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Mummified Precocial Bird Wings in Mid-Cretaceous

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Mummified Precocial Bird Wings in Mid-Cretaceous ARTICLE Received 18 Jan 2016 | Accepted 27 May 2016 | Published 28 Jun 2016 DOI: 10.1038/ncomms12089 OPEN Mummified precocial bird wings in mid-Cretaceous Burmese amber Lida Xing1,2,*, Ryan C. McKellar3,4,*, Min Wang5,*, Ming Bai6,*, Jingmai K. O’Connor5, Michael J. Benton7, Jianping Zhang2, Yan Wang8, Kuowei Tseng9, Martin G. Lockley10, Gang Li11, Weiwei Zhang12 & Xing Xu5,* 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. 1 State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Beijing 100083, China. 2 School of the Earth Sciences and Resources, China University of Geosciences, Beijing 100083, China. 3 Palaeontology, Royal Saskatchewan Museum, Regina, Saskatchewan, Canada S4P 2V7. 4 Biology Department, University of Regina, Regina, Saskatchewan, Canada S4S 0A2. 5 Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China. 6 Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China. 7 School of Earth Sciences, University of Bristol, Bristol BS8 1RJ, UK. 8 Institute of Geology and Paleontology, Linyi University, Linyi 276000, China. 9 Department of Exercise and Health Science, University of Taipei, Taipei 11153, China. 10 Dinosaur Tracks Museum, University of Colorado Denver, Denver, Colorado 80217, USA. 11 Institute of High Energy Physics, Chinese Academy of Science, Beijing 100049, China. 12 P.O. Box 4680, Chongqing 400015, China. * These authors contributed equally to this work. Correspondence and requests for materials should be addressed to L.X. (email: [email protected]) or to R.C.M. (email: [email protected]). NATURE COMMUNICATIONS | 7:12089 | DOI: 10.1038/ncomms12089 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms12089 he mid-Cretaceous Burmese amber deposit of northeastern including Archaeopteryx, Jeholornis and Confuciusornis18–20,25. Myanmar is one of the most prolific and well-studied The minor metacarpal terminates distal to the major metacarpal, Tsources of exceptionally preserved Mesozoic arthropod and a synapomorphy of enantiornithines20,26. The minor metacarpal plant fossils, but work on feathers from this deposit has just is dorsoventrally expanded, in caudal view appearing as robust as begun1–4. Previous studies of plumage in Cretaceous amber the major metacarpal, a feature common in enantiornithines27. have been based on isolated feathers, leaving taxonomy of the Both specimens preserve a single, reduced, wedge-shaped phalanx feather-bearers open to debate5,6, and amber in vertebrate in the minor digit as in some ornithothoracines. bone beds has seldom yielded fossils7. Otherwise, Cretaceous feathers are commonly known from carbonaceous compression fossils8–10, and three-dimensional preservation in amber is Plumage in DIP-V-15100. Specimen DIP-V-15100 (Fig. 2, extremely rare. The combined fossil record of amber and Supplementary Figs 1 and 2) preserves a range of plumage from compression fossils has provided many insights into how the the manus and distal forearm. This includes the basal portions of feather types associated with modern birds developed11,12, but nine highly asymmetrical primary flight feathers and five these glimpses are restricted by preservation in each fossil type. secondary feathers (six of the primaries are conclusive, but the The discovery of two partial bird wings in Burmese amber unites distinction between primary and secondary feathers is obscured taxonomic and ontogenetic information from osteology with by overlap within the proximal part of the wing; Figs 1a and 2c). microscopic preservation down to the level of individual feather The rachises within primaries are sub-cylindrical in cross-section barbules and their pigment distributions. This new source of (expanded dorsoventrally and constricted laterally), with a weakly information includes integumentary features incompletely known developed ventral ridge and groove combination (Fig. 2d). Each in the compression fossil record13. barb ramus is lanceolate and bears an asymmetrical arrangement The studied specimens come from the Angbamo site, Tanai of proximal barbules that are blade-shaped throughout most of Township, Myitkyina District, Kachin Province of Myanmar. A their length, along with blade-shaped distal barbules that taper combination of biostratigraphy and radiometric dating have into a poorly-defined pennulum bearing hooklets (Fig. 2e). established an age estimate of 98.8±0.6 Ma for this deposit2,14,15. The alula has three feathers clearly visible, and is distinct from the The two partial wings (DIP-V-15100 and DIP-V-15101) are tiny, main surface of the wing (Fig. 2a,g). Barbs within the alula and are preserved within a few cubic centimeters of amber. have much broader and more asymmetrical barbules than in the They were examined by combining synchrotron X-ray micro-CT primaries and coverts, distal barbules have a well-developed data for osteology, with standard macro- and microscopic observations of integumentary structures. The small size and poorly-defined articular facets indicate that both specimens ab were juveniles at the time of death. Although the specimens are similar in gross morphology, proportions and some plumage characteristics, their immaturity limits detailed comparisons. We tentatively suggest that the specimens belong to the same mi ma species, and suggest that the following anatomical description should be treated with some caution, given the potential for ul mim mam large-scale ontogenetic changes. ra al Results am Osteology. In both wing fragments, the ulna and radius are incomplete and missing their proximal parts (Fig. 1). The ulna is mediolaterally compressed and bears a well-defined semilunate cde trochlear surface distally. There is no sign of quill knobs for the attachment of the secondary remiges. The radius is straight and measures less than half the width of the ulna. Only three digits are present, and the preserved phalanges suggest that the manual formula is 2-3-1. To avoid confusion about digital identities among three-fingered theropods including birds (I-II-III or ma II-III-IV; see ref. 16 and references therein), we use the alular, mi major and minor digit to refer to the anterior, middle and posterior mam digits, respectively. The alular metacarpal is rod-like and long, approaching one-quarter of the major digit in length, and 455% of the length of alular phalanx-1, whereas in basal avialans and mim non-avialan theropods, like dromaesaurids, the latter ratio is al higher17–21. As in most basal avialans21,22, alular phalanx-1 fails to reach the distal end of the major metacarpal (Fig. 1b,e), but the opposite is true in most non-avialan theropods, such as dromaeosaurids and scansoriopterygids17,23. The alular ungual Figure 1 | SR X-ray lCT reconstructions of osteology in DIP-V-15100 and is slightly smaller than that of the major digit, and both claws are DIP-V-15101. (a) Mummified DIP-V-15100, showing rachises, skin, muscle strongly recurved. The major metacarpal is robust and rod-like, and claws. (b) Skeletal morphology of DIP-V-15100, using different density and forms a weakly defined ginglymoid articular facet for major threshold. (c) Mummified DIP-V-15101, showing rachises, skin, muscle and phalanx-1. As in Sapeornis and more advanced birds such as claws. (d) Skeletal morphology of DIP-V-15101. (e) Reconstruction of enantiornithines and ornithuromorphs21,22,24, major phalanx-1 osteology based on the CT data. al, alular digit; am, alular metacarpal; ma, is longer than major phalanx-2; in contrast, the latter phalanx is major digit; mam, major metacarpal; mi, minor digit; mim, minor longer in most other non-avialan theropods and basal avialans, metacarpal; ra, radius; ul, ulna. Scale bars, 5 mm. 2 NATURE COMMUNICATIONS | 7:12089 | DOI: 10.1038/ncomms12089 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | DOI: 10.1038/ncomms12089 ARTICLE i e a j f b g k c d h l Figure 2 | DIP-V-15100 photomicrographs. (a) Overview of dorsal wing surface, with claws (red arrows), dorsal details in a–h.(b) Primary feathers and barbs truncated by amber surface. (c) Primaries (white arrows), secondaries (yellow arrows) and indeterminate feather (orange arrow), in basal zone of overlap (slightly oblique view). (d) Detail of primary rachis, with weak ventral ridge (inclined arrow) and barb ramus attachment
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