Skip to main content
×
×
Home

Hind limb morphometry of terror birds (Aves, Cariamiformes, Phorusrhacidae): functional implications for substrate preferences and locomotor lifestyle

  • Federico J. Degrange (a1)
Abstract

The hind limbs of birds have long been considered a key feature in the conquest of different environments. However, the high level of morphological diversity encountered complicates the foundation of a good theoretical correlation between morphology, locomotor habits and substrate preference and this, in turn, complicates palaeobiological interpretations. Phorusrhacids (Aves, Cariamiformes) are a good example, since they have been unequivocally categorised as terrestrial birds due to their reduced forelimbs; and as apex predators with the ability to pursue prey based only on their hind limb morphology. Multivariate techniques (PCA and discriminant analysis), based on traditional metrics and geomorphometrics of the hind limb and pelvis, were applied in order to explore terrestriality and cursoriality in phorusrhacids. Although several groups of birds could be identified, when looking solely at hind limb metrics, some phorusrhacids appear to be associated with walking birds, while others are associated with cursorial birds. However, the pelvis separates cursorial birds and phorusrhacids from walking and wading birds. This scenario is complicated further by a lack of clear definition of the different locomotor modes and substrate preferences in extant birds, and this makes it difficult to confirm phorusrhacid cursoriality based solely on morphometrics. However, some qualitative features of the pelvis and foot make the picture a little clearer. To study limb adaptations in fossil birds, a more holistic study, with an emphasis on qualitative features of the whole posterior locomotor module, is necessary, since morphometrics leaves some issues unresolved. A comparison with the wings is also needed, in order to make a more complete analysis of locomotor behaviour.

  • View HTML
    • Send article to Kindle

      To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

      Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

      Find out more about the Kindle Personal Document Service.

      Hind limb morphometry of terror birds (Aves, Cariamiformes, Phorusrhacidae): functional implications for substrate preferences and locomotor lifestyle
      Available formats
      ×
      Send article to Dropbox

      To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

      Hind limb morphometry of terror birds (Aves, Cariamiformes, Phorusrhacidae): functional implications for substrate preferences and locomotor lifestyle
      Available formats
      ×
      Send article to Google Drive

      To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

      Hind limb morphometry of terror birds (Aves, Cariamiformes, Phorusrhacidae): functional implications for substrate preferences and locomotor lifestyle
      Available formats
      ×
Copyright
References
Hide All
Abourachid, A. & Höfling, E. 2012. The legs: a key to bird evolutionary success. Journal of Ornithology 153, 193–98.
Abourachid, A. & Renous, S. 2000. Bipedal locomotion in ratites (Paleognatiform): examples of cursorial birds. Ibis 142, 538–49.
Adams, D. C., Rohlf, F. J. & Slice, D. E. 2004. Geometric morphometrics: ten years of progress following the ‘revolution’. Italian Journal of Zoology 71, 516.
Alexander, R. M. 1998. All-time giants: the largest animals and their problems. Palaeontology 41, 1231–45.
Alexander, R. M. 2004. Bipedal animals and their differences from humans. Journal of Anatomy 204, 321–30.
Alvarenga, H. M. F. & Höfling, E. 2003. Systematic revision of the Phorusrhacidae (Aves: Ralliformes). Papeis Avulsos de Zoologia 43, 5591.
Ameghino, F. 1895. Sobre las aves fósiles de Patagonia. Boletín del Instituto Geográfico de Argentina 15, 501602.
Andrews, C. 1899. On the extinct birds of Patagonia, I, the Skull and skeleton of Phororhacos inflatus Ameghino. Transactions of the Zoological Society of London 15, 5586.
Baumel, J. J., King, A. S., Breazile, J. E., Evans, H. E. & Vanden Berge, J. C. 1993. Handbook of Avian Anatomy: Nomina Anatomica Avium, 2nd Edition. Cambridge, Massachusetts: Nuttall Ornithological Club.
Bertelli, S., Chiappe, L. M. & Tambussi, C. P. 2007. A new phorusrhacid (Aves, Cariamae) from the middle Miocene of Patagonia, Argentina. Journal of Vertebrate Paleontology 27, 409–19.
Blanco, R. E. & Jones, W. W. 2005. Terror birds on the run: A mechanical model to estimate its maximum running speed. Proceedings of the Royal Society B 272, 1769–73.
Bookstein, F. L. 1991. Morphometric tools for landmark data: geometry and biology. New York: Cambridge University Press.
Bookstein, F. L., Chernoff, B., Elder, R. L., Humphries, J. M. Jr., Smith, G. R. & Strauss, R. E. 1985. Morphometrics in evolutionary biology. Philadelphia: Academy of Natural Sciences Press.
Campbell, K. E Jr. & Marcus, L. 1992. The relationship of hindlimb bone dimensions to body weight in birds. Natural History Museum of Los Angeles County, Science Series 36, 395412.
Carrano, M. T. 1997. Morphological indicators of foot posture in mammals: a statistical and biomechanical analysis. Zoological Journal of the Linnean Society 121, 77104.
Carrano, M. T. 1999. What, if anything, is a cursor? Categories versus continua for determining locomotor habit in mammals and dinosaurs. Journal of Zoology, London 247, 2942.
Chiappe, L. M & Bertelli, S. 2006. Skull morphology of giant terror birds. Nature 443, 929.
Collar, J. 1996. Family Otididae (Bustards). In del Hoyo, J., Elliot, A. & Sargatal, J. (eds) Handbook of Birds of the world, Volume 3: Hoatzin to Auks, 240–73. Barcelona: Lynx.
Coombs, W. P. 1978. Theoretical aspects of cursorial adaptations in Dinosaurs. The Quarterly Review of Biology 53, 393418.
Degrange, F. J. 2012. Morfología del cráneo y complejo apendicular en aves fororracoideas: implicancias en la dieta y modo de vidax. Unpublished PhD Thesis, La Plata University, La Plata, Argentina. 390 pp.
Degrange, F. J., Tambussi, C. P., Moreno, K., Witmer, L. W. and Wroe, S. 2010. Mechanical Analysis of Feeding Behavior in the Extinct ‘‘Terror Bird’’ Andalgalornis steulleti (Gruiformes: Phorusrhacidae). PLoS ONE 5, e11856.
Degrange, F. J., Noriega, J. I. & Vizcaíno, S. F. 2015. Morphology of the forelimb of Psilopterus bachmanni (Aves, Cariamiformes) (Early Miocene of Patagonia). Paläontologische Zeitschrift 89, 1087–96.
del Hoyo, J., Elliot, A. & Sargatal, J. 1996. Handbook of Birds of the world, Volume 3: Hoatzin to Auks. Barcelona: Lynx.
Dial, K. P. 2003. Evolution of avian locomotion: correlates of flight style, locomotor modules, nesting biology, body size, development and the origin of flapping flight. The Auk 120, 941–52.
Dunning, J. B. 2008. CRC Handbook of Avian Body Masses. London: Taylor & Francis Group.
Garland, T. Jr. & Janis, C. M. 1993. Does metatarsal/femur ratio predict maximal running speed in cursorial mammals? Journal of Zoology 229, 133–51.
Gatesy, S. M., Bäker, M. & Hutchinson, J. R. 2009. Constraint-based exclusion of limb poses for reconstructing theropod dinosaur locomotion. Journal of Vertebrate Paleontology 29, 535–44.
Gatesy, S. M & Biewener, A. A. 1991. Bipedal locomotion: effects of speed, size and limb posture in birds and humans. Journal of Zoology of London 224, 127–47.
Gatesy, S. M. & Dial, K. P. 1996. Locomotor modules and the evolution of avian flight. Evolution 50, 331–40.
Gatesy, S. M & Middleton, K. M. 1997. Bipedalism, and the evolution of theropod diversity. Journal of Vertebrate Paleontology 17, 308–29.
Gebo, D. L & Rose, K. D. 1993. Skeletal morphology and locomotor adaptation in Prolimnocyon atavus, an early Eocene hyaenodontid creodont. Journal of Vertebrate Paleontology 13, 125–44.
Gonzaga, L. P. 1996. Family Cariamidae (Seriemas). In del Hoyo, J., Elliot, A. & Sargatal, J. (eds) Handbook of Birds of the world, Volume 3: Hoatzin to Auks, 234–39. Barcelona: Lynx.
Gregory, W. K. 1912. Notes on the principles of quadrupedal locomotion and on the mechanism of the limbs in hoofed animals. Annals of the New York Academy of Sciences 22, 267–94.
Habib, M. B. & Ruff, C. B. 2008. The effects of locomotion on the structural characteristics of avian limb bones. Zoological Journal of the Linnean Society 153, 601–24.
Hayes, G. & Alexander, R. McN. 1983. The hopping gaits of crows (Corvidae) and other bipeds. Journal of Zoology 200, 205–13.
Hertel, F. & Campbell, K. E. Jr. 2007. The antitrochanter of birds: form and function in balance. The Auk 124, 789805.
Hinić-Frlog, S. & Motani, R. 2009. Relationship between osteology and aquatic locomotion in birds: determining modes of locomotion in extinct Ornithurae. Journal of Evolutionary Biology 23, 372–85.
Holtz, T. R. 1994. The phylogenetic position of the Tyrannosauridae: implications for theropod systematics. Journal of Paleontology 68, 1100–17.
Hutchinson, J. R. & Gatesy, S. M. 2001. Bipedalism. In Enyclopedia of the Life Sciences, 16. London: Macmillan.
Jones, W. W. 2010. Nuevos aportes sobre la paleobiología de los fororrácidos (Aves: Phorusrhacidae) basados en el análisis de estructuras biológicas. Unpublished PhD Thesis, Universidad de Ciencias, Uruguay. 213 pp.
Klingenberg, C. P. 2011. MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources 11, 353–57.
Kubo, T. & Kubo, M. O. 2012. Associated evolution of bipedality and cursoriality among Triassic archosaurs: a phylogenetically controlled evaluation. Paleobiology 38, 474–85.
Leisch, F., Hornik, K. & Ripley, B. D. 2015. mda: mixture and flexible discriminant analysis. R package version 0.4-8. https://CRAN.R-project.org/package=mda
Middleton, K. M. & Gatesy, S. M. 2000. Theropod forelimb design and evolution. Zoological Journal of the Linnean Society 28, 149–87.
Mourer-Chauviré, C., Tabuce, R., Mahboubi, M., Adaci, M. & Bensalah, M. 2011. A Phororhacoid bird from the Eocene of Africa. Naturwissenschaften 98(10), 815–23.
Osborn, H. F. 1916. Skeletal adaptations of Ornitholestes, Struthiomimus, Tyrannosaurus . Bulletin of the American Museum of Natural History 35, 733–71.
Osborn, H. F. 1929. The Titanotheres of ancient Wyoming, Dakota, and Nebraska. US Geological Survey, Monograph 55, 1953.
Ostrom, J. H. 1976. Archaeopteryx and the origin of birds. Biological Journal of the Linnean Society 8, 91182.
Oxnard, C. 1984. The Order of Man. Hong Kong: Hong Kong University Press.
Paul, G. S. 2002. Dinosaurs of the air: the evolution and loss of flight in dinosaurs and birds. Baltimore: Johns Hopkins Press.
Pennycuick, C. J. 1989. Bird Flight Performance. Oxford: Oxford University Press.
Pennycuick, C. J. 2007. Modelling the flying bird. London: Academic Press.
Peters, R. H. 1983. The ecological implications of Body Size. Cambridge: Cambridge University Press.
Picasso, M. B. J. 2010. The hindlimb muscles of Rhea americana (Aves, Palaeognathae, Rheidae). Anatomia, Histologia, Embryolgia 39, 462–72.
Raikow, R. J. 1985. Locomotor system. In King, A. S. & McLelland, J. (eds) Form and Function in birds, 57147. London: Academic Press.
Rohlf, F. J. 1993. Relative warp analysis and an example of its application to mosquito wings. In Marcus, L. F., Bello, E. & García-Valdecasas, A. (eds) Contributions to Morphometrics, 131–58. Madrid: Museo Nacional de Ciencias Naturales.
Rohlf, F. J. 2003. TpsRelw, version 1.35. Department of Ecology and Evolution, State University of New York, Stony Brook, New York.
Rohlf, F. J. 2005. TpsDig, version 2.04. Department of Ecology and Evolution, State University of New York, Stony Brook, New York.
Rohlf, F. J. & Slice, D. 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39, 4059.
Sereno, P. C, Dutheil, D. B., Iarochene, M., Larsson, H. C. E., Lyon, G. H., Magwene, P. M., Sidor, C. A., Varricchio, D. J. & Wilson, J. A. 1996. Predatory dinosaurs from the Sahara and Late Cretaceous faunal differentiation. Science 272, 986–91.
Sherman, P. T. 1996. Family Psophiidae (Trumpeters). In del Hoyo, J., Elliot, A. & Sargatal, J. (eds) Handbook of Birds of the world, Volume 3: Hoatzin to Auks, 96107. Barcelona: Lynx.
Sinclair, W. & Farr, M. 1932. Aves of the Santa Cruz beds. In Scott, W. (ed.) Reports of the Princeton University expeditions to Patagonia (1896-1899).Volume 7, 157–91. New Jersey: Princeton University.
Smith, J. M. & Savage, R. J. G. 1956. Some locomotory adaptations in mammals. Journal of the Linnean Society (Zoology) 42, 603–22.
Storer, R. W. 1971. Adaptative radiation of birds. In Farner, D. S. & King, J. R. (eds) Avian Biology, 149–88. New York: Academic Press.
Tambussi, C. P. 1997. Algunos aspectos biomecánicos de la locomoción de los fororracos (Aves, Gruiformes). Ameghiniana 34, 541.
Tambussi, C. P., Picasso, M. B. J. & Mosto, M. C. 2010. Graviportalidad en aves sí o no? In Ballent, S., Artabe, A. E. & Tortello, M. F. (eds) Resúmenes del X Congreso Argentino de Paleontología y Bioestratigrafía y VII Congreso Latinoamericano de Paleontología, 214. La Plata, Argentina: Museo de La Plata.
Tambussi, C. P., de Mendoza, R., Degrange, F. J. & Picasso, M. B. J. 2012. Flexibility along the Neck of the Neogene Terror Bird Andalgalornis steulleti (Aves, Phorusrhacidae). PLoS ONE 7, e37701.
Tambussi, C. P. & Noriega, J. I. 1996. Summary of the Avian Fossil Record from Southern South America. In Arratia, G. (ed.) Contributions of the southern south America to vertebrate paleontology, 245–64. München: Müncher Geowissenschaftliche Abhandlungen.
Toledo, N., Bargo, M. S., Cassini, G. H. & Vizcaíno, S. F. 2012. The forelimb of early Miocene Sloths (Mammalia, Xenarthra, Folivora): Morphometrics and functional implications for substrate preferences. Journal of Mammalian Evolution 19, 185–98.
Tonni, E. P. 1977. El rol ecológico de algunas aves fororracoideas. Ameghiniana 14, 316.
Tonni, E. P. & Tambussi, C. P. 1988. Un nuevo Psilopterinae (Aves: Ralliformes) del Mioceno tardío de la provincia de Buenos Aires, República Argentina. Ameghiniana 25, 155–60.
Verstappen, M., Aerts, P. & van Damme, R. 2000. Terrestrial locomotion in the Black-Billed Magpie: kinematic analysis of walking, running and out-of-phase hopping. The Journal of Experimental Biology 203, 2159–70.
Verstappen, M. & Aerts, P. 2000. Terrestrial locomotion in the Black-Billed Magpie. I. Spatiotemporal gait characteristics. Motor Control 4, 150–64.
Vizcaíno, S. F., Bargo, M. S. & Fariña, R. A. 2008. Form, function and paleobiology in xenarthrans. In Vizcaíno, S. F. & Loughry, W. J. (eds). The Biology of the Xenarthra, 8699. Gainesville: University Press of Florida.
Vizcaíno, S. F., Bargo, M. S., Kay, R. F., Fariña, R. A., Di Giacomo, M., Perry, M. G., Prevosti, F. J., Toledo, N., Cassini, G. H. & Fernicola, J. C. 2010. A baseline paleoecological study for the Santa Cruz Formation (late early Miocene) at the Atlantic coast of Patagonia, Argentina. Palaeogeography, Palaeoclimatology, Palaeoecology 292, 507–19.
Zeffer, A., Johansson, L. C. & Marmebro, A. 2003. Functional correlation between habitat use and leg morphology in birds (Aves). Biological Journal of the Linnean Society 79, 461–84.
Zelditch, M. L., Swiderski, D. L., Sheets, H. D. & Fink, W. L. 2004. Geometric Morphometrics for Biologists: A Primer. San Diego: Elsevier Academic Press.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Earth and Environmental Science Transactions of The Royal Society of Edinburgh
  • ISSN: 1755-6910
  • EISSN: 1755-6929
  • URL: /core/journals/earth-and-environmental-science-transactions-of-royal-society-of-edinburgh
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Type Description Title
PDF
Supplementary materials

Degrange supplementary material
Degrange supplementary material 1

 PDF (2.1 MB)
2.1 MB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed