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The Craniolingual Morphology of Waterfowl (Aves, Anseriformes) and Its Relationship with Feeding Mode Revealed Through Contrast-Enhanced X-Ray Computed Tomography and 2D Morphometrics

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Abstract

Within Anseriformes, waterfowl (ducks, geese, and swans) exhibit three specialized feeding modes that are distinctive among Aves: filter-feeding with fine and dense keratinous lamellae on a flat, mediolaterally expanded bill; cropping or grazing vegetation with large and robust lamellae with a dorsoventrally expanded bill; and sharp lamellae associated with a narrow bill used in acquiring mixed invertebrates and fish underwater mainly by grasping. Here we assess morphometric variation in cranial and hyolingual structures as well as hyolingual myology in a diverse sample of Anatidae to explore the relationship of tongue variation and feeding mode. Phylogenetically informed principal component analysis (phyl.PCA) of cranial-lingual measurements for 67 extant and two extinct anatids recovers grazers and filter-feeding taxa in largely distinct areas of morphospace, while underwater graspers and other mixed feeders show less distinct clustering. The relationship between morphometric differences in skeletal features and muscular variation was further explored through a reassessment of hyolingual musculature enabled by contrast-enhanced X-ray computed tomography (CT) imagery acquired from three exemplar species (Branta canadensis, Chen caerulescens, and Aythya americana) with distinctive ecologies and morphologies of the bony hyoid. Data for these duck and geese exemplars reveal further significant, and previously unstudied, morphological differences between filter-feeding and grazing species. Grazers have a larger hyolingual apparatus with highly-developed extrinsic hyoid muscles; while filter-feeding species are characterized by relatively more diminutive extrinsic hyoid muscles and larger intrinsic hyoid muscles. The feeding modes of two extinct taxa (i.e., Presbyornis and Thambetochen) were also estimated from morphometric data. The results indicate a derived terrestrial browsing or grazing ecology for Thambetochen but do not unequivocally support a specialized filter-feeding ecology for Presbyornis, which is recovered with mixed feeders including swans. The combination of detailed, CT-mediated acquisition of fine muscular anatomy with morphometric approaches shows promise for illuminating form–function relationships in extant taxa more generally.

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Acknowledgments

We are grateful to H. James and C. Milensky for hosting the author (Z.L.) during his visits to the Smithsonian Institution (NMNH); we are also grateful to H. James, C. Milensky and P. Sweet in accessing skeletal specimens in NMNH and AMNH. We thank E. Theriot (Texas Memorial Museum) for assistance with the acquisition of key extant specimens. We are grateful to C. Sagebiel and K. Bader for accessing specimens in TMM Collections at The University of Texas Vertebrate Paleontology Laboratory, and T. LaDuc for using Laboratory space of Texas Natural History Collections (TNHC) for specimen processing. We are grateful to M. Colbert for acquiring excellent CT scans of these specimens; X. Wang, R. Rong and J. Mitchell for their discussion and comments. This research was funded by the Jackson School of Geosciences at the University of Texas at Austin (J.A.C.) as well as a Predoctoral Fellowship from the Smithsonian Institution to Z. Li.

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  1. Department of Geological Sciences, University of Texas at Austin, Austin, TX, USA

    Zhiheng Li & Julia A. Clarke

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  1. Zhiheng Li
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Correspondence to Zhiheng Li.

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Appendix 1

Skeletal measurements of the hyoid apparatus and skull, feeding types and body mass data used in the phylogenetically informed principle component analysis. (XLSX 21 kb)

Appendix 2

Phylo.tree files used in the three analyses. Selected phylogeny from “Birdtree.org” (Jetz et al. 2012), Livezey (1997a, b) and Sorenson et al. (1999). (DOCX 13 kb)

Appendix 3

Loadings and variance explained by phylogenetic principal component analyses of the phylogenetically size-corrected measurements. (CSV 4 kb)

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Li, Z., Clarke, J.A. The Craniolingual Morphology of Waterfowl (Aves, Anseriformes) and Its Relationship with Feeding Mode Revealed Through Contrast-Enhanced X-Ray Computed Tomography and 2D Morphometrics. Evol Biol 43, 12–25 (2016). https://doi.org/10.1007/s11692-015-9345-4

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