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Late Cretaceous bird from Madagascar reveals unique development of beaks

Nature volume 588, pages 272–276 (2020)Cite this article

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Abstract

Mesozoic birds display considerable diversity in size, flight adaptations and feather organization1,2,3,4, but exhibit relatively conserved patterns of beak shape and development5,6,7. Although Neornithine (that is, crown group) birds also exhibit constraint on facial development8,9, they have comparatively diverse beak morphologies associated with a range of feeding and behavioural ecologies, in contrast to Mesozoic birds. Here we describe a crow-sized stem bird, Falcatakely forsterae gen. et sp. nov., from the Late Cretaceous epoch of Madagascar that possesses a long and deep rostrum, an expression of beak morphology that was previously unknown among Mesozoic birds and is superficially similar to that of a variety of crown-group birds (for example, toucans). The rostrum of Falcatakely is composed of an expansive edentulous maxilla and a small tooth-bearing premaxilla. Morphometric analyses of individual bony elements and three-dimensional rostrum shape reveal the development of a neornithine-like facial anatomy despite the retention of a maxilla–premaxilla organization that is similar to that of nonavialan theropods. The patterning and increased height of the rostrum in Falcatakely reveals a degree of developmental lability and increased morphological disparity that was previously unknown in early branching avialans. Expression of this phenotype (and presumed ecology) in a stem bird underscores that consolidation to the neornithine-like, premaxilla-dominated rostrum was not an evolutionary prerequisite for beak enlargement.

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Fig. 1: Cranium of the Cretaceous enantiornithine bird Falcatakely forsterae (UA 10015, holotype).
Fig. 2: Mosaic evolution of the avialan facial skeleton as depicted among select early branching forms.
Fig. 3: Geometric morphometric analyses of the facial shape of Falcatakely among paravians.

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Data availability

UA 10015 is catalogued into the collections at the Université d’Antananarivo. Details regarding the development of the digital files and the derivatives of these files (such as DICOM or PLY) used as part of the study are included in the Supplementary Information and archived on the MorphoSource website (https://www.morphosource.org/Detail/ProjectDetail/Show/project_id/7894). Phylogenetic character information and parameters used in the analyses are provided in the Supplementary Information. Executable files for phylogenetic analyses, character–taxon matrices, an interactive three-dimensional morphospace plot and interactive three-dimensional PDFs are hosted on DRYAD (https://doi.org/10.5061/dryad.mkkwh70wg). This published study, including the novel genus (urn:lsid:zoobank.org:act:5BA26059-B428-4896-BFEA-2475419C61FC) and species (urn:lsid:zoobank.org:act:69314771-F0D8-4C15-946C-524164385FB7) along with the associated nomenclatural acts, have been registered in ZooBank: urn:lsid:zoobank.org:pub:4595D69E-FE12-4DAD-B155-89F084254F73.

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Acknowledgements

We thank the Université d’Antananarivo, the Mahajanga Basin Project field teams and the villagers of the Berivotra Study Area for support; the ministries of Mines, Higher Education and Culture of the Republic of Madagascar for permission to conduct field research; the National Geographic Society (8597-09) and the US National Science Foundation (EAR–0446488, EAR–1525915, EAR–1664432) for funding; and M. Witton for drafting the line drawings used in Fig. 1 and Extended Data Figs. 1, 2. Collection of avian three-dimensional morphometric data was funded by European Research Council grant no. STG-2014-637171 (to A. Goswami). Full acknowledgments are provided in the Supplementary Information.

Author information

Authors and Affiliations

  1. Department of Biomedical Sciences, Heritage College of Osteopathic Medicine, Ohio University, Athens, OH, USA

    Patrick M. O’Connor & Joseph R. Groenke

  2. Ohio Center for Ecological and Evolutionary Studies, Ohio University, Athens, OH, USA

    Patrick M. O’Connor

  3. Department of Earth Sciences, Denver Museum of Nature & Science, Denver, CO, USA

    Patrick M. O’Connor, Raymond R. Rogers & David W. Krause

  4. Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY, USA

    Alan H. Turner & David W. Krause

  5. Centre for Integrative Anatomy, Department of Cell and Developmental Biology, University College London, London, UK

    Ryan N. Felice

  6. Geology Department, Macalester College, St Paul, MN, USA

    Raymond R. Rogers

  7. Département de Sciences de la Terre et de l’Environnement, Université d’Antananarivo, Antananarivo, Madagascar

    Lydia J. Rahantarisoa

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Contributions

P.M.O., A.H.T. and J.R.G. designed the project; P.M.O., A.H.T., J.R.G., R.R.R., D.W.K. and L.J.R. conducted the fieldwork. J.R.G. performed the mechanical preparation of the specimen; J.R.G. and P.M.O. conducted the digital preparation and interpretation of the specimen using microcomputed tomography and carried out the rapid prototyping of UA 10015; R.R.R. and L.J.R. provided geological data and taphonomic interpretation; P.M.O., A.H.T., J.R.G. and R.N.F. completed the laboratory work on and digital representation of the fossil and provided input on descriptions and comparisons; A.H.T. and P.M.O. contributed to the character coding and phylogenetic analysis; R.N.F. completed the morphometric analyses; P.M.O., A.H.T. and J.R.G. developed the manuscript, with contributions and/or editing from all authors.

Corresponding author

Correspondence to Patrick M. O’Connor.

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The authors declare no competing interests.

Additional information

Peer review information Nature thanks Bhart-Anjan Bhullar and Daniel Field for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data figures and tables

Extended Data Fig. 1 Rostrum of the Cretaceous enantiornithine bird Falcatakely (UA 10015, holotype).

a, Reconstruction (not to scale) illustrating the preserved (in white) elements of the cranium. b, Digital polygon surface reconstruction (from microcomputed tomography scans) of the right nasal in rostrodorsal view (caudal to the top) highlighting the midline depression and dimpled surface texture. c, Digital polygon surface reconstruction of the right nasal in dorsal view illustrating the dimpled architecture on the frontal and rostral portions, which extends laterally onto the lacrimal. d, Digital polygon surface reconstruction of the right facial elements in right lateral view to illustrate the shape and inter-element relationships of the nasal, maxilla and lacrimal (note the surface texture of the right maxilla with neurovascular sulci broadly expressed over the lateral surface, deep to the inferred keratinous covering (that is, beak)). e, Digital polygon surface reconstruction of the lower lateral face to highlight arrangement of the maxilla, lacrimal, jugal and postorbital (all elements from the right side). f, Digital polygon surface reconstruction of left maxilla and premaxilla articulation (rostral to the left). AOF, antorbital fenestra; cdp, caudodorsal process of the lacrimal; cp, choanal process of the palatine; ect, ectopterygoid; EN, external nares; ITF, infratemporal fenestra; fpn, frontal process of the nasal; inb, internarial bar; jpmx, jugal process of the maxilla; ju, jugal; lbo, lacrimal boot; lc, lacrimal; ld, lacrimal dimpling; le, lacrimal excavation; lf, lacrimal foramen; mpmx, midline premaxilla; mx, maxilla; mxpj, maxillary process of the jugal; na, nasal; nd, nasal dimpling; nf, nasal fossa; nvs, neurovascular sulci; pal, palatine; pmpm, premaxillary process of the maxilla; pmx, premaxilla; po, postorbital; qj, quadratojugal; rdp, rostrodorsal process of the lacrimal; rpn, rostral process of the nasal; tm, tomial margin; to, tooth; vr, ventral ramus of the lacrimal.

Extended Data Fig. 2 Palatal and lateral facial regions of the Cretaceous enantiornithine bird Falcatakely (UA 10015, holotype).

a, Digital polygon surface reconstruction (from microcomputed tomography scans) of the palate and lateral face in ventral view. b, Reconstructed outline drawing of Falcatakely in palatal view (shaded regions are not preserved). c, Digital polygon surface reconstruction of internal aspect of left facial skeleton (premaxilla, maxilla and nasal) and palate in right lateral view. The left and right sides are indicated as (l) and (r), respectively. The dashed line in c represents the approximate contour of the caudal margin (that is, the ventral ramus of the lacrimal) of the antorbital fenestra. Scale bar, 5 mm; the scale bar is representative for a and c; the reconstruction in b is not to the same scale. AOF, antorbital fenestra; bs, basisphenoid rostrum; cp, choanal process of the (right) palatine; ect, ectopterygoid; EN, external nares; jpmx, jugal process of the maxilla; mpmx, midline premaxilla; mx, maxilla; na, nasal; pal, palatine; pmx, premaxilla; pter, pterygoid; to, tooth; up, uncinate process of the ectopterygoid; vm, vomers.

Extended Data Fig. 3 Majority- rule tree of Falcatakely among coelurosaurians from the Bayesian analysis of the TWiG matrix.

Clades outside of the Avialae are collapsed for brevity. Posterior probabilities are placed above the nodes.

Extended Data Fig. 4 Majority -rule tree of Falcatakely among avialans from the Bayesian analysis of a modified matrix that was previously published.

A matrix modified from a previous study25 was used. Posterior probabilities are placed above the nodes.

Extended Data Fig. 5 Geometric morphometric analysis of rostrum shape in Falcatakely among avians.

Plot of the first two principal components of the three-dimensional landmark analysis of total rostrum shape of Falcatakely and extant avian taxa. Whereas the unique configuration of the maxilla and premaxilla in Falcatakely is more similar to those of non-avialan paravians (Fig. 3), the overall three-dimensional rostrum phenotype occupies the morphospace that is converged on by subsequent radiations of neornithine birds (Supplementary Data). See Supplementary Information for analytical protocols.

Extended Data Fig. 6 Landmarking procedure for three-dimensional geometric morphometric analysis in dorsal and lateral views.

a, Dorsal view. b, Lateral view. Red spheres represent anatomical (type I) landmarks; yellow spheres are sliding semi-landmarks.

Supplementary information

Supplementary Information

This file includes details related to the provenance of the specimens, preparation (mechanical and digital) of the specimen, and the parameters of both the geometric morphometric and phylogenetic analyses undertaken for the publication. Location:NPG website and DRYAD.

Reporting Summary

Supplementary Data

An interactive morphopace plot of Falcatakely forsterae and extant avian taxa (HTML format). Also available at https://doi.org/10.5061/dryad.mkkwh70wg.

Video 1

Polygon surface model reconstruction (from CT data) of Falcatakely forsterae, as preserved, with rotation around a dorsoventral axis (relative to left maxilla). Location: NPG Website and DRYAD.

Video 2

Polygon surface model reconstruction (from CT data) of Falcatakely forsterae, Beauchêne-style, with rotation around a dorsoventral axis axis (relative to left maxilla). Location: NPG Website and DRYAD.

Video 3

Polygon surface model reconstruction (from CT data) of Falcatakely forsterae, as preserved, with rotation around a mediolateral axis (relative to left maxilla). Location: NPG Website and DRYAD.

Video 4

Polygon surface model reconstruction (from CT data) of Falcatakely forsterae, Beauchêne-style, with rotation around a mediolateral axis (relative to left maxilla). Location: NPG Website and DRYAD.

Video 5

Polygon surface model reconstruction (from CT data) of Falcatakely forsterae, as preserved, with rotation around a rostrocaudal axis (relative to left maxilla). Location: NPG Website and DRYAD.

Video 6

Polygon surface model reconstruction (from CT data) of Falcatakely forsterae, Beauchêne-style, with rotation around a rostrocaudal axis (relative to left maxilla). Location: NPG Website and DRYAD.

Video 7

Animation of in-situ to Beauchêne-style state changes in polygon reconstructions (relative to left maxilla). Location: NPG Website and DRYAD.

Video 8

Montage highlighting stages of data recovery used for study of Falcatakely forsterae. Location: NPG Website and DRYAD.

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O’Connor, P.M., Turner, A.H., Groenke, J.R. et al. Late Cretaceous bird from Madagascar reveals unique development of beaks. Nature 588, 272–276 (2020). https://doi.org/10.1038/s41586-020-2945-x

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