & Zhang 2003a, b; Chiappe Jehol Group, the Yixian and Jiufotang formations, which et al. 2008). This may reflect the fact that many of the preserve late Hauterivian—early lake deposits span- first ornithothoracine taxa discovered from this area were ning approximately 5 million years (125–120 million years initially based on very incomplete holotype specimens (i.e. ago) (He et al. 2004; Yang et al. 2007; Zhu et al. 2007). The Boluochia zhengi, longidigitrus, Chaoyan- third and oldest member, the Dabeigou Formation, dated at gia beishanensis) (Hou & Zhang 1993; Zhou 1995; Hou 131 million years ago (He et al. 2006), has also produced 1997). With a very limited understanding of Early Creta- a few birds such as the basal enantiornithine ceous enantiornithine morphology and diversity, much fengningensis (Zhang & Zhou 2000) and the basal confu- initial identification, although generally accurate at the ciusornithid zhengi (Zhang et al. 2008); time, must now be reinterpreted in the light of new knowl-

Downloaded by [Institute of Vertebrate Paleontology and Paleoanthropology] at 18:10 13 November 2011 hence the Jehol records approximately 11 million years of edge and additional comparative data. Here, using knowl- this avifauna (Zhou 2006; Zhang et al. edge of the currently known avifauna to reappraise B. 2008). zhengi, we reveal new information and elucidate the phylo- Not only have fossil birds been unearthed from these genetic relationships of this poorly known taxon. sediments, but also a rich biota of fossil plants, insects and Boluochia zhengi was one of the earliest enantiornithines other invertebrates, fish, amphibians, pterosaurs, mammals to be named from the Jehol Group (Zhou 1995). Because the and non-avian (Zhou et al. 2003). Recent discov- holotype and only known specimen is very incomplete, this

∗Corresponding author. Email: [email protected]

ISSN 1477-2019 print / 1478-0941 online Copyright C 2011 The Natural History Museum DOI: 10.1080/14772019.2010.512614 http://www.informaworld.com 52 J. K. O’Connor et al.

ping, which further obscures the morphology of this bird (Figs 2, 3). The original study of B. zhengi was further hindered by the limited information available regarding the anatomy of enantiornithines during the mid-1990s. Despite this, B. zhengi was the first enantiornithine from the Jehol Group to be recognized as such (Zhou 1995); the specimen was referred to this clade on the basis of a reduced metatarsal IV, a proximally located dorsal process of the ischium, a narrow intercondylar incisure of the tibiotarsus, and slender outer (lateral) sternal trabeculae (Zhou 1995). IVPP V9770 was further distinguished from other enantiornithine taxa known at the time on the basis of its hooked beak, the concave surface between the premaxillary corpus and the nasal processes (processus frontalis), a small lateral expan- sion of the outer trabeculae of the sternum, and because metatarsals II–IV are approximately equal in their distal Figure 1. Photograph of the holotype of Longipteryx chaoyan- extent (Zhou 1995). This original diagnosis was subse- gensis (IVPP V12325). Scale bar represents 1 cm. quently updated in light of more recent discoveries of other enantiornithines; the most current iteration (Zhou & Zhang 2006) differentiates B. zhengi from all other taxon has typically been excluded from phylogenetic analy- enantiornithines by the absence of premaxillary teeth, the ses and other forms of comparative research (Chiappe et al. presence of a rostrally hooked premaxilla, a narrow inter- 2006; O’Connor et al. 2009; Zhou et al. 2009). Attention on condylar incisure on the tibiotarsus, tibiotarsal condyles B. zhengi has been focused instead on its purported rostral that are approximately equal, a medial tibiotarsal condyle specializations (e.g. the presence of an edentulous, hooked with a flat cranial margin in distal view, metatarsals II–IV premaxilla). The holotype is a single slab on which most that are subequal in length and extend distally to approx- bones are preserved as impressions; a mould that replicates imately the same level, and a trochlea for metatarsal II the bones in positive relief was prepared for the purpose that is wider than those of metatarsals III and IV (Zhou & of this study. Our reassessment of this fragmentary speci- Zhang 2006). Because most of the skull in this specimen men now suggests that this taxon is in fact closely related is missing, whether or not B. zhengi possesses the rostral to the much more complete and well-known Longipteryx elongation that characterizes other known longipterygids chaoyangensis Zhang et al. 2000 (Fig. 1) and is a member cannot be determined. Furthermore, because of its poor of the most speciose clade of Early Cretaceous enantior- preservation, interpretations of some other areas of the nithines, the Longipterygidae (Zhang et al. 2000; O’Connor specimen are equivocal. Nevertheless, as discussed below, et al. 2009). Here we re-describe the holotype specimen B. zhengi is still considered a valid taxon, although of B. zhengi, emphasizing comparison with contemporary several of its ‘diagnostic’ features are reinterpreted longipterygids. here. In contrast to B. zhengi, L. chaoyangensis is known from several, nearly complete, single-slab specimens (including a subadult), all of which are preserved as recrystallized Institutional abbreviations bone that has been crushed (Zhang et al. 2000) (Fig. 1). The published specimens and referred materials all come DNHM: Dalian Natural History Museum, Dalian, China; from localities around Chaoyang, , approximately IVPP: Institute of Vertebrate Palaeontology and Palaeoan- 50 km from the Boluochi locality where B. zhengi was Downloaded by [Institute of Vertebrate Paleontology and Paleoanthropology] at 18:10 13 November 2011 thropology, Beijing, China. found (Zhang et al. 2000; Zhou & Hou, 2002; Gao, C-H. personal communication 2010). At the time of its descrip- Background information tion, the rostrum of L. chaoyangensis was considered elon- Boluochia zhengi is currently known from a single, gate relative to other known enantiornithines, and unique in incomplete specimen (IVPP V9770) collected at the that it possesses large, recurved teeth only in its premaxilla Xidagou locality of the near Boluochi, and rostral portion of the dentary. This rostral elongation Chaoyang, in Liaoning Province. IVPP V9770 preserves the and unique dental pattern suggests that L. chaoyangensis voids of parts of the skull and sternum bones, the caudal half was specialized for a piscivorous feeding niche (Zhang of the axial skeleton, and the pelvic girdle and hindlimbs. et al. 2000); this taxon was the first recognized enan- The voids of the bones in IVPP V9770 are largely overlap- tiornithine to possess a major morphological innovation Reappraisal of Boluochia zhengi and discussion of Jehol avifauna 53

Figure 2. Photographs of the holotype of Boluochia zhengi (IVPP V9770). A, slab; B, mould. Scale bar represents 1 cm.

associated with a particular trophic specialization, with its O’Connor et al., 2009 and pani Morschhauser rostral elongation paralleling adaptations seen within crown et al., 2009, although morphology aligns these new taxa group Aves. more closely with Longirostravis hani than L. chaoyan- Following this discovery, another enantiornithine from gensis. Currently, primitive longipterygids (forms compa- the Jehol Group was reported with a similar elongated rable to L. chaoyangensis) are unknown from the Yixian rostrum and rostrally restricted dentition, but this time Formation. from the stratigraphically lower Yixian Formation (Hou Longipterygidae is not only supported by observed et al. 2004). The similarity in rostral morphology suggested morphological similarities among taxa, but also receives that the new taxon, Longirostravis hani Hou et al., 2004, unambiguous support in phylogenetic studies (Chiappe may be related to the previously discovered L. chaoyangen- et al. 2006; O’Connor et al. 2009). The clade has been sis (Chiappe et al., 2006); however, major morphological resolved in several cladistic analyses, including one that differences in the sternum and manus suggest that Longiros- incorporated all four longipterygids recognized at the time Downloaded by [Institute of Vertebrate Paleontology and Paleoanthropology] at 18:10 13 November 2011 travis hani is more derived despite its older geological age (O’Connor et al. 2009). As a result, Longipterygidae is (Chiappe et al. 2006; O’Connor et al. 2009). Nevertheless, the most diverse subclade currently recognized within these taxa were resolved together in a clade of rostrally the Jehol avifauna and one of the only enantiornithine specialized enantiornithines, Longipterygidae (Zhang et al. clades that consistently receives phylogenetic support. The 2000; Chiappe et al. 2006; O’Connor et al. 2009). The pres- fact that this clade is so diverse may reflect the ease with ence of the more derived longipterygid in the older forma- which synapomorphies (i.e. elongate rostra and rostrally tion of the Jehol suggested that this clade has further diver- restricted teeth) can be recognized; it may also suggest sity yet to be found. This hypothesis was confirmed with that the elongation of the rostrum in this lineage facilitated the subsequent discoveries of Shanweiniao cooperorum greater diversification. 54 J. K. O’Connor et al.

Figure 3. Interpretative drawing of the holotype specimen of Boluochia zhengi (IVPP V9770). Scale bar represents 1 cm. Anatomical abbreviations: c2?, possible claw of second digit; den?, possible dentary fragment; fe, femur; il, ilium; isc, ischium; mt1, metatarsal I; Downloaded by [Institute of Vertebrate Paleontology and Paleoanthropology] at 18:10 13 November 2011 mt4, metatarsal IV; ot, outer trabeculae; pmx, premaxilla; pub, pubis; pyg, pygostyle; stn, sternum; tbt, tibiotarsus; th, tooth; tmt, tarsometatarsus; xp, xiphoid process.

Morphological reassessment and limitations, the morphology that can be observed suggests a comparison close relationship between this taxon and L. chaoyangensis. From the preserved material, the two taxa cannot be differ- The holotype of B. zhengi was studied from the original entiated except in size, with B. zhengi being smaller, falling slab as well as from a mould (Fig. 2). Despite preservational outside the known size range of L. chaoyangensis (Table 1), Reappraisal of Boluochia zhengi and discussion of Jehol avifauna 55

Table 1. Selected measurements of known longipterygids. An asterisk denotes estimated measurements; parentheses indicate incomplete elements. All measurements are taken from the holotype specimens, with the exception of the subadult Longipteryx chaoyangensis, IVPP V12552.

Longipteryx Boluochia Longipteryx chaoyangensis Shanweiniao Rapaxavis Longirostravis zhengi chaoyangensis subadult cooperorum pani hani

Sternum, L (18.9) (19) 25.7(11.7) 16.216.3 Ilium, 7.5∗ 10.58∗ —4.8∗ 6.1∗ post-acetabulum Ischium 17 19.717.7 — 14 10∗ Pubis 25.15 28.222.418.2∗ 19.319.8 Pygostyle 21.5 24∗ 24.512.414.513 Tibiotarsus (24.3) 30.129∗ 22.724.5∗ 25.1 Tarsometatarsus 17.4L − 17.7R 20 19.211.813.413.7

and a difference in the morphology of the tarsometatarsus. terpreted as present but slightly exaggerated. The rostral- As a result of this difference in size, extensive comparisons most tip of the premaxilla in B. zhengi appears slightly are made here with a juvenile specimen of L. chaoyangensis sharper than that of L. chaoyangensis, which we consider and the several smaller known longipterygids (Longiros- an artefact of poor preservation; the distinct hook previously travis hani, R. pani and S. cooperorum). considered characteristic of this taxon, and unique among known enantiornithines, is absent in this taxon (contra Zhou Skull 1995). The skull of the holotype of B. zhengi is largely incom- As described by Zhou (1995), the maxillary process plete, preserving only part of the premaxilla and fragments of the premaxilla in B. zhengi is long and tapers sharply of the nasal and dentary (Figs 4A, B). The only element whereas the nasal process is robust and rod-like; both of that can be clearly identified is the premaxilla. Preserva- these features are also present in L. chaoyangensis (Zhang tion in this region is extremely poor, which resulted in et al. 2000) (Fig. 4). These morphologies are also shared the identification of a hooked bill and other morpholo- by other longipterygids, although the morphology of the gies not actually present. The premaxilla is missing the premaxillary processes are less clear in S. cooperorum and caudal half of the nasal process and the maxillary process Longirostravis hani (Hou et al. 2004; O’Connor et al. 2009). is damaged (Figs 4A, B). As in L. chaoyangensis (Figs In contrast with earlier claims that B. zhengi may have an 4C, D) and other longipterygids, the dorsal and ventral edentulous premaxilla, we interpret the recurved and taper- margins of the premaxillary corpus are nearly parallel, ing structures protruding from the ventral margin of the forming a long imperforate region before diverging into premaxilla as teeth. Only one tooth clearly preserves its nasal and maxillary processes (Fig. 4). In enantiornithines morphology but we estimate that four teeth were present that do not possess an elongated rostrum, the premaxil- (Figs 4A, B). The large size and curvature of the teeth lary corpus is short, and the dorsal and ventral margins in B. zhengi are consistent with those of L. chaoyangensis, are not parallel (e.g. yandica, whereas the teeth in S. cooperorum and Longirostravis hani buhleri, houi) (O’Connor & Chiappe forthcom- are proportionally much smaller and more ‘peg-like’ (Hou ing). This strongly suggests that the rostrum was elongate et al. 2004; O’Connor et al. 2009). In B. zhengi, the teeth in B. zhengi. appear to be more caudally inclined than in L. chaoyan- In B. zhengi, the region immediately rostral to the nasal gensis, however, given the nature of the preservation of process was described as slightly concave dorsally (Zhou IVPP V9770, we cannot tell if this is an actual morphology 1995) (Figs 4A, qB). Although this cannot be determined or an artefact of preservation (Fig. 4). Just ventral to the Downloaded by [Institute of Vertebrate Paleontology and Paleoanthropology] at 18:10 13 November 2011 in the holotypes of L. chaoyangensis (IVPP V12325) or S. distal end of the preserved nasal process of the premax- cooperorum because of the preservation, a juvenile referred illa, two small bone fragments are present, interpreted as specimen of L. chaoyangensis (IVPP V12552) with a well- the sharply tapering rostral ends of the nasal premaxillary preserved rostrum has the same slight concavity (Fig. 4C). processes (Figs 4A, B). Other known longipterygids possess On closer inspection this morphology is also present in schizorhinal nostrils in which the nasals lack a descend- Longirostravis hani and R. pani, although less defined in ing maxillary process (O’Connor & Chiappe forthcoming) the delicate rostrum of the former and exaggerated by crush- (Figs 4C, D); this morphology cannot be confirmed in B. ing in the latter (Hou et al. 2004; Morschhauser et al. zhengi but may also have been present. Ventral to the prox- 2009). In B. zhengi, the margins of the premaxilla appear imal end of the preserved premaxilla, a fairly large, straight abraded in this region; this morphology is therefore rein- bone fragment is preserved, interpreted as the rostral end 56 J. K. O’Connor et al.

Figure 4. Camera lucida drawings of skulls. A, B, Boluochia zhengi, IVPP V9770; A, from slab; B, from cast. C, Longipteryx chaoyan- gensis, IVPP V12552; D, Longipteryx chaoyangensis, IVPP V12325 (holotype). Scale bars all 1 cm; same scale for A and B. Anatomical abbreviations: den?, possible dentary fragment; nas?, possible nasal fragments; pmx, premaxilla; th, tooth; th?, possible tooth.

of the dentary (Figs 4A, B). A single dentary tooth was and a distal constriction are clearly present (Chiappe & reported to be present, but this cannot be confirmed (contra Walker 2002). What is distinct about the pygostyles in Zhou 1995); the rostral-most end of the dentary preserves a both B. zhengi and L. chaoyangensis (Figs 1, 3), rela- dorsal projection that may represent a single tooth but this tive to other enantiornithines, is their unusual size and region is poorly preserved and difficult to interpret (Figs robustness. The pygostyle is shorter than the tarsometatar- 4A, B). sus in Longirostravis hani, approximately equal in length in S. cooperorum and 10% longer in R. pani (we use Axial skeleton the tarsometatarsus for comparison because of preserva- The vertebral column of B. zhengi is nearly entirely tional limitations in the Boluochia holotype, acknowledg- Downloaded by [Institute of Vertebrate Paleontology and Paleoanthropology] at 18:10 13 November 2011 preserved, starting with the synsacrum, although over- ing that the proportions of the tarsometatarsus vary slightly lap and poor preservation of bones provides virtually between taxa; see Table 1 for comparative measurements no anatomical information (Figs 2, 3). The pygostyle is of longipterygids). In B. zhengi and L. chaoyangensis,in the only vertebral element for which information can be contrast, the pygostyle is 20% longer than the tarsometatar- obtained (Fig. 3); although preservation is unclear, its shape sus and very robust when compared with other enantior- appears typical of other enantiornithines (e.g. C. yandica, nithines in which the pygostyle is typically shorter and Halimornis thompsoni, L. chaoyangensis, santen- narrower than the tarsometatarsus (e.g. Dapingfangornis sis) (Zhou et al. 1992; Chiappe et al. 2002; Sereno et al. sentisorhinus, Vescornis hebeiensis, E. buhleri,) (Chiappe 2002). The presence of a dorsal fork cannot be deter- & Walker 2002; Zhang et al. 2004; Zhou et al. 2005; Li mined, although ventrolaterally projecting lateral processes et al. 2006) (Figs 1, 3). Reappraisal of Boluochia zhengi and discussion of Jehol avifauna 57

Figure 5. Longipterygid sterna. A, reconstruction of the sternum of Longipteryx chaoyangensis based on IVPP V12325; B, preserved sternum of juvenile Longipteryx chaoyangensis, IVPP V12552; C, preserved sternum of Boluochia zhengi. Scale bar represents 1 cm.

Sternum distal ends of the ischia in B. zhengi approach and appear Only the distal half of the sternum is preserved in B. zhengi, to contact each other (Figs 2, 3), a morphology that cannot and what is present is extremely poorly preserved (Figs be confirmed in L. chaoyangensis (Fig. 1), but that is also 3, 5). The xiphoid process (xiphial region) and strap-like present in the longipterygid R. pani (O’Connor et al. in outer trabeculae are consistent with morphologies seen in press). In both B. zhengi and L. chaoyangensis, the pubis L. chaoyangensis in that the trabeculae are slightly splayed is gently curved caudodorsally so that its ventral margin is laterally and the caudal end of the xiphoid process is simple convex (Figs 1, 3). In B. zhengi and most other enantior- and blunt (Fig. 5A). Distal expansions of the outer trabec- nithines the entire pubic shaft is gently curved; the prox- ulae, present in L. chaoyangensis and other taxa (e.g. C. imal portion of the pubis in L. chaoyangensis,however, yandica, lacustris) (Sanz & Buscalioni 1992), is relatively straight (Fig. 1). The poor preservation of the are either not preserved in the holotype of B. zhengi or were pubis in IVPP V9770 prevents the use of this character to absent in this species (Fig. 5C). They are also not preserved further differentiate B. zhengi and L. chaoyangensis.The in the juvenile L. chaoyangensis (IVPP V12552; Fig. 5B), pubis of R. pani was described as kinked mid-shaft rather which suggests that this feature develops during the course than curved (Morschhauser et al. 2009); however, we rein- of ontogeny; this, however, remains purely speculative in terpret this morphology as being broadly concave dorsally the absence of a more complete growth series. Unlike the throughout (O’Connor et al. in press). The distal end of the morphology preserved in B. zhengi,inLongirostravis hani pubis in B. zhengi has a boot-like expansion that appears the medial margins of the outer trabeculae are strongly fairly large, tapered distally, and oriented nearly perpendic- concave and the xiphoid process is expanded slightly and ular to the long axis of the pubis, as is typical of other Early has a flat caudal margin. The outer trabeculae of R. pani and Cretaceous enantiornithines (Sereno & Rao 1992; Zhang S. cooperorum, although less clearly preserved in the latter, et al. 2000; Morschhauser et al. 2009). are oriented caudally as opposed to caudolaterally (as in B. zhengi and L. chaoyangensis) (Morschhauser et al. 2009; Hindlimbs O’Connor et al. in press). In the holotype of B. zhengi, both hindlimbs are preserved in their entirety; however, the only element preserved clearly Pelvis on both sides is the tarsometatarsus. The voids of the proxi- The pelvic girdle is preserved in near articulation at the mal bones of the legs are heavily damaged and obscured by Downloaded by [Institute of Vertebrate Paleontology and Paleoanthropology] at 18:10 13 November 2011 level of the acetabulum in the holotype specimens of both B. overlap with other elements (Fig. 2). The femora provide zhengi and L. chaoyangensis (Figs 2, 3). However, compar- no anatomical information and the deep longitudinal groove isons are limited by the large overlap between elements mentioned by Zhou (1995) is reinterpreted here as a preser- in the former. Only the postacetabular wing of the ilium vational artefact. The proximal end of neither tibiotarsus is clearly preserved in both specimens; this wing is trian- reveals any anatomical information; distally the tibiotarsi gular and tapers distally. Although proportions cannot be are also poorly preserved but no longer overlap with other compared between the two holotypes, in both B. zhengi elements (Fig. 3). The size and proportions of the distal and L. chaoyangensis the ischium is long and strap-like condyles have been described previously (Zhou 1995) but and has a proximally located dorsal process, as is typical the specimen is reinterpreted here as preserved in caudal of other enantiornithines (Chiappe & Walker 2002). The view so these morphologies are in fact equivocal (Figs 3, 6). 58 J. K. O’Connor et al.

Figure 6. Photographs and interpretive drawings of left ankles and feet: A, B, Boluochia zhengi, IVPP V9770; C, D, Longipteryx chaoyangensis, IVPP V12325.

In caudal view, the medial condyle appears to be larger than The morphology of the tarsometatarsus in both B. zhengi the lateral condyle on the right tibiotarsus (Fig. 7) and sube- and L. chaoyangensis is unique compared with the typi- qual on the left (Fig. 6). The morphology is unclear in both cal enantiornithine condition, in which metatarsal III is the the slab and the mould because of the incomplete removal longest, followed by IV and II (e.g. , Concor- of bone from the voids, however, it appears that fusion was nis lacustris, Pengornis houi, Sinornis santensis) (Chiappe not complete in IVPP V9770. The proximal tarsals can be & Walker 2002; Zhou et al. 2008). In B. zhengi and L. distinguished from the tibia on the right tibiotarsus in caudal chaoyangensis, in contrast, metatarsal IV slightly exceeds view, where the tarsals cap the tibia forming the caudodistal and distal margins of the tibiotarsus (Fig. 7). Both tarsometatarsi are completely preserved in IVPP V9770 (Figs 2, 3, 6); although it appears that there was some degree of proximal fusion between the distal tarsals and metatarsals, preservation makes interpretation difficult. The distal tarsals form a single element that caps the prox- imal ends of the metatarsals; the metatarsals are poorly co-ossified if at all, and can still be distinguished (Figs 6, 7). A similar morphology is preserved in R. pani, in which

Downloaded by [Institute of Vertebrate Paleontology and Paleoanthropology] at 18:10 13 November 2011 the distal tarsals appear fully fused into a single cap, but fusion is absent between the tarsal cap and the metatarsals and between the metatarsals themselves (O’Connor et al. in press). As such, these two specimens provide direct evidence for the presence of a tarsal cap in Enantiornithes (contra Martin 1987). The apparently incomplete fusion of the tibiotarsus and tarsometatarsus may suggest that IVPP Figure 7. Interpretive drawing of the right ankle of Boluochia V9770 is not fully mature, although with no significant zhengi (IVPP V9770), illustrating the incomplete fusion of the tarsals and the presence of a tarsal cap. A, from slab; B, from bone fragments preserved a histological analysis can never mould. Anatomical abbreviations: dt, distal tarsals; pt, proximal be conducted to confirm this hypothesis. tarsals. Reappraisal of Boluochia zhengi and discussion of Jehol avifauna 59

III in length, followed by metatarsal II, which is the short- identical morphologies. The first metatarsal is preserved est (Fig. 6). This configuration is currently known among disarticulated on the right foot of B. zhengi (Fig. 3) and in Early Cretaceous birds only in these two taxa. Longiros- articulation with the medial surface of the left metatarsal travis hani, R. pani and S. cooperorum possess similar II in L. chaoyangensis (Fig. 1). The bone is straight proxi- morphologies but are more comparable to other enantior- mally, distally expanding caudomedially so that it is shaped nithines; in these specimens, metatarsal III is longer than like an inverted P. In other longipterygids this element is IV, which exceeds II in distal projection. In all longiptery- poorly preserved, with the exception of the holotype of R. gids, the trochlea of metatarsals II and IV extends beyond pani in which it appears to be straight (contra Morschhauser the proximal surface of the metatarsal III trochlea such et al. 2009). that they articulate at nearly the same level, as opposed to The preserved unguals in IVPP V9770 are fairly large taxa in which metatarsals II and IV end at the proximal and heterogeneous. One claw is clearly more robust than end of the metatarsal III trochlea, so that there is a signif- the others, although disarticulation of the toes makes it icant difference in length between metatarsals II and IV, difficult to determine which digit it belongs to (Fig. 3). and III (e.g. Avisaurus, P. houi, Soroavisaurus australis) Only the hallux claw is preserved in the holotype of L. (Chiappe & Walker 2002; Zhou et al. 2008). In modern chaoyangensis, but the feet are completely preserved in birds, in which the metatarsals distally terminate at the same the juvenile specimen IVPP V12252. In this specimen it is level, this configuration is usually indicative of a perch- clear that the same ungual heterogeneity also characterizes ing ecology (Zhang 2006). Together with the specialized L. chaoyangensis, and that the robust claw belongs to the rostral morphology of these specimens, this suggests that second digit. B. zhengi and L. chaoyangensis may have been piscivores well-suited for arboreal lifestyles, similar to modern king- fishers. Although specialized arboreal pedal proportions have been observed in some other Early Cretaceous enan- Discussion tiornithines (Hopson 2001), the pedal proportions of the longipterygid R. pani are farther along this spectrum than Boluochia zhengi shares a number of morphologies with L. other known enantiornithines because of the proportion- chaoyangensis—premaxilla with elongate and imperforate ally longer distal phalanges (Morschhauser et al. 2009). rostral portion, large recurved teeth, robust nasal processes, However, the presence of specialized pedal proportions large and robust pygostyle, laterally splayed outer trabecula cannot be inferred directly from the holotypes of either of the sternum, metatarsal I ‘p’-shaped, and metatarsals B. zhengi or L. chaoyangensis because of disarticulation II–IV subequal in length—that suggest the two taxa are and lack of preservation (Figs 1, 2). closely related. Despite these features, the holotype of B. Boluochia zhengi differs from L. chaoyangensis and zhengi can be differentiated from L. chaoyangensis by the all other known enantiornithines in that the distal end of lateral deflection of the distal end of metatarsal IV (Fig. 6). metatarsal IV is deflected laterally such that metatarsals For this reason, we consider B. zhengi to be a distinct taxon III and IV are separated for the distal one-fifth of their but because it shares several of the synapomorphies that lengths (Fig. 6). This is not considered a diagenetic arte- unite longipterygids, we feel justified in assigning B. zhengi fact because of the similar appearance of both the right to this diverse clade. The following new synapomorphies of and left tarsometatarsi in the holotype. In L. chaoyangen- Longipterygidae are recognized: premaxilla with elongate sis the metatarsals, though unfused, contact each other imperforate rostral end; dorsal surface of premaxilla with along their entire lengths, even in the juvenile speci- a slight concavity rostral to the nasal processes; pygostyle men (IVPP V12252), which suggests that this is not an subequal to, or larger than, the tarsometatarsus; trochleae ontogenetic feature in the B. zhengi holotype. Further- for metatarsals II and IV extending beyond the proximal more, the tarsometatarsus is an element that ossifies early surface of the trochlea for metatarsal III. during the ontogeny of precocial birds including enan- Because B. zhengi was published 5 years before tiornithines (Starck & Ricklefs 1998; Starck & Chinsamy L. chaoyangensis, the ‘first discovered longiptery- Downloaded by [Institute of Vertebrate Paleontology and Paleoanthropology] at 18:10 13 November 2011 2002). Although its precise ontogenetic stage is unknown, gid’ paradoxically does not preserve the characteristic given that IVPP V9770 is not a hatchling, we consider ‘longirostrine’ skull morphology. Although the premaxil- the morphology of the tarsometatarsus unlikely to change lary morphology preserved in B. zhengi does leave clues as further with age. to the presence of an elongate rostrum, this could not have The first metatarsal is known to show considerable vari- been determined until the subsequent discovery of more ation within Enantiornithes, ranging from straight in some complete longipterygids, which rendered synapomorphies taxa (R. pani) (O’Connor et al. in press), to strongly J- of the clade apparent. In addition, although B. zhengi was shaped in others (avisaurids) (Chiappe & Walker 2002). named earlier, higher level taxonomic names (Boluochi- The first metatarsals are preserved in the holotype speci- formes, Boluochidae) were erected after Longipterygidae mens of both L. chaoyangensis and B. zhengi and display and Longipterygiformes so the latter names have priority 60 J. K. O’Connor et al.

over all other clade names that have been proposed (Zhou We do not present a phylogenetic analysis with which & Zhang 2006). to support our morphological observations because of the incompleteness of the B. zhengi holotype. Enan- Systematic palaeontology tiornithine inter-relationships are notoriously difficult to unravel (Chiappe et al. 2006; Chiappe & Walker 2002) Enantiornithes Walker, 1981 because of the incompleteness of many of the named Longipterygidae Zhang et al., 2000 taxa (nearly half of all taxa are known from a single bone or less) (O’Connor 2009), and the extreme morpho- Stratigraphical distribution. Yixian and Jiufotang logical similarity that characterizes the clade. A recent formations of the Jehol Group, Lower Cretaceous, 125–120 cladistic analysis sampled every known valid enantior- million years ago (Swisher et al. 2002; He et al. 2004; Zhu nithine, including B. zhengi and L. chaoyangensis,but et al. 2007). resulted in an almost complete lack of resolution, support- ing neither a longipterygid clade nor a relationship between Geographical distribution. Chaoyang, Lingyuan and B. zhengi and L. chaoyangensis (O’Connor 2009). Conser- Yixian, western Liaoning Province, northeastern China. vative phylogenetic analyses have typically not included B. zhengi because the only known specimen is so fragmentary. Revised diagnosis. Small to medium-sized enantior- Therefore, pending new, more complete discoveries of B. nithine birds with the rostral portion of the skull equal zhengi, the phylogenetic position of this taxon relative to L. to, or exceeding, 60% of the total skull length; premaxilla chaoyangensis is inferred based on preserved morphology with elongate imperforate rostral end with parallel dorsal alone. and ventral margins; dorsal surface of premaxilla with Currently there are a large number of names that refer slight concavity just rostral to the nasal processes; denti- to included species of ‘Longipterygidae’ at various taxo- tion restricted to the premaxilla and rostral-most portion of nomic levels (i.e. Boluochidae, Boluochiformes, Longiros- the dentary; coracoid with nearly straight lateral margin; travisidae, Longirostravisiformes). We have discussed why pygostyle approaches or exceeds tarsometatarsus in length; Longipterygidae and Longipterygiformes take priority; trochleae of metatarsals II and IV extend beyond proximal however, because we use Linnaean terminology we feel surface of metatarsal III trochlea (modified from O’Connor a discussion of the implications of their usage is also et al. 2009). necessary. Here we follow O’Connor et al. (2009) and Boluochia zhengi Zhou, 1995 use the name Longipterygidae to refer to the clade formed by the most common ancestor of Longirostravis hani and Revised diagnosis. A small enantiornithine bird charac- L. chaoyangensis and all its descendants. Although no terized by the unique combined presence of the following Linnaean taxonomic categorical level was explicitly applied morphologies: premaxilla rostral to external nares imper- to this term by O’Connor et al. (2009), the ending denotes forate with parallel dorsal and ventral margins; dorsal a familial relationship between included taxa. The amount surface of premaxilla with slight concavity just rostral to of morphological disparity encapsulated by extant families the nasal processes; premaxilla with large, recurved teeth; differs throughout Aves. Although we use this name, we large and robust pygostyle 20% longer than tarsometatar- recognize that the fairly large variation among longiptery- sus; metatarsals II–III subequal in length and ending distally gid taxa (e.g. hand reduced vs unreduced, major morpho- at approximately the same level; metatarsal IV longer than logical differences in the sternal trabeculae, caudal rectrices II and III and laterally deflected along the distal one-fifth of present or absent) could be argued as indicative of a family- the tarsometatarsus (modified from Zhou & Zhang, 2006). level or even order-level relationship. Although Longipterygidae is one of few enantiornithine Mesozoic avian clades resolved in multiple cladistic analyses (which only We have provided evidence that B. zhengi is closely related include the most complete taxa), support (although unam- to L. chaoyangensis, but maintain the taxa as distinct genera biguous) is often weak (limited to one or two characters) and Downloaded by [Institute of Vertebrate Paleontology and Paleoanthropology] at 18:10 13 November 2011 not only for taxonomic simplicity but because the two taxa published analyses differ in the taxa included and their rela- can be distinguished by osteological differences. Among tive placement (Chiappe et al. 2006; Cau & Arduini 2008; living birds, species within a genus are typically distin- O’Connor et al. 2009); new fossils continue to add to the guished by behaviour, DNA and other differences that do diversity and change the resultant phylogenetic hypotheses. not typically fossilize, and even in living taxa were not For example, a recent phylogenetic study suggested that apparent until the advent of more advanced observational smaller longipterygids, especially R. pani and Longiros- techniques (Amadon 1963; Isler et al. 1999; Zimmer & travis hani, form a more exclusive relationship (or clade) Whittaker 2000). Within avian fossil taxonomy, species- (O’Connor et al. 2009), a conclusion later not supported in a level distinctions will always have a degree of ambiguity larger, more inclusive analysis (O’Connor 2009). Given the (O’Connor & Dyke 2010). plasticity between the results of current cladistic analyses, Reappraisal of Boluochia zhengi and discussion of Jehol avifauna 61

we find it most parsimonious to await either the discov- flight have been recognized within Longipterygidae, includ- ery of more complete specimens of B. zhengi or a well- ing both skeletal and integumentary specializations. The supported phylogenetic hypothesis before outlining a more Jiufotang Formation longipterygid R. pani preserves the definite taxonomic hierarchy. We hope this helps to avoid most reduced manus known within Enantiornithes with a confusion and the further proliferation of superfluous taxo- manual formula of 1-2-2-x-x (Morschhauser et al. 2009). nomic names. Pending a normalization of Mesozoic avian This taxon also preserves a pair of bizarre bones (paracora- phylogeny, groups of related taxa should simply be referred coidal ossifications, O’Connor et al. in press) whose loca- to as clades. tion, dorsal to the coracoid–sternum articulation, suggests that they may be related to flight. These features are also Early Cretaceous subclade diversity known in Concornis lacustris (Sanz & Buscalioni 1992), With the addition of B. zhengi, the diversity of Longiptery- although the absence of preserved skull material in this gidae is increased to five taxa, and is the most diverse known Spanish enantiornithine prevents the identification of the clade within Enantiornithes (although there are numerous most obvious characters that could potentially align this species assigned to Cathayornis, the taxonomy is unsup- taxon with other longipterygids. Although it is not known ported; for further discussion on this issue see O’Connor & how these ossifications affected flight, the reduction of the Dyke 2010). There is markedly greater diversity than that manus certainly increased aerodynamic capabilities in R. observed in sympatric subclades of ornithothoracine Jehol pani by streamlining the wing and decreasing weight. birds, supporting inferences that enantiornithines were the Another longipterygid, S. cooperorum, preserves the only dominant avian clade during the Cretaceous (Chiappe & evidence of an aerodynamic feathered tail within Enantior- Walker 2002; Chiappe 2007). Within the enantiornithine nithes (O’Connor et al. 2009). The morphology of this sister clade, Ornithuromorpha, the largest subclade includes taxon represents a distinct departure from the typical enan- three taxa: linghensis, martini and tiornithine that either does not have elongate rectrices (Zhou grabaui (Clarke et al. 2006). The greater diver- et al. 2005) or possesses no more than two or four very sity of the enantiornithine subclade may simply reflect the elongate display feathers (Zhang & Zhou 2000; Zheng ecological dominance of the enantiornithines at that time; et al. 2007). The holotype of S. cooperorum preserves alternatively the diversity of this subclade may be high more than four rectrices of unknown length (distal ends not for two reasons. The first and simplest reason is that the preserved) overlapping to form a single surface, a morphol- synapomorphies of this clade are easily identifiable and ogy that would have represented a considerable aerody- a large-scale detailed inspection of all known specimens namic advantage over other known enantiornithine feath- is not needed to identify clade synapomorphies (with the ered tails (O’Connor et al. 2009). The phylogenetic position exception of some fragmentary specimens, as demonstrated of S. cooperorum suggests that this morphology is derived here). The higher diversity may also be reflected in the within the lineage that includes this taxon but excludes more nature of the diagnostic features of the clade: the elongate primitive longipterygids (O’Connor et al. 2009). Where rostra and unique dental patterns represent trophic special- feathers are preserved, a fan-shaped tail appears absent in izations that depart from the morphologies of other known all known specimens of L. chaoyangensis; the holotype enantiornithines (O’Connor & Chiappe forthcoming). This (IVPP V12325) preserves a halo of short feathers with- suggests that members of the clade were able to retrieve food out any elongate tail rectrices around the pygostyle. The items from sources unavailable to other enantiornithines. absence of elongate tail feathers in the basal longipterygid The diversity of the clade was probably further facili- L. chaoyangensis is considered a true feature rather than an tated by niche partitioning among closely related species artefact of preservation, given that several specimens are within the group; longipterygid taxa preserve a wide range known. Tail morphologies are unknown for Longirostravis of dental and pedal morphologies that suggest different hani, R. pani and B. zhengi. The evolution of advanced aero- primary food items and habitats, respectively (O’Connor dynamic features would surely have facilitated the survival & Chiappe forthcoming). Longipterygidae also occupies a of this clade of small birds, especially in a wooded habitat, fairly large range of body sizes (Table 1), another form of as inferred for the Jehol (Zhou 2006). Downloaded by [Institute of Vertebrate Paleontology and Paleoanthropology] at 18:10 13 November 2011 resource partitioning. By using otherwise unused resources, longipterygid enantiornithines may have facilitated the speciation of their clade. Acknowledgements Longipterygids are known from the Yixian Formation through the Jiufotang Formation, which spans approxi- We thank Xinzhen Liu for preparing casts of the holotype of mately 5 million years (O’Connor et al. 2009). The success Boluochia zhengi for study and Wei Gao for photographing and diversity of this clade suggests that trophic special- the specimen. Thanks go to Gareth Dyke for comments ization was a major factor in the success of early birds, during the manuscript stage, and Jerry Harris and one and perhaps, in this clade, second to flight ability, given other reviewer for comments on an earlier version of this that numerous adaptations related to the refinement of manuscript. This project has been supported by the National 62 J. K. O’Connor et al.

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