An unusually large bird wing in mid-Cretaceous Burmese amber

Journal Pre-proof An unusually large bird wing in mid-Cretaceous Burmese amber Lida Xing, Ryan C. McKellar, Jingmai K. O'Connor PII:

S0195-6671(19)30459-8

DOI:

https://doi.org/10.1016/j.cretres.2020.104412

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YCRES 104412

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Cretaceous Research

Received Date: 29 October 2019 Revised Date:

28 January 2020

Accepted Date: 29 January 2020

Please cite this article as: Xing, L., McKellar, R.C., O'Connor, J.K., An unusually large bird wing in midCretaceous Burmese amber, Cretaceous Research, https://doi.org/10.1016/j.cretres.2020.104412. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Ltd.

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An unusually large bird wing in mid-Cretaceous Burmese amber

2 3

Lida Xing 1, 2, Ryan C. McKellar 3, 4, 5*, Jingmai K. O'Connor 6

4 5

1. State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Beijing 100083, China

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2. School of the Earth Sciences and Resources, China University of Geosciences, Beijing 100083, China

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3. Royal Saskatchewan Museum, Regina, Saskatchewan S4P 4W7, Canada

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4. Biology Department, University of Regina, Regina, Saskatchewan S4S 0A2, Canada

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5. Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, Kansas, 66045, USA.

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6. Key Laboratory of Vertebrate Evolution and Human Origins of the Chinese Academy of Sciences, Institute of Vertebrate

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Paleontology and Paleoanthropology, Beijing 100044, China

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Correspondence and requests for materials should be addressed to R.M ([email protected]).

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Abstract

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All of the bird specimens previously recovered from Burmese amber have belonged to either

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immature specimens, or small-bodied taxa belonging to Enantiornithes. This has led to

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questions about whether the size bias inherent to preservation in amber has limited inclusions

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to smaller individuals or species, or if the avifauna of the amber-producing forest had a

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stronger representation of small-bodied taxa than other Cretaceous assemblages. A newly

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discovered inclusion of a fragmentary bird wing is described here: specimen LV-0321 likely

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belonged to an individual that was in excess of 10 cm long (snout to vent length). The new

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specimen also displays more prominent light-and-dark banding patterns among the primary

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flight feathers than any of the wings previously described from the deposit. In addition to

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increasing the known size range for enantiornithines within the assemblage, the new specimen

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sheds further light on the appearance of the plumage in these Cretaceous birds.

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Keywords: Enantiornithes; Myanmar; Albian-Cenomanian; palaeoecology; pigmentation

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1. Introduction

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Burmese amber has provided a surprisingly abundant and diverse suite of enantiornithine

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inclusions over the last five years. This material has included isolated wing fragments from

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juveniles (Xing et al., 2016a), the skin and bones from the right side of a hatchling (Xing et

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al., 2017), and a more complete but strongly compressed juvenile skeleton (Xing et al.,

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2018c). A series of feet from perching, probing, and raptorial species (Xing et al., 2019a,b, in

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press) have recently expanded the known diversity of ecological roles for enantiornithines

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within the Burmese amber forest and for the clade as a whole. Some of these feet are

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accompanied by wing fragments or specialized plumage. Nearly all of the enantiornithine

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remains recovered to date have been from osteologically immature specimens, or from

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individuals that may have been approaching maturity, but belong to small-bodied taxa. It

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appears that the deposit may contain a diverse assemblage of small-bodied birds that are

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unlike those sampled by compression fossil records elsewhere: this is either a result of

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preservational bias in the amber record (Martínez-Delclós et al., 2004), or indicates that the

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West Burma Block contained a fauna that was distinct from that of mainland Asia during the

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mid-Cretaceous (e.g., Poinar, 2018). In addition to skeletal remains, Burmese amber has

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proven to be a rich source of isolated feather fossils (Grimaldi et al., 2002; Nascimbene et al.,

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2013, 2014; Peñalver et al., 2018; Xing et al. 2018a, submitted). Most of these specimens

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appear to have come from enantiornithines, based on structural similarities, as well as

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discoveries of similar plumage attached to skeletal material in the deposit and within

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specimens from the Jehol Biota (such as O’Connor et al., 2013; O'Connor and Zhou, 2015)

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and elsewhere (Carvalho et al., 2015). Together with the skeletally associated feathers, the

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isolated feathers have shed light on enigmatic feather morphotypes, such as the

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rachis-dominated feathers (RDFs) which form the tail plumage in Confuciusornithiformes and

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many enantiornithines. They are also improving our understanding of the trophic relationships

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(Peñalver et al., 2017), microstructure, and pigmentation patterns (Xing et al., submitted a) in

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enantiornithines.

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Here we describe a new wing specimen from Burmese amber, LV-0321. This specimen is significantly larger than the wings previously described from the deposit. Consequently, its

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preservation is reduced compared to some of the previous discoveries, leaving only a few of

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the bones from the manus preserved alongside a series of flight feathers that display clear

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pigmentation patterns.

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2. Material and Methods

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A new amber piece, LV-0321 (Lvming Amber Exhibition Hall, Beijing, China), contains an

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incomplete avian forelimb. LV-0321 is 49.9 mm x 53.3 mm x 52.3 mm, and it weighs 79.4 g.

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Based on biostratigraphic evidence (ammonites and pollen) from the Xipiugong site, LV-0321

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can be dated as late Albian–Cenomanian (~105 to 95 Ma) (Cruickshank and Ko, 2003; Ross

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et al., 2010). This estimation is consistent with radiogenic isotope data (U-Pb) from

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volcaniclastic zircons indicating a 98.8 ± 0.6 Ma (Shi et al., 2012) age for the deposit.

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LV-0321 was scanned with a Nikon Metrology XTH 225/320 LC dual source industrial

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micro-computed tomographic scanner, housed in the China University of Geosciences,

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Beijing (CUGB), China. The specimen was scanned with beam strength of 130 KV, and an

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absorption contrast and a spatial resolution of 32.43 µm. Photographs were taken using a

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Canon digital camera (Canon EOS 5D DSLR and EF 100mm F/2.8L IS USM) and were

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processed using Helicon Focus 5.1 and Adobe Photoshop CS5 software to increase depth of

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field in the images.

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Destructive sampling was not permitted for LV-0321 (necessary for SEM or TEM

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analyses). As a result, our discussion of feather colours is restricted to the intensity and

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distribution of pigmentation, and the apparent colour patterns that these features present under

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visible light. SEM analyses have revealed eumelanosomes within darkly pigmented areas of

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other feathers from the deposit (Xing et al., 2016b), but the presence and types of chemical

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pigments within each sample, and their taphonomic histories of labile molecules in amber are

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in the early stages of study (Thomas et al., 2014; McCoy et al., 2018, 2019).

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3. Description

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3.1. Osteology

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Three articulated manual elements of the right wing are preserved (Fig. 1), consisting of two

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complete phalanges and a proximal element of uncertain identity (see Discussion). Their

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combined length measures less than a centimeter. As preserved, the proximal element is

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rectangular; the preserved length is twice the craniocaudal width, which is 50% greater than

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the dorsoventral thickness (ungual 2 mm; penultimate phalanx 4.7 mm; proximal element 1.2

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mm). The proximal exposed surface is triangular with the acute angle caudally oriented. The

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element is weakly tapered so that the proximal end is larger than the distal articular surface.

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The latter surface is poorly developed and relatively flat, apparently not ginglymous, and

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weakly angled proximocranial-caudodistally. The cranial surface appears excavated although

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this may be a preservational artifact. The penultimate phalanx is twice as long as the

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preserved length of the preceding element. The shaft tapers distally although the distal

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articular surface is expanded relative to the shaft and ginglymous. The ungual phalanx has

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been rotated so that the dorsal surface is caudally oriented. It measures slightly less than half

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the length of the penultimate phalanx but the distal third appears to consist of keratinous

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sheath and not bone. The ungual is strongly recurved. This curvature is exaggerated by the

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keratinous sheath. The entire claw is dorsoventrally compressed. Proximally a well-developed

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flexor tubercle is present.

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3.2. Feathers and skin

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Most of the primary remiges are preserved and clearly visible from their dorsal surface, but

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the remainder of the wing is only represented by small regions of plumage due to its basal

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truncation (Fig. 2). Near the base of the preserved wing section, two alular coverts are visible

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as relatively complete feathers that conceal much of the putative major digit. A third alular

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covert is partially visible in cross-section, in the region where the wing is truncated by the

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polished surface of the amber piece. These feathers suggest that the adjacent bones belong to

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the major digit (see Discussion). The major digit bears a sparse coat of diminutive contour

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feathers which have a pale brown colour (Fig. 2E).

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Eight primaries are well preserved, although additional primaries may have existed

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posterior to the preservational window in the amber piece, and fragments of barbs from a

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ninth primary appear to be preserved on the edge of the amber piece (Fig. 2D). The primaries

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exhibit strong vane asymmetry (anterior barbs less than 0.4 times length of adjacent posterior

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barbs), with primaries P6 to P9 exhibiting pointed apices, while more basal feathers appear to

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have blunt apices. Rachises on the primaries are pale, thick, and subcylindrical; they are

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weakly drawn out ventrally, with barbs that are attached near their dorsal margins. Barb rami

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are pale and blade-like in cross sectional view, with barbules attached near the middle of their

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heights (dorsoventrally). Where visible, proximal barbules on the anterior vane of P6 diverge

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from the ramus at ~43° and are gently curved apically, while distal barbules diverge from the

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ramus at ~70°, and are strongly angled adapically within the distal halves of their lengths.

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Due to the thickness of the overlying amber, it is not possible to discern details of the

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pennulum or hooklets on the barbules.

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The primaries are generally preserved with a dark, walnut brown colour, and with pale

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regions along their lengths (Fig. 2B,F). A longitudinal pale area occurs basal to the midlength

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of each feather, extending along the rachis with small protrusions that reach the anterior

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margin of the feather (in all but P9) and approximately one-third of the distance down each

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barb in the posterior vane (Fig. 2B). A more diffuse and transverse pale patch occurs

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subapically on all but P9; the region of reduced pigmentation extends all the way to the

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posterior feather margin. The pale spot is taphonomically exaggerated in P2, where separation

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from the surrounding amber has created a silvery surface (Fig. 2B). The pale patches observed

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in LV-0321 are much more pronounced than the diffuse pale areas observed in the wings of

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DIP-V-15000, DIP-V-15101, DIP-V-15105, the Elektorornis chenguangi specimen HPG-15-2,

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or the hatchling specimen HPG-15-1 (Xing et al., 2016a, 2017, 2019a,b).

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Primary coverts appear to be short and are only represented by a few preserved feather

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apices near the alular coverts—these apices only extend to reach the midlength of the

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anteriormost alular covert. A small region of the ventral plumage is visible where the wing is

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sectioned by the polished surface of the amber piece (Fig. 2C). This area contains a dense mat

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of plumulaceous feathers, and some contours that transition from plumulaceous bases to

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pennaceous apices. Near the manus, the ventral surface of the wing bears a mixture of down

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and contour feathers that lack pigmentation, suggesting that these feathers were either pale or

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white in life.

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4. Taphonomy

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Soft tissue within the wing, as well as the bases of the wing bones, appear to have been

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partially replaced during diagenesis. This has resulted in reduced contrast for X-ray micro-CT

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scanning, partially blurring the distinction between bones and soft tissues, as well as the

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boundaries of the bones themselves (Fig. 1). Where the manus is sectioned by the polished

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surface of the amber piece, the areas that would have contained soft tissues are infilled by a

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grey mass with small amounts of pyrite and carbonized material (Fig. 2C,D). The latter

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components have distinctive optical properties that make them identifiable at high

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magnifications, but it was not possible to confirm their chemical composition through

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destructive sampling of the specimen. SEM observations of material with similar

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preservational characteristics (from other vertebrate samples in the deposit) have indicated

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that this infill is largely composed of clay minerals and pyrite (Xing et al., 2016a), but it was

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not possible to destructively sample LV-0321 to confirm the presence of this material. These

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contents are thought to be sourced from the surrounding matrix, and to fill voids within the

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amber after polymerization has taken place (Grimaldi et al., 2002; Shi et al., 2012).

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Much of the ventral surface of the wing is obscured by a large mass of milky amber that

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formed while the resin was still fluid. This mass has deflected the feathers on the ventral

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surface of the wing (Fig. 2C), and enveloped part of rachidial bases on feathers P6 to P8,

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creating a gap in their rendering data (Fig. 1B). The large amount of milky amber within the

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ventral mass, as well as the small halo of milky amber found around the margin of the wing

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tissues suggest that the wing entered the resin while it was still relatively moist. This

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taphonomic feature has been related to moisture or decay products interacting with resin

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(Martínez-Delclós et al., 2004; Grimaldi and Engel, 2005). The flow ventral to the wing may

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indicate that a larger part of the body was encapsulated in the resin, at least at the beginning

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of the taphonomic process.

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5. Discussion

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Unfortunately, LV-0321 preserves very little skeletal material. Three articulated manual

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elements are preserved but only the distal two phalanges can be unequivocally regarded as

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complete. These two phalanges could represent those of the alular digit, in which case the

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preceding element would be interpreted as the complete alular metacarpal, consistent with its

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length as well as the proportions of the two complete phalanges. Alternatively, the phalanges

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could be regarded as those of the major digit and the element preceding the articulating

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phalanx and ungual would be identified as the incomplete distal portion of the first phalanx.

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This latter interpretation is supported by the insertions of the primary remiges, which are

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preserved extending up to the caudal margin of the first articulated element. Such elongate

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remiges do not attach to the alular digit; the feathers that form the alula are much shorter, and

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can be seen near the base of the preserved wing region in LV-0321 (Fig. 2B,D). Furthermore,

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the absence of elongate remiges along the distal elements of the hand is consistent with

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observations from other bird wings in amber previously collected from the same deposits

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(DIP-V-15100 and DIP-V-15101) as well as by observations from birds belonging to the

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diverse Early Cretaceous Jehol avifauna.

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Superficially, the three preserved elements do strongly resemble the alular digit of many

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enantiornithines and other basal birds. The preserved claw is strongly recurved, and the

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penultimate phalanx appears fairly elongate and delicate. In most Cretaceous birds the alular

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claw is typically larger and more recurved than the major digit ungual, and the penultimate

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phalanx is typically shorter than the first phalanx of the major digit. However, none of these

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morphologies can be confirmed due to the incompleteness of LV-0321. Further complicating

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the assessment here: the major digit claw is largest and strongly recurved, and the penultimate

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phalanx is longer than the first phalanx of the major digit in the enantiornithines Protopteryx

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fengningensis and Longipteryx chaoyangensis, as well as in Sapeornis chaoyangensis, a basal

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pygostylian, all from the Early Cretaceous Jehol avifauna (Zhang and Zhou, 2000; Wang et al.,

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2016). The simple articulation between the proximal element and the penultimate phalanx

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further supports identification of these elements as belonging to the major digit. Based on

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skeletal morphology alone, both interpretations are viable, but the preserved plumage appears

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to indicate the bones belong to the major digit. If the elements are interpreted as representing

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the alular digit, then the preserved feathers have been displaced (which is not supported) and

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potentially the absence of a preserved alula would support identification of this fragmentary

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specimen as belonging to an avian lineage stem-ward of the Enantiornithes; an alula appears

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to be a synapomorphy of Ornithothoraces.

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Size comparisons to previous discoveries in Burmese amber are made difficult by the

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partial nature of LV-0321 (Fig. 3). However, if the apicalmost phalanx (which is

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approximately 4.7 mm long) is considered to be part of the major digit in LV-0321, and the

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total length of its P6 is estimated to be approximately 37 mm long, some basic comparisons

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can be made. The juvenile wing fragments DIP-V-15100 and DIP-V-15101 have distal major

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digit phalanges that are 1.28 and 2.14 mm in length, respectively, and truncated primaries

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(Xing et al., 2016a). The hatchling HPG-15-1 has an apicalmost phalanx that is ~1.33 mm

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long, and truncated primaries, the longest of which is ~27 mm in length (Xing et al., 2017).

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The probable juvenile DIP-V-15102 does not preserve the major digit clearly, and the

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preservation of the primaries is imperfect, but the longest preserved primary is ~24 mm long.

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Where bones are available for comparison, those from LV-0321 are more than twice as long

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as those from previously described specimens, and where feathers are the only evidence

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available, LV-0321 has plumage approximately 1.5 times as long as the next largest specimen

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available. This may suggest that the remains come from an older growth stage, or a

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larger-bodied species than previous specimens. The new specimen was not a large bird by

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today’s standards, but it increases the known size limit of individuals preserved in this deposit,

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although notably this appears to be associated with decreasing completeness. The

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second-largest individual reported from the deposit, DIP-V-15102, measured 6.2 cm from the

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base of the skull to the posterior margin of the pubis. If the difference in feather sizes between

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this specimen and LV-0321 are directly proportional to total body size, the new specimen may

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have come from a bird that was approximately 9.3 cm long: the skull and tail would have

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further added to this length estimate.

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6. Conclusions

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Although LV-0321 is a partial specimen, it is significantly larger than any of the wings

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previously discovered within Burmese amber. This specimen is best interpreted as

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representing the distal remains of the major digit, and is surrounded by a relatively complete

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set of primary flight feathers. If this osteological assessment is correct, scaling the specimen

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based on other enantiornithine remains recovered from the deposit would extend the known

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size of specimens into the range of birds in excess of 10 cm body lengths. The wing feathers

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appear predominantly dark-brown in colour, and have pale transverse and longitudinal

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markings that are more prominent than previously described specimens from the deposit.

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Given the taxonomic and ontogenetic uncertainties that surround LV-0321, it remains unclear

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whether differences in colour patterns are attributable to sampling a new taxon, or a more

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mature specimen.

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Acknowledgements We thank two anonymous reviewers for their improvements to the initial

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manuscript. This research was funded by the National Natural Science Foundation of China

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(No. 41888101, 41790455, 41772008), the Natural Sciences and Engineering Research

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Council of Canada (2015-00681), the National Geographic Society, USA (EC0768-15), and

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"The Foreign Cultural and Educational Experts Employment Program" from Foreign Experts

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Service Division, Ministry of Science and Technology of China (G20190001245).

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Author Contributions All authors designed the project, performed the research, and wrote

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the manuscript.

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Competing Interests The authors declare no competing interests.

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enantiornithine foot and tail feather preserved in Burmese amber. Scientific Reports.

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Zhang, F., Zhou, Z. 2000. A primitive enantiornithine bird and the origin of feathers. Science 290, 1955–1959.

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Figure Captions.

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Fig. 1. X-ray µCT renderings of LV-0321 bones, feather rachises, and decay products.

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(A) Ventral view. (B) Dorsal view. (C) Detail of phalanges and P9 rachis. Abbreviations: P2–

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P9, primary feather numbers; ung, ungual; ph, distal phalanx of alula or major digit; ph/am,

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incomplete proximal phalanx of major digit or alular metacarpal. Scale bars 5 mm in (A,B); 2

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mm in (C).

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Fig. 2. Plumage and taphonomy of LV-0321 dorsal surface.

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(A) Specimen overview. (B) Detail of specimen base and pigment distribution in primaries.

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(C) Detail of truncated base of wing, indicating taphonomy. (D) Illustration of feather

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positions and taphonomic areas. (E) Detail of ungual and plumage surrounding phalanx. (F)

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Dorsal surface of P6, showing pigment distribution and barbule morphology. Abbreviations: );

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dec, decay product mass of milky amber (pale grey in D); min, mineral infill within zone of

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soft tissue (dark grey in D); P1–P9, primary feather numbers; ph/am, transverse section

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through basalmost phalanx or alular metacarpal (white in D); plu, plumulaceous feathers on

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underside of wing (striated in D).

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Fig. 3. Osteological comparison between LV-0321 and previous amber discoveries.

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(A) Specimen LV-0321 major or alular digit, with corresponding manus reconstruction. (B)

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DIP-V-1500 manus, radius and ulna, with corresponding manus reconstruction. (C)

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DIP-V-1501 partial manus, with corresponding manus reconstruction. (D) HPG-15-1 manus,

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radius and ulna, with corresponding manus reconstruction. Grey areas difficult to observe due

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to fractures, bone overlap, or soft tissue obstructions; dashed lines denote uncertain

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boundaries or bone regions truncated by amber polishing. All illustrations share 5 mm scale

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bar. Data for illustrations follow Xing et al. (2016a, 2017). Abbreviations: al, alular

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metacarpal; ma, major metacarpal, II; mi, minor metacarpal, III; p, manual phalanx with

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number in Arabic numerals; ra, radius; ul, ulna; ulr, ulnare.

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Author Contributions All authors designed the project, performed the research, and wrote the manuscript.

Declaration of interests ☒ The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. ☒The authors declare the following financial interests/personal relationships which may be considered as potential competing interests:

Competing Interests The authors declare no competing interests.

(Ryan McKellar, on behalf of all co-authors)