Mummified precocial bird wings in mid-Cretaceous Burmese amber

doi:10.1038/ncomms12089

. 2016 Jun 28:7:12089.

doi: 10.1038/ncomms12089.

Mummified precocial bird wings in mid-Cretaceous Burmese amber

Lida Xing^{1

2}, Ryan C McKellar^{3

4}, Min Wang⁵, Ming Bai⁶, Jingmai K O'Connor⁵, Michael J Benton⁷, Jianping Zhang², Yan Wang⁸, Kuowei Tseng⁹, Martin G Lockley¹⁰, Gang Li¹¹, Weiwei Zhang, Xing Xu⁵

Affiliations

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.

PMID: 27352215
PMCID: PMC4931330
DOI: 10.1038/ncomms12089

Mummified precocial bird wings in mid-Cretaceous Burmese amber

Lida Xing et al. Nat Commun. 2016.

. 2016 Jun 28:7:12089.

doi: 10.1038/ncomms12089.

Authors

Affiliations

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.

PMID: 27352215
PMCID: PMC4931330
DOI: 10.1038/ncomms12089

Abstract

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.

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Figures

**Figure 1. SR X-ray μCT reconstructions of osteology in DIP-V-15100 and DIP-V-15101.**
(a) Mummified DIP-V-15100, showing rachises, skin, muscle and claws. (b) Skeletal morphology of DIP-V-15100, using different density threshold. (c) Mummified DIP-V-15101, showing rachises, skin, muscle and claws. (d) Skeletal morphology of DIP-V-15101. (e) Reconstruction of osteology based on the CT data. al, alular digit; am, alular metacarpal; ma, major digit; mam, major metacarpal; mi, minor digit; mim, minor metacarpal; ra, radius; ul, ulna. Scale bars, 5 mm.

**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 somewhat low on side of rachis (horizontal arrow). (e) Primary feather microstructure and pigment distribution (t.l.), with hooklets on distal barbules (arrow). (f) Alula barbs with blunted apices and blade-like barbules with banded pigmentation. (g) Anterodorsal view highlighting alula separation from wing surface (arrows), as well as overall colour patterning (light hitting bubbles in amber creates a bright band paralleling edge of wing). (h) Bone and integument breaching amber surface, with well-preserved osteon complexes (circle of mottled bone at arrow), while most voids in bone and tissue have been permeated by milky amber, and skin is reduced to a translucent film not visible at this scale. (i) Extent of gas vacuoles and milky amber emanating from dorsal and ventral surfaces of wing, in anterior view. (j) Contrast between coverts and ventral coat of down and contours, with ventral details in j–l. (k) Current position of claw (red arrow) and claw marks within flow lines (yellow arrows). (l) Bases of down feathers attached to apterium with preserved skin texture and signs of saponification. Scale bars, 2.5 mm (a,c); 1 mm (b,h–l); 0.5 mm (d); 0.25 mm (e,f); 1.5 mm (g); t.l., transmitted light.

**Figure 3. Photomicrographs of DIP-V-15101.**
(a) Overview of dorsal wing surface, with claws (red arrows), and extent of coverts along posterior edge of wing (white arrow), dorsal details in a–e. (b) Pale or white plumage spot at base of alula. (c) Contrasting plumage colours and structure near alular digit and claw. (d) Narrow, flexible barb morphology and paler pigmentation in secondary coverts (near arrow in a). (e) Pigment distribution within blade-shaped barbules of alula. (f) Ventral wing surface (apex of primaries in upper left corner), with flap of feather-bearing skin trailing off the proximal edge of wing in counterclockwise direction (arrow), ventral details in f–l. (g) Primaries, where they were apically truncated by amber polishing (arrow). (h) Secondaries, where they have been curled by resin flows, displaying their flexible barbs, and the mixture of contour feathers and down that protrude through a veil of milky amber towards the middle of the wing surface. (i) Barbule morphology and pigmentation in an isolated flight feather. (j) Mat of white plumulaceous barbs (down) near proximal margin of skin flap, with skin towards bottom of image. (k) Definitive down inserting into skin surface, with calamus (arrow) and small sheath basally. (l) Pennaceous and plumulaceous barbs from contour feathers on the skin flap. Scale bars, 2.5 mm (a,f); 1 mm (b–d,g,h,j); 0.5 mm (e,i,k,l).

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References

1. Grimaldi D. A., Engel M. S. & Nascimbene P. C. Fossiliferous Cretaceous amber from Myanmar (Burma): its rediscovery, biotic diversity, and paleontological significance. Am. Mus. Novit. 3361, 1–72 (2002).
1. Ross A., Mellish C., York P. & Crighton B. in Biodiversity of Fossils in Amber from the Major World Deposits ed. Penney D. 208–235Siri Scientific Press (2010).
1. Nascimbene P. C., Dove C. J., Grimaldi D. A. & Schmidt A. R. in 9th European Palaeobotany-Palynology Conference, Abstract Book 113–114 (Padova, Italy, (2014).
1. Thomas D. B., Nascimbene P. C., Dove C. J., Grimaldi D. A. & James H. F. Seeking carotenoid pigments in amber-preserved fossil feathers. Sci. Rep. 4, 5226 (2014). - PMC - PubMed
1. Perrichot V., Marion L., Néraudeau D., Vullo R. & Tafforeau P. The early evolution of feathers: fossil evidence from Cretaceous amber of France. Proc. R. Soc. B 275, 1197–1202 (2008). - PMC - PubMed

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[1] Grimaldi D. A., Engel M. S. & Nascimbene P. C. Fossiliferous Cretaceous amber from Myanmar (Burma): its rediscovery, biotic diversity, and paleontological significance. Am. Mus. Novit. 3361, 1–72 (2002).

[2] Grimaldi D. A., Engel M. S. & Nascimbene P. C. Fossiliferous Cretaceous amber from Myanmar (Burma): its rediscovery, biotic diversity, and paleontological significance. Am. Mus. Novit. 3361, 1–72 (2002).

[3] Ross A., Mellish C., York P. & Crighton B. in Biodiversity of Fossils in Amber from the Major World Deposits ed. Penney D. 208–235Siri Scientific Press (2010).

[4] Ross A., Mellish C., York P. & Crighton B. in Biodiversity of Fossils in Amber from the Major World Deposits ed. Penney D. 208–235Siri Scientific Press (2010).

[5] Nascimbene P. C., Dove C. J., Grimaldi D. A. & Schmidt A. R. in 9th European Palaeobotany-Palynology Conference, Abstract Book 113–114 (Padova, Italy, (2014).

[6] Nascimbene P. C., Dove C. J., Grimaldi D. A. & Schmidt A. R. in 9th European Palaeobotany-Palynology Conference, Abstract Book 113–114 (Padova, Italy, (2014).

[7] Thomas D. B., Nascimbene P. C., Dove C. J., Grimaldi D. A. & James H. F. Seeking carotenoid pigments in amber-preserved fossil feathers. Sci. Rep. 4, 5226 (2014). - PMC - PubMed

[8] Thomas D. B., Nascimbene P. C., Dove C. J., Grimaldi D. A. & James H. F. Seeking carotenoid pigments in amber-preserved fossil feathers. Sci. Rep. 4, 5226 (2014). - PMC - PubMed

[9] Perrichot V., Marion L., Néraudeau D., Vullo R. & Tafforeau P. The early evolution of feathers: fossil evidence from Cretaceous amber of France. Proc. R. Soc. B 275, 1197–1202 (2008). - PMC - PubMed

[10] Perrichot V., Marion L., Néraudeau D., Vullo R. & Tafforeau P. The early evolution of feathers: fossil evidence from Cretaceous amber of France. Proc. R. Soc. B 275, 1197–1202 (2008). - PMC - PubMed

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Mummified precocial bird wings in mid-Cretaceous Burmese amber

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Mummified precocial bird wings in mid-Cretaceous Burmese amber

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