The fossil record and limb disparity of enantiornithines, the dominant flying birds of the Cretaceous

Morphometric and stratigraphic analyses that encompass the known fossil record of enantiornithine birds (Enantiornithes) are presented. These predominantly flighted taxa were the dominant birds of the second half of the Mesozoic; the enantiornithine lineage is known to have lasted for at least 60 million years (Ma), up until the end of the Cretaceous. Analyses of fossil record dynamics show that enantiornithine 'collectorship' since the 1980s approaches an exponential distribution, indicating that an asymptote in proportion of specimens has yet to be achieved. Data demonstrate that the fossil record of enantiornithines is complete enough for the extraction of biological patterns. Comparison of the available fossil specimens with a large data set of modern bird (Neornithes) limb proportions also illustrates that the known forelimb proportions of enantiornithines fall within the range of extant taxa; thus these birds likely encompassed the range of flight styles of extant birds. In contrast, most enantiornithines had hindlimb proportions that differ from any extant taxa. To explore this, ternary diagrams are used to graph enantiornithine limb variation and to identify some morphological oddities ( Otogornis , Gobipteryx ); taxa not directly comparable to modern birds. These exceptions are interesting – although anatomically uniform, and similar to extant avians in their wing proportions, some fossil enantiornithines likely had flight styles not seen among their living counterparts.     

对长趾辽宁鸟的重新认识(英文)

早期发现于中国东北热河群的今鸟类化石多呈高度零散保存,本文对于惟一已知的长趾辽宁鸟( Liaoningornis longidigitrus) 标本的研究表明,该分类单元实际上是反鸟类的成员。虽然材料保存较差且破碎,但缺失发达的胸骨、胫骨脊和退化的脚爪,显示其应该被排除于更为进步的鸟胸类( ornithothoracines) 之外。辽宁鸟与所有已知的反鸟均有显著不同,但显示了与西班牙发现的 Eoalulavis hoyasi 的相似性: 它们相似的胸骨特征表明二者可能存在较密切的关系,尽管与其他反鸟类的不同表明,这可能是个体发育造成的假相。由于辽宁鸟标本过于零碎,因此目前难以确定其在反鸟类系统发育中的位置。     

对长趾辽宁鸟的重新认识(英文)

早期发现于中国东北热河群的今鸟类化石多呈高度零散保存,本文对于惟一已知的长趾辽宁鸟( Liaoningornis longidigitrus) 标本的研究表明,该分类单元实际上是反鸟类的成员。虽然材料保存较差且破碎,但缺失发达的胸骨、胫骨脊和退化的脚爪,显示其应该被排除于更为进步的鸟胸类( ornithothoracines) 之外。辽宁鸟与所有已知的反鸟均有显著不同,但显示了与西班牙发现的 Eoalulavis hoyasi 的相似性: 它们相似的胸骨特征表明二者可能存在较密切的关系,尽管与其他反鸟类的不同表明,这可能是个体发育造成的假相。由于辽宁鸟标本过于零碎,因此目前难以确定其在反鸟类系统发育中的位置。     

The patterns and modes of the evolution of disparity in Mesozoic birds

The origin of birds from non-avian theropod dinosaurs is one of the greatest transitions in evolution. Shortly after diverging from other theropods in the Late Jurassic, Mesozoic birds diversified into two major clades—the Enantiornithes and Ornithuromorpha—acquiring many features previously considered unique to the crown group along the way. Here, we present a comparative phylogenetic study of the patterns and modes of Mesozoic bird skeletal morphology and limb proportions. Our results show that the major Mesozoic avian groups are distinctive in discrete character space, but constrained in a morphospace defined by limb proportions. The Enantiornithines, despite being the most speciose group of Mesozoic birds, are much less morphologically disparate than their sister clade, the Ornithuromorpha—the clade that gave rise to living birds, showing disparity and diversity were decoupled in avian history. This relatively low disparity suggests that diversification of enantiornithines was characterized in exhausting fine morphologies, whereas ornithuromorphs continuously explored a broader array of morphologies and ecological opportunities. We suggest this clade-specific evolutionary versatility contributed to their sole survival of the end-Cretaceous mass extinction.     

A New Species of Pengornithidae (Aves: Enantiornithes) from the Lower Cretaceous of China Suggests a Specialized Scansorial Habitat Previously Unknown in Early Birds

We describe a new enantiornithine bird, Parapengornis eurycaudatus gen. et sp. nov. from the Lower Cretaceous Jiufotang Formation of Liaoning, China. Although morphologically similar to previously described pengornithids Pengornis houi, Pengornis IVPP V18632, and Eopengornis martini, morphological differences indicate it represents a new taxon of the Pengornithidae. Based on new information from this specimen we reassign IVPP V18632 to Parapengornis sp. The well preserved pygostyle of the new specimen elucidates the morphology of this element for the clade, which is unique in pengornithids among Mesozoic birds. Similarities with modern scansores such as woodpeckers may indicate a specialized vertical climbing and clinging behavior that has not previously been inferred for early birds. The new specimen preserves a pair of fully pennaceous rachis-dominated feathers like those in the holotype of Eopengornis martini; together with the unique morphology of the pygostyle, this discovery lends evidence to early hypotheses that rachis-dominated feathers may have had a functional significance. This discovery adds to the diversity of ecological niches occupied by enantiornithines and if correct reveals are remarkable amount of locomotive differentiation among Enantiornithes.     

An embryonic enantiornithine bird and associated eggs from the cretaceous of Mongolia

Enantiornithes is the most speciose clade of Cretaceous birds, but many taxa are known from isolated postcranial skeletons. Two embryonic enantiornithine bird skeletons of Gobipipus reshetovi gen. et sp. nov. from the Upper Cretaceous (Campanian) Barun Goyot Formation of the Gobi Desert in Mongolia provide new insights into the anatomy, radiation, and mode of development of early avialans. In recent times, both enantiornithine and ornithuromorph birds are known from the Barun Goyot Formation as well as from the Djadokhta and Nemegt Formations. The 80-million-year-old Gobipipus skeletons encased within eggshells shows several features characteristic of enantiornithine birds. The wing skeleton and shoulder girdle show morphological features indicating that Gobipipus achieved sophisticated powered flight. Gobipipus reshetovi gen. et sp. nov. is quite distinct from the sympatric enantiornithine species Gobipteryx minuta from the same strata in many anatomical features. Phylogenetic analysis of 26 avialan ingroup taxa based on distribution of 202 characters indicate that Gobipipus is a basal member of enantiornithine birds along with Confuciusornis and shares more characters with ornithuromorphs than previously recognized. The embryonic nature of Gobipipus specimens sheds new light on the developmental history of enantiornithine birds. The well-ossified bones of the fore- and hind limbs, and fusion of many skeletal elements indicate a precocial mode of development in Gobipipus. Apparently Gobipipus hatchlings could walk away from the ground nests as soon as they emerged from their eggs. The asymmetry of egg poles are unique features of Gobipipus eggs (oogenus Gobioolithus) among Cretaceous avialans. The microstructure of the shell in Gobioolithus eggs with the embryos of Gobipipus is typical avian (of ornithoid basic type) and less ratite-like in morphology of the spongy layer than is that in the other possible egg-remains of enantiornitine birds (oofamily Laevisoolithidae).     

A new fossil bird from the Early Cretaceous of Gansu Province,northwestern China

We report on the discovery of an Early Cretaceous bird from northwestern Gansu Province, in northwestern China. Represented by a nearly complete left wing and shoulder girdle the size of a rock dove, the new bird was quarried from laminated yellowish mudstones of the Xiagou Formation (Xinminpu Group) near Changma, in the Jiuquan area. These deposits have previously yielded the only known specimen of Gansus yumenensis, a basal ornithuromorph represented by the distal half of a hind limb with long and slender digits. Several derived characters of the new occurrence supports its allocation within Enantiornithes: (1) a convex lateral margin of the coracoid, (2) a minor metacarpal that projects distally more than the major metacarpal and (3) a proximal phalanx of the major digit longer than the intermediate (second) phalanx. The general proportions of the wing suggest it was a flier comparable to most other known enantiornithine birds. Although, direct comparisons between the new fossil and Gansus are not possible, phylogenetic based inferences supports their placement into two different clades. While the new fossil falls definitively within the enantiornithines, G. Yumenensis falls within the ornithuromorphs. The new occurrence thus adds to the taxonomic diversity of Early Cretaceous birds from Gansu Province in particular and central Asia in general.     

A new enantiornithine bird from Upper Cretaceous non-marine deposits at Villespassans (Hérault,southern France)

A coracoid of an enantiornithine bird from Upper Cretaceous (probably late Campanian) fluvial sediments at Castigno (Villespassans, Hérault, southern France) is described. It differs from all hitherto reported enantiornithine coracoids and is referred a new genus and species, Castignovolucris sebei. This bone is large and robust, indicating a bird that was among the largest known enantiornithines, possibly the size of a Canada Goose (Branta canadensis). The new taxon is an addition to the short list of Late Cretaceous birds from France and confirms that enantiornithines were an important component of European avifaunas until late in the Cretaceous.     

A new basal ornithuromorph bird (Aves: Ornithothoraces) from the Early Cretaceous of China with implication for morphology of early Ornithuromorpha

Ornithuromorpha is the most derived avian group in the Early Cretaceous, advanced members of which encompass all living birds (Neornithes). Here we report on a new basal ornithuromorph bird, Bellulia rectusunguis gen. et sp. nov., represented by a nearly complete skeleton from the Early Cretaceous Jehol Biota in northeastern China. A comprehensive phylogenetic analysis resolved the new taxon in a basal position that is only more derived than Archaeorhynchus and Jianchangornis among ornithuromorphs, increasing the morphological diversity of basal ornithuromorphs. The new specimen has a V‐shaped furcula with a short hypocleidium, a feature otherwise known only in Schizooura among Cretaceous ornithuromorphs. We discuss the implications of the new taxon on the evolution of morphology of primitive ornithuromorphs, particularly of pectoral girdle, sternum and limb proportion pertaining to powered flight. The preserved gastroliths and pedal morphology indicate herbivory and lakeshore adaption for this new species. © 2015 The Linnean Society of London     

Previously Unrecognized Ornithuromorph Bird Diversity in the Early Cretaceous Changma Basin,Gansu Province,Northwestern China

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

A new piscivorous ornithuromorph from the Jehol Biota

We report on a new species of basal ornithuromorph bird, Piscivoravis liigen. et sp. nov., based on a well-preserved and nearly complete specimen from the Lower Cretaceous Jiufotang Formation in western Liaoning Province, northeastern China. The new specimen preserves several unique anatomical features previously unreported in Early Cretaceous ornithuromorphs, such as a robust furcula with strongly tapered omal tips, a broad sternum without craniocaudal elongation and large and strongly curved manual unguals. Phylogenetic analysis indicates that Piscivoravis is more derived than Archaeorynchus, but in a basal polytomy with Jianchangornis, Patagopteryx, and the clade including all more derived ornithuromorphs. The preserved wing and tail feathers provide new information on feather diversity and evolution in Early Cretaceous ornithuromorphs. The preservation of fish bones ventral to the dentary and in the stomach provides direct evidence that the new species was piscivorous – previously only reported in Yanornis, and as in some living birds, was capable of moving food bidirectionally through the alimentary canal.http://www.zoobank.org/urn:lsid:zoobank.org:pub:92F23126-9E89-4E51-9700-C6608E0D66EB     

Early Cretaceous Enantiornithine Birds (Aves,Ornithothoraces) and Establishment of the Ornithuromorpha Morphological Type

New data on the taxonomic and morphological diversity of Early Cretaceous Enantiornithes are reviewed. A new hypothesis concerning the phylogenetic position of Pengornithidae is proposed. These birds traditionally treated as primitive enantiornithines may in fact be more closely related to Ornithuromorpha. This phylogenetic placement implies that the fan-shaped tail and modern-type humeral joint was formed once in the early evolution of birds. Hence, the similarity between Pengornithidae and other enantiornithines may be plesiomorphic. The ecology of Early Cretaceous enantiornithines is discussed. The increased mobility of neck in Holbotia is possibly accounted for by the cranioinertial swallowing mechanism, as in modern ratites. The hypotheses of scansorial adaptations in Parapengornis and Fortunguavis are criticized. In addition, the phylogenetic position of Mystiornis is discussed.     

Reidentification of Avian Embryonic Remains from the Cretaceous of Mongolia

Embryonic remains within a small (4.75 by 2.23 cm) egg from the Late Cretaceous, Mongolia are here re-described. High-resolution X-ray computed tomography (HRCT) was used to digitally prepare and describe the enclosed embryonic bones. The egg, IGM (Mongolian Institute for Geology, Ulaanbaatar) 100/2010, with a three-part shell microstructure, was originally assigned to Neoceratopsia implying extensive homoplasy among eggshell characters across Dinosauria. Re-examination finds the forelimb significantly longer than the hindlimbs, proportions suggesting an avian identification. Additional, postcranial apomorphies (strut-like coracoid, cranially located humeral condyles, olecranon fossa, slender radius relative to the ulna, trochanteric crest on the femur, and ulna longer than the humerus) identify the embryo as avian. Presence of a dorsal coracoid fossa and a craniocaudally compressed distal humerus with a strongly angled distal margin support a diagnosis of IGM 100/2010 as an enantiornithine. Re-identification eliminates the implied homoplasy of this tri-laminate eggshell structure, and instead associates enantiornithine birds with eggshell microstructure composed of a mammillary, squamatic, and external zones. Posture of the embryo follows that of other theropods with fore- and hindlimbs folded parallel to the vertebral column and the elbow pointing caudally just dorsal to the knees. The size of the egg and embryo of IGM 100/2010 is similar to the two other Mongolian enantiornithine eggs. Well-ossified skeletons, as in this specimen, characterize all known enantiornithine embryos suggesting precocial hatchlings, comparing closely to late stage embryos of modern precocial birds that are both flight- and run-capable upon hatching. Extensive ossification in enantiornithine embryos may contribute to their relatively abundant representation in the fossil record. Neoceratopsian eggs remain unrecognized in the fossil record.     

A new,three‐dimensionally preserved enantiornithine bird (Aves: Ornithothoraces) from Gansu Province,north‐western China

In recent years, the Lower Cretaceous (Aptian) Xiagou Formation has yielded approximately 100 avian partial skeletons, many with soft‐tissue traces, from sites in the Changma Basin of Gansu Province, north‐western China. The most abundant taxon amongst these is the ornithuromorph Gansus yumenensis, but enantiornithines have also been identified in the sample. Here we describe two incomplete, semi‐articulated appendicular skeletons, the first consisting of a partial left pelvic girdle and complete pelvic limb, and the second comprised of a nearly complete right pelvic limb. Both specimens bear characteristics diagnostic of Enantiornithes, and are referred to a new taxon, Qiliania graffini gen. et sp. nov. The exceptional, three‐dimensional preservation of these specimens (compared to the crushed, nearly two‐dimensional condition of most other Early Cretaceous avian fossils) reveals new information regarding enantiornithine anatomy, evolution, and diversity. © 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 162 , 201–219.     

Pelvis morphology suggests that early Mesozoic birds were too heavy to contact incubate their eggs

Numerous new fossils have driven an interest in reproduction of early birds, but direct evidence remains elusive. No Mesozoic avian eggs can be unambiguously assigned to a species, which hampers our understanding of the evolution of contact incubation, which is a defining feature of extant birds. Compared to living species, eggs of Mesozoic birds are relatively small, but whether the eggs of Mesozoic birds could actually have borne the weight of a breeding adult has not yet been investigated. We estimated maximal egg breadth for a range of Mesozoic avian taxa from the width of the pelvic canal defined by the pubic symphysis. Known elongation ratios of Mesozoic bird eggs allowed us to predict egg mass and hence the load mass an egg could endure before cracking. These values were compared to the predicted body masses of the adult birds based on skeletal remains. Based on 21 fossil species, we show that for nonornithothoracine birds body mass was 187% of the load mass of the eggs. For Enantiornithes, body mass was 127% greater than the egg load mass, but some early Cretaceous ornithuromorphs were 179% heavier than their eggs could support. Our indirect approach provides the best evidence yet that early birds could not have sat on their eggs without running the risk of causing damage. We suggest that contact incubation evolved comparatively late in birds.     

The origin and early evolution of birds

Birds evolved from and are phylogenetically recognized as members of the theropod dinosaurs; their first known member is the Late Jurassic Archaeopteryx, now represented by seven skeletons and a feather, and their closest known non-avian relatives are the dromaeosaurid theropods such as Deinonychus. Bird flight is widely thought to have evolved from the trees down, but Archaeopteryx and its outgroups show no obvious arboreal or tree-climbing characters, and its wing planform and wing loading do not resemble those of gliders. The ancestors of birds were bipedal, terrestrial, agile, cursorial and carnivorous or omnivorous. Apart from a perching foot and some skeletal fusions, a great many characters that are usually considered ‘avian’ (e.g. the furcula, the elongated forearm, the laterally flexing wrist and apparently feathers) evolved in non-avian theropods for reasons unrelated to birds or to flight. Soon after Archaeopteryx, avian features such as the pygostyle, fusion of the carpometacarpus, and elongated curved pedal claws with a reversed, fully descended and opposable hallux, indicate improved flying ability and arboreal habits. In the further evolution of birds, characters related to the flight apparatus phylogenetically preceded those related to the rest of the skeleton and skull. Mesozoic birds are more diverse and numerous than thought previously and the most diverse known group of Cretaceous birds, the Enantiornithes, was not even recognized until 1981. The vast majority of Mesozoic bird groups have no Tertiary records: Enantiornithes, Hesperornithiformes, Ichthyornithiformes and several other lineages disappeared by the end of the Cretaceous. By that time, a few Linnean ‘Orders’ of extant birds had appeared, but none of these taxa belongs to extant ‘families’, and it is not until the Paleocene or (in most cases) the Eocene that the majority of extant bird ‘Orders’ are known in the fossil record. There is no evidence for a major or mass extinction of birds at the end of the Cretaceous, nor for a sudden ‘bottleneck’ in diversity that fostered the early Tertiary origination of living bird ‘Orders’.     

New enantiornithine bird (Aves, Ornithothoraces) from the Late Cretaceous of NW Argentina

A new enantiornithine bird, Intiornis inexpectatus gen. et sp. nov, is described here. It is based on a partial hind limb found in beds of the Upper Cretaceous Las Curtiembres Formation (Campanian), North-West Argentina. The new taxon is referred to the family Avisauridae on the basis of its cranially convex third metatarsal. Several features suggest close relationships between Intiornis and the avisaurid Soroavisaurus, from the Lecho Formation (Maastrichtian; North-West Argentina). Intiornis was the size of a sparrow, thus representing the smallest Enantiornithes known from South America. The new species shows adaptations for a perching mode of life. Moreover, the hypothesis suggesting that the flying pterosaur reptiles decrease in taxonomic diversity due to competitive interaction with birds is discussed. The new species shows adaptations for a perching mode of life. Moreover, the hypothesis suggesting that the flying pterosaur reptiles decrease in taxonomic diversity due to competitive interaction with birds is discussed.     

Synsacrum of a primitive bird from the Upper Cretaceous of Uzbekistan

A partial synsacrum of a primitive bird from the Zenge Kurgan 3 locality in the Kyzyl Kum Desert (Uzbekistan) is described. The vertebrate fauna from this locality is similar to that of the Bissekty Formation of the Dzharakuduk locality (Central Kyzyl Kum, Uzbekistan); however, this synsacrum differs considerably from all other synsacra from Dzharakuduk. The taxonomic position of this bird remains uncertain; it is most similar to some Enantiornithes, although it could have belonged to a primitive ornithuromorph bird. The functional significance of structural differences in the synsacrum of ornithurine and enantiornithine birds is discussed.     

中国中生代鸟类后肢骨骼的长度比例特征及栖息习性的分析

通过对18目59科137例现生不同栖息习性鸟类的后肢3块骨骼(股骨、胫跗骨和跗跖骨)长度比例的观察和特征分析,推断出鸟类的栖息习性与后肢3块骨骼中各骨骼长度所占总长度的比例存在密切的关系。即在所有鸟类的后肢骨骼中,胫跗骨的长度占3块骨骼的比例为最大;地栖鸟类后肢骨骼中股骨的长度要短于跗跖骨;树栖鸟类后肢骨骼中股骨的长度要长于跗跖骨。鸟类后肢3块骨骼的长度比例特征是鸟类长期对栖息等行为适应的结果。在此基础上,对中国中生代14例鸟类的栖息习性进行了分析,利用三元投影的统计方法,并以国内外新生代(古近纪和新近纪)21例鸟类标本作为对比参考,得出辽西中生代不同类型鸟类的栖息行为特征:基干鸟类以树栖为主要习性,其中个别鸟类还具有攀援的习性,而反鸟类则是典型的树栖鸟类,今鸟类兼有树、地栖的习性。研究表明,在现行的鸟类系统发育框架下,树栖适应(及攀援)代表了鸟类演化历史中最原始的生活方式。这一结论也支持鸟类飞行的树栖起源假说。中生代鸟类栖息习性分异的多样性反映了早期鸟类演化过程中自身以及与其他同期生物在生态空间和食物资源的竞争的加剧和对环境的不断适应。     

Barb geometry of asymmetrical feathers reveals a transitional morphology in the evolution of avian flight

The geometry of feather barbs (barb length and barb angle) determines feather vane asymmetry and vane rigidity, which are both critical to a feather''s aerodynamic performance. Here, we describe the relationship between barb geometry and aerodynamic function across the evolutionary history of asymmetrical flight feathers, from Mesozoic taxa outside of modern avian diversity (Microraptor, Archaeopteryx, Sapeornis, Confuciusornis and the enantiornithine Eopengornis) to an extensive sample of modern birds. Contrary to previous assumptions, we find that barb angle is not related to vane-width asymmetry; instead barb angle varies with vane function, whereas barb length variation determines vane asymmetry. We demonstrate that barb geometry significantly differs among functionally distinct portions of flight feather vanes, and that cutting-edge leading vanes occupy a distinct region of morphospace characterized by small barb angles. This cutting-edge vane morphology is ubiquitous across a phylogenetically and functionally diverse sample of modern birds and Mesozoic stem birds, revealing a fundamental aerodynamic adaptation that has persisted from the Late Jurassic. However, in Mesozoic taxa stemward of Ornithurae and Enantiornithes, trailing vane barb geometry is distinctly different from that of modern birds. In both modern birds and enantiornithines, trailing vanes have larger barb angles than in comparatively stemward taxa like Archaeopteryx, which exhibit small trailing vane barb angles. This discovery reveals a previously unrecognized evolutionary transition in flight feather morphology, which has important implications for the flight capacity of early feathered theropods such as Archaeopteryx and Microraptor. Our findings suggest that the fully modern avian flight feather, and possibly a modern capacity for powered flight, evolved crownward of Confuciusornis, long after the origin of asymmetrical flight feathers, and much later than previously recognized.