Evolutionary Biology

, Volume 43, Issue 1, pp 12–25 | Cite as

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

  • Zhiheng LiEmail author
  • Julia A. Clarke
Research Article


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.


Anatidae Feeding modes Hyoid Morphometrics 



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.

Compliance with Ethical Standards

Conflict of interest

The authors declare no competing financial interests.

Supplementary material

11692_2015_9345_MOESM1_ESM.xlsx (22 kb)
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)
11692_2015_9345_MOESM2_ESM.docx (13 kb)
Appendix 2 Phylo.tree files used in the three analyses. Selected phylogeny from “” (Jetz et al. 2012), Livezey (1997a, b) and Sorenson et al. (1999). (DOCX 13 kb)
11692_2015_9345_MOESM3_ESM.csv (5 kb)
Appendix 3 Loadings and variance explained by phylogenetic principal component analyses of the phylogenetically size-corrected measurements. (CSV 4 kb)


  1. Baldassarre, G. A., Bolen, E. G., & Sayre, T. R. (2006). Waterfowl ecology and management. Malabar, FL: Krieger.Google Scholar
  2. Batt, B. D. J., Afton, A. D., Anderson, M. G., Ankney, C. D., Johnson, D. H., Kadlec, J. A., et al. (1992). Ecology and management of breeding waterfowl. Minneapolis and London: University of Minnesota Press.Google Scholar
  3. Blackburn, D. C., Siler, C. D., Diesmos, A. C., McGuire, J. A., Cannatella, D. C., & Brown, R. M. (2013). An adaptive radiation of frogs in a Southeast Asian island archipelago. Evolution, 67, 2631–2646.PubMedCentralCrossRefPubMedGoogle Scholar
  4. Carboneras, C. (1992). Anseriformes. In J. Del Hoyo, A. Elliott, & J. Sargatal (Eds.), Handbook of the birds of the world (1st ed., Vol. 1, pp. 527–628). Barcelona: Lynx Edicions.Google Scholar
  5. Diogo, R. (2004). Muscles versus bones: Catfishes as a case study for a discussion on the relative contribution of myological and osteological features in phylogenetic reconstructions. Animal Biology-Leiden, 54, 373–392.CrossRefGoogle Scholar
  6. Donne-Goussé, C., Laudet, V., & Hänni, C. (2002). A molecular phylogeny of anseriformes based on mitochondrial DNA analysis. Molecular Phylogenetics and Evolution, 23, 339–356.CrossRefPubMedGoogle Scholar
  7. Dunning, J. C. (2008). CRC handbook of avian body masses (2nd ed.). Boca Raton: CRC Press.Google Scholar
  8. Durant, D. (2013). The digestion of fibre in herbivorous Anatidae: A review. Wildfowl, 54, 7–24.Google Scholar
  9. Dyreson, E., & Maddison, W. P. (2003). Rhetenor package for morphometrics for the Mesquite system. version 1.0.
  10. Erickson, P. G. P. (1997). Systematic relationships of the palaeogene family Presbyornithidae (Aves: Anseriformes). Zoological Journal of the Linnean Society, 121, 429–483.CrossRefGoogle Scholar
  11. Feduccia, A. (1999). The origin and evolution of birds (2nd ed.). New Haven, CT: Yale Univ Press.Google Scholar
  12. Garland, T, Jr, Harvey, P. H., & Ives, A. R. (1992). Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology, 41, 18–32.CrossRefGoogle Scholar
  13. George, J. C., & Berger, A. J. (1966). Avian myology. New York and London: Academic Press.Google Scholar
  14. Gibbs, S., Collard, M., & Wood, B. (2000). Soft-tissue characters in higher primate phylogenetics. Proceedings of the National Academy of Sciences, 97, 11130–11132.CrossRefGoogle Scholar
  15. Givnish, T. J., Sytsma, K. J., Smith, J. F., & Hahn, W. J. (1994). Thorn-like prickles and heterophylly in Cyanea: Adaptations to extinct avian browsers on Hawaii? Proceedings of the National Academy of Sciences, 91, 2810–2814.CrossRefGoogle Scholar
  16. Gonzalez, J., Düttmann, H., & Wink, M. (2009). Phylogenetic relationships based on two mitochondrial genes and hybridization patterns in Anatidae. Journal of Zoology, 279, 310–318.CrossRefGoogle Scholar
  17. Goodman, D. C., & Fisher, H. I. (1962). Functional anatomy of the feeding apparatus in waterfowl (Aves: Anatidae). Carbondale: Southern Illinois University Press.Google Scholar
  18. Green, A. J. (1992). The status and conservation of the White-winged Wood Duck Cairina scutulata. Special publication no. 17. Slimbridge: IWRB.Google Scholar
  19. Gurd, D. B. (2007). Predicting resource partitioning and community organization of filter-feeding dabbling ducks from functional morphology. The American Naturalist, 169, 334–343.CrossRefPubMedGoogle Scholar
  20. Harvey, P. H., & Pagel, M. (1991). The comparative method in evolutionary biology. New York, Oxford: University Press.Google Scholar
  21. Homberger, D. G., & Meyers, R. A. (1989). Morphology of the lingual apparatus of the domestic chicken, Gallus gallus, with special attention to the structure of the fasciae. American Journal of Anatomy, 186, 217–257.CrossRefPubMedGoogle Scholar
  22. Iwaniuk, A. N., Nelson, J. E., James, H. F., & Olson, S. L. (2004). A comparative test of the correlated evolution of flightlessness and relative brain size in birds. Journal of Zoology, 263, 317–327.CrossRefGoogle Scholar
  23. Iwasaki, S., Tomoichiro, A., & Chiba, A. (1997). Ultrastructureal study of the keratinization of the dorsal epithelium of the tongue of Middendorff’s Bean Goose, Anser fabalis middendorffii (Anseres, Antidae). The Anatomical Record, 247, 149–163.CrossRefPubMedGoogle Scholar
  24. Jackowiak, H., Skieresz-Szewczyk, K., Godynicki, S., Iwasaki, S. I., & Meyer, W. (2011). Functional morphology of the tongue in the domestic goose (Anser anser f. Domestica). The Anatomical Record, 294, 1574–1584.CrossRefPubMedGoogle Scholar
  25. James, H. F., & Burney, D. A. (1997). The diet and ecology of Hawaii’s extinct flightless waterfowl: Evidence from coprolites. Biological Journal of the Linnean Society, 62, 279–297.CrossRefGoogle Scholar
  26. Jeffery, N., Stephenson, R., Gallagher, J., Jarvis, J., & Cox, P. (2011). Micro-computed tomography with iodine staining resolves the arrangement of muscle fibres. Journal of Biomechanics, 44, 189–192.CrossRefPubMedGoogle Scholar
  27. Jetz, W., et al. (2012). The global diversity of birds in space and time. Nature, 491, 444–448.CrossRefPubMedGoogle Scholar
  28. Kear, J. (2005). Ducks, geese and swans: Species accounts (Cairina to Mergus) (Vol. 2). Oxford: University Press.Google Scholar
  29. Kehoe, F. P., & Thomas, V. G. (1987). A comparison of interspecific differences in the morphology of the external and internal feeding apparatus among North American Anatidae. Canadian Journal of Zoology, 65, 1818–1822.CrossRefGoogle Scholar
  30. Köntges, G., & Lumsden, A. (1996). Rhombencephalic neural crest segmentation is preserved throughout craniofacial ontogeny. Development, 122, 3229–3242.PubMedGoogle Scholar
  31. Kooloos, J. G. M., Kraaijeveld, A. R., Langenbach, G. E. J., & Zweers, G. A. (1989). Comparative mechanics of filter feeding in Anas platyrhynchos, Anas clypeata and Aythya fuligula (Aves, Anseriformes). Zoomorphology, 108, 269–290.CrossRefGoogle Scholar
  32. Kooloos, J. G. M., & Zweers, G. A. (1991). Integration of pecking, filter feeding and drinking mechanisms in waterfowl. Acta Biotheoretica, 39, 107–140.CrossRefPubMedGoogle Scholar
  33. Lagerquist, B. A., & Ankney, C. D. (1989). Interspecific differences in bill and tongue morphology among diving ducks (Aythya spp., Oxyura jamaicensis). Canadian Journal of Zoology, 67, 2694–2699.CrossRefGoogle Scholar
  34. Leggitt, V. L., Buchheim, H., & Biaggi, R. E. (1998). The stratigraphic setting of three Presbyornis nesting sites: Eocene Fossil Lake, Lincoln County, Wyoming. National Park Service Paleontological Research, 3, 61–68.Google Scholar
  35. Livezey, B. C. (1997a). A phylogenetic classification of waterfowl, including selected fossil species. Annals of Carnegie Museum, 66, 457–496.Google Scholar
  36. Livezey, B. C. (1997b). A phylogenetic analysis of basal Anseriformes, the fossil Presbyornis, and the interordinal relationships of waterfowl. Zoological Journal of the Linnean Society, 121, 361–428.Google Scholar
  37. Lovvorn, J., Liggins, G. A., Borstad, M. H., Calisal, S. M., & Mikkelsen, J. (2001). Hydrodynamic drag of diving birds: Effects of body size, body shape and feathers at steady speeds. Journal of Experimental Biology, 204, 1547–1557.PubMedGoogle Scholar
  38. Maddison, W. P., & Maddison, D. R. (2011). Mesquite: A modular system for evolutionary analysis. Version, 2, 75.Google Scholar
  39. Metscher, B. D. (2009). MicroCT for comparative morphology: Simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues. BMC Physiology, 9, 11.PubMedCentralCrossRefPubMedGoogle Scholar
  40. Monteiro, L. R. (2013). Morphometrics and the comparative method: Studying the evolution of biological shape. Hystrix, the Italian Journal of Mammalogy, 24, 25–32.Google Scholar
  41. Nudds, T. D., Elmberg, J., Pöysä, H., Sjöberg, K., & Nummi, P. (2000). Ecomorphology in breeding Holarctic dabbling ducks: The importance of lamellar density and body length varies with habitat type. Oikos, 91, 583–588.CrossRefGoogle Scholar
  42. Nummi, P. (1993). Food-niche relationships of sympatric mallards and green-winged teals. Canadian Journal of Zoology, 71, 49–55.CrossRefGoogle Scholar
  43. Olson, S. L., & Feduccia, A. (1980). Presbyornis and the origin of the Anseriformes. Washington, DC: Smithsonian Institution Press.Google Scholar
  44. Olson, S. L., & James, H. E. (1991). Descriptions of 32 new species of Hawaiian birds. Part I. Non-Passeriformes. Ornithological Monograph, 45, 1–88.CrossRefGoogle Scholar
  45. Owen, M., & Black, J. M. (1990). Waterfowl ecology. London: Blackie and Son Ltd.Google Scholar
  46. Polly, P. D., Lawing, A. M., Fabre, A. C., & Goswami, A. (2013). Phylogenetic principal components analysis and geometric morphometrics. Hystrix, the Italian Journal of Mammalogy, 24, 33–41.Google Scholar
  47. Pöysä, H. (1983). Morphology-mediated niche organization in a guild of dabbling ducks. Ornis Scandinavica, 14, 317–326.CrossRefGoogle Scholar
  48. Revell, L. J. (2009). Size-correction and principal components for interspecific comparative studies. Evolution, 63, 3258–3268.CrossRefPubMedGoogle Scholar
  49. Revell, L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217–223.CrossRefGoogle Scholar
  50. Rylander, M. K., & Bolen, E. G. (1974). Feeding adaptations in whistling ducks (Dendrocygna). The Auk, 91, 86–94.CrossRefGoogle Scholar
  51. Sorenson, M. D., Cooper, A., Paxinos, E. E., Quinn, T. W., James, H. F., Olson, S. L., et al. (1999). Relationships of the extinct moa-nalos, flightless Hawaiian waterfowl, based on ancient DNA. Proceedings of the Royal Society of London. Series B: Biological Sciences, 266, 2187–2193.PubMedCentralCrossRefPubMedGoogle Scholar
  52. Suzuki, M., & Nomura, S. (1975). Electromyographic studies on the deglutition movements in the fowl. The Japanese Journal of Veterinary Science, 37, 289–293.CrossRefPubMedGoogle Scholar
  53. Tome, M. W., & Wrubleski, D. A. (1988). Underwater foraging behavior of canvasbacks, lesser scaups, and ruddy ducks. Condor, 90, 168–172.CrossRefGoogle Scholar
  54. Tremblay, S., & Couture, R. (1986). Bucco-lingual morphology of a guild of dabbling ducks. Canadian Journal of Zoology, 64, 2176–2180.CrossRefGoogle Scholar
  55. Van Der Leeuw, A. H. J., Kurk, K., Snelderwaard, P. C., Bout, R. G., & Berkhoudt, H. (2003). Conflicting demands on the trophic system of Anseriformes and their evolutionary implications. Animal Biology-Leiden, 53, 259–301.CrossRefGoogle Scholar
  56. Van Der Meij, M. A. A., & Bout, R. G. (2004). Scaling of jaw muscle size and maximal bite force in finches. Journal of Experimental Biology, 207, 2745–2753.CrossRefPubMedGoogle Scholar
  57. Vanden Berge, J. C., & Zweers, G. A. (1993). Myologia. In J. J. Baumel, A. S. King, J. E. Breazile, H. E. Evans, & J. C. Vanden Berge (Eds.), Handbook of avian anatomy: Nomina anatomica avium (2nd ed., pp. 189–247). Cambridge, MA: Publications of the Nuttall Ornithological Club.Google Scholar
  58. Witmer, L. M. (1995). The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. In J. J. Thomason (Ed.), Functional morphology in vertebrate paleontology (pp. 19–33). New York: Cambridge University Press.Google Scholar
  59. Zelenitsky, D. K., Therrien, F., Ridgely, R. C., McGee, A. R., & Witmer, L. M. (2011). Evolution of olfaction in non-avian theropod dinosaurs and birds. Proceedings of the Royal Society B: Biological Sciences, 278, 3625–3634.PubMedCentralCrossRefPubMedGoogle Scholar
  60. Zweers, G. A. (1974). Structure movement and myography of the feeding apparatus of the Mallard (Anas platyrhynchos L.). Netherlands Journal of Zoology, 24, 323–467.CrossRefGoogle Scholar
  61. Zweers, G. A., Gerritsen, A. F. C., & van Kranenburg-Voogd, P. J. (1977). Mechanics of feeding of the Mallard (Anas platyrhynchos L., Aves, Anseriformes). Contributions to Vertebrate Evolution, 3, 1–109.Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  1. 1.Department of Geological SciencesUniversity of Texas at AustinAustinUSA

Personalised recommendations