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Concept: Enantiornithes

132

Fossils of juvenile Mesozoic birds provide insight into the early evolution of avian development, however such fossils are rare. The analysis of the ossification sequence in these early-branching birds has the potential to address important questions about their comparative developmental biology and to help understand their morphological evolution and ecological differentiation. Here we report on an early juvenile enantiornithine specimen from the Early Cretaceous of Europe, which sheds new light on the osteogenesis in this most species-rich clade of Mesozoic birds. Consisting of a nearly complete skeleton, it is amongst the smallest known Mesozoic avian fossils representing post-hatching stages of development. Comparisons between this new specimen and other known early juvenile enantiornithines support a clade-wide asynchronous pattern of osteogenesis in the sternum and the vertebral column, and strongly indicate that the hatchlings of these phylogenetically basal birds varied greatly in size and tempo of skeletal maturation.

Concepts: Evolution, Biology, Developmental biology, Skeletal system, Bird, Cretaceous, Intramembranous ossification, Enantiornithes

60

Our knowledge of Cretaceous plumage is limited by the fossil record itself: compression fossils surrounding skeletons lack the finest morphological details and seldom preserve visible traces of colour, while discoveries in amber have been disassociated from their source animals. Here we report the osteology, plumage and pterylosis of two exceptionally preserved theropod wings from Burmese amber, with vestiges of soft tissues. The extremely small size and osteological development of the wings, combined with their digit proportions, strongly suggests that the remains represent precocial hatchlings of enantiornithine birds. These specimens demonstrate that the plumage types associated with modern birds were present within single individuals of Enantiornithes by the Cenomanian (99 million years ago), providing insights into plumage arrangement and microstructure alongside immature skeletal remains. This finding brings new detail to our understanding of infrequently preserved juveniles, including the first concrete examples of follicles, feather tracts and apteria in Cretaceous avialans.

Concepts: Bird, Fossil, Paleontology, Dinosaur, Enantiornithes

28

The sternum is one of the most important and characteristic skeletal elements in living birds, highly adapted for flight and showing a diverse range of morphologies. New exceptional material of young juvenile specimens from the Early Cretaceous Jehol Group in northeastern China reveals the unique sequence of development in the sternum of Enantiornithes, the dominant clade of Cretaceous birds. We recognize six ossifications that together form the sternum, three of which were previously unknown. Here we show that although basal living birds apparently have retained the dinosaurian condition in which the sternum develops from a bilateral pair of ossifications (present in paravian dinosaurs and basal birds), the enantiornithine sternal body primarily develops from two unilateral proximo-distally arranged ossifications. This indicates that although superficially similar, the sternum formed very differently in enantiornithines and ornithuromorphs, suggesting that several ornithothoracine sternal features may represent parallelism. This highlights the importance of ontogenetic studies for understanding homology and the evolution of skeletal features in palaeontology.

Concepts: Evolution, Bird, Cretaceous, Paleontology, Dinosaur, Cretaceous–Tertiary extinction event, Enantiornithes, Psittacosaurus

18

Enantiornithes are the most successful clade of Mesozoic birds. Here, we describe a new enantiornithine bird, Cruralispennia multidonta gen. et sp. nov., from the Protopteryx-horizon of the Early Cretaceous Huajiying Formation of China. Despite being among the oldest known enantiornithines, Cruralispennia displays derived morphologies that are unexpected at such an early stage in the evolution of this clade. A plough-shaped pygostyle, like that of the Ornithuromorpha, evolved convergently in the Cruralispennia lineage, highlighting the homoplastic nature of early avian evolution. The extremely slender coracoid morphology was previously unknown among Early Cretaceous enantiornithines but is common in Late Cretaceous taxa, indicating that by 131 million years ago this clade had already experienced considerable morphological differentiation. Cruralispennia preserves unusual crural feathers that are proximally wire-like with filamentous distal tips, a new morphotype previously unknown among fossil or modern feathers, further increasing the known diversity of primitive feather morphologies.

Concepts: Evolution, Bird, Cretaceous, Dinosaur, Feather, Cretaceous–Tertiary extinction event, Enantiornithes, Psittacosaurus

8

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.

Concepts: Bird, Reptile, Difference, Cretaceous, Dinosaur, Feather, Cretaceous–Tertiary extinction event, Enantiornithes

5

Modern birds differ from their theropod ancestors in lacking teeth and heavily constructed bony jaws, having evolved a lightly built beak and a specialized digestive system capable of processing unmasticated food [1, 2]. Enantiornithes, the most successful clade of Mesozoic birds, represents the sister group of the Ornithuromorpha, which gave rise to living birds [3]. Nevertheless, the feeding habits of enantiornithines have remained unknown because of a lack of fossil evidence. In contrast, exceptionally preserved fossils reveal that derived avian features were present in the digestive systems of some non-enantiornithine birds with ages exceeding 125 million years [4, 5]. Here, we report a new piscivorous enantiornithine from the Early Cretaceous Jehol Biota of China. This specimen preserves a gastric pellet that includes fish bones. The new enantiornithine, like many modern piscivores and raptors, seems to have swallowed its prey whole and regurgitated indigestible materials such as bones, invertebrate exoskeletons, scales, and feathers. This fossil represents the oldest unambiguous record of an avian gastric pellet and the only such record from the Mesozoic. The pellet points to a fish diet and suggests that the alimentary tract of the new enantiornithine resembled that of extant avians in having efficient antiperistalsis and a two-chambered stomach with a muscular gizzard capable of compacting indigestible matter into a cohesive pellet. The inferred occurrence of these advanced features in an enantiornithine implies that they were widespread in Cretaceous birds and likely facilitated dietary diversification within both Enantiornithes and Ornithuromorpha.

Concepts: Digestive system, Bird, Human gastrointestinal tract, Abdomen, Digestion, Paleontology, Dinosaur, Enantiornithes

0

The midline pattern of sternal ossification characteristic of the Cretaceous enantiornithine birds is unique among the Ornithodira, the group containing birds, non-avian dinosaurs and pterosaurs. This has been suggested to indicate that Enantiornithes is not the sister group of Ornithuromorpha, the clade that includes living birds and their close relatives, which would imply rampant convergence in many non-sternal features between enantiornithines and ornithuromorphs. However, detailed comparisons reveal greater similarity between neornithine (i.e. crown group bird) and enantiornithine modes of sternal ossification than previously recognized. Furthermore, a new subadult enantiornithine specimen demonstrates that sternal ossification followed a more typically ornithodiran pattern in basal members of the clade. This new specimen, referable to the Pengornithidae, indicates that the unique ossification pattern observed in other juvenile enantiornithines is derived within Enantiornithes. A similar but clearly distinct pattern appears to have evolved in parallel in the ornithuromorph lineage. The atypical mode of sternal ossification in some derived enantiornithines should be regarded as an autapomorphic condition rather than an indication that enantiornithines are not close relatives of ornithuromorphs. Based on what is known about molecular mechanisms for morphogenesis and the possible selective advantages, the parallel shifts to midline ossification that took place in derived enantiornithines and living neognathous birds appear to have been related to the development of a large ventral keel, which is only present in ornithuromorphs and enantiornithines. Midline ossification can serve to medially reinforce the sternum at a relatively early ontogenetic stage, which would have been especially beneficial during the protracted development of the super-precocial Cretaceous enantiornithines. This article is protected by copyright. All rights reserved.

Concepts: Bird, Phylogenetics, Clade, Dinosaur, Crown group, Cretaceous–Tertiary extinction event, Enantiornithes, Ornithothoraces

0

Enantiornithines are the most diverse avian clade in the Cretaceous. However, morphological specializations indicative of specific ecological roles are not well known for this clade. Here we report on an exquisitely well-preserved specimen from the Lower Cretaceous Jehol Group of northeastern China, which pedal morphology is suggestive of a unique ecological specialization within Enantiornithes. The morphology of the new specimen is largely indistinguishable from that of the holotype of the bohaiornithid enantiornithine Zhouornis hani, albeit the latter is somewhat larger. The new specimen provides important and previously unknown details of the skull of Zhouornis hani, which add to the limited knowledge about the cranial anatomy and evolution of enantiornithines. The information offered by the new specimen also augments our understanding of the postcranial morphology of bohaiornithid enantiornithines, a clade that has been only recently recognized. With the description of this specimen, Zhouornis hani becomes one of the most anatomically complete known enantiornithine species, which will facilitate future morphological studies.

Concepts: Evolution, Biology, Bird, China, Anatomy, Cretaceous, Cretaceous–Tertiary extinction event, Enantiornithes