, Volume 101, Issue 5, pp 447–452 | Cite as

Insight into the growth dynamics and systematic affinities of the Late Cretaceous Gargantuavis from bone microstructure

  • Anusuya Chinsamy
  • Eric Buffetaut
  • Aurore Canoville
  • Delphine Angst
Short Communication


Enigmatic avialan remains of Gargantuavis philoinos from the Ibero-Armorican island of the Late Cretaceous European archipelago (Southern France) led to a debate concerning its taxonomic affinities. Here, we show that the bone microstructure of Gargantuavis resembles that of Apteryx, the extinct emeids and Megalapteryx from New Zealand, and indicates that like these slow-growing terrestrial birds, it took several years to attain skeletal maturity. Our findings suggest that the protracted cyclical growth in these ornithurines may have been in response to insular evolution.


Bone histology Bone microstructure Avialans Gargantuavis Growth dynamics 



Samuel Turvey is thanked for the image of Megalapteryx. Jean Le Loeuff granted permission to sample specimen MDE-A08. The National Research Foundation (South Africa) and the Claude Leon Foundation (South Africa) are acknowledged for funding support to Chinsamy and Canoville, respectively. This work was partly supported by the Interrvie programme of CNRS. Finally, Michel Laurin, Lorna Steel and an anonymous referee are thanked for comments that have improved this article.


  1. Amprino R, Godina G (1947) La struttura delle ossa nei vertebrati. Pontifica Acad Sci 9:329–463Google Scholar
  2. Bourdon E, Castanet J, Ricqlès A de, Scofield P, Tennyson A, Lamrous H, Cubo J (2009) Bone growth marks reveal protracted growth in New Zealand kiwi (Aves, Apterygidae). Biol Lett 5:639–642Google Scholar
  3. Buffetaut E, Angst D (2013) New evidence of a giant bird from the Late Cretaceous of France. Geol Mag 150:173–176CrossRefGoogle Scholar
  4. Buffetaut E, Le Loeuff J (1998) A new giant ground bird from the Upper Cretaceous of southern France. J Geol Soc Lond 155:1–4CrossRefGoogle Scholar
  5. Buffetaut E, Le Loeuff J (2010) Gargantuavis philoinos: giant bird or giant pterosaur? Ann Paléontol 96:135–141CrossRefGoogle Scholar
  6. Buffetaut E, Le Loeuff J, Mechin P, Mechin-Salessy A (1995) A large French Cretaceous bird. Nature 377:110CrossRefGoogle Scholar
  7. Bunce M, Worthy TH, Phillips MJ, Holdaway RN, Willersley E, Haile J, Shapiro B, Scofield RP, Drummond A, Kamp PJJ, Cooper A (2009) The evolutionary history of the extinct ratite moa and New Zealand Neogene paleogeography. Proc Natl Acad Sci U S A 106:20646–20651PubMedCentralPubMedCrossRefGoogle Scholar
  8. Canoville A, Laurin M (2010) Evolution of humeral microanatomy and lifestyle in amniotes, and some comments on paleobiological inferences. Biol J Linn Soc 100:384–406CrossRefGoogle Scholar
  9. Castanet J, Smirina E (1990) Introduction to the skeletochronological method in amphibians and reptiles. Ann Sci Nat 11:191–196Google Scholar
  10. Castanet J, Francillon-Vieillot H, Meunier FJ, De Ricqles A (1993) Bone and individual aging. Bone: Bone Growth B 7:245Google Scholar
  11. Chinsamy A (1995) Histological perspectives on growth in the birds Struthio camelus and Sagittarius serpentarius. Cour Forschungsinstitut Senckenberg 181:317–323Google Scholar
  12. Chinsamy A, Raath MA (1992) Preparation of fossil bone for histological examination. Palaeontol Afr 29:39–44Google Scholar
  13. Chinsamy A (1990) Physiological implications of the bone histology of Syntarsus rhodesiensis (Saurischia: Theropoda). Palaeontol Afr 27:77–82Google Scholar
  14. Chinsamy-Turan A (2005) The microstructure of dinosaur bones: deciphering biology through fine scale techniques. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  15. Chinsamy-Turan A (2012) The forerunners of mammals: radiation, histology, biology. Indiana University Press, BloomingtonGoogle Scholar
  16. Chinsamy A, Chiappe L, Dodson P (1994) Growth rings in Mesozoic avian bones: physiological implications for basal birds. Nature 368:196–197Google Scholar
  17. Chinsamy A, Codorniu L, Chiappe L (2009) Palaeobiological implications of the bone histology of Pterodaustro guinazui. Anat Rec 292:1462–1477Google Scholar
  18. Cojan I, Moreau MG (2006) Correlation of terrestrial climatic fluctuations with global signals during the Upper Cretaceous-Danian in a compressive setting (Provence, France). J Sed Res 76:589–604CrossRefGoogle Scholar
  19. Enlow DH, Brown SO (1958) A comparative histological study of fossil and recent bone tissues. Part III. Texas J Sci 10:187–230Google Scholar
  20. Erickson GM (2005) Assessing dinosaur growth patterns: a microscopic revolution. Trends Ecol Evol 20:677–684PubMedCrossRefGoogle Scholar
  21. Erickson GM, Rauhut OWM, Zhou Z, Turner AH, Inouye BD, Hu D, Norell MA (2009) Was dinosaurian physiology inherited by birds? Reconciling slow growth in Archaeopteryx. PLoS One 4:e7390PubMedCentralPubMedCrossRefGoogle Scholar
  22. Erismis UC, Chinsamy-Turan A (2010) Ontogenetic changes in the epiphyseal cartilage of Rana (Pelophylax) caralitana (Anura: Ranidae). Anat Rec 293:1825–1837CrossRefGoogle Scholar
  23. Klein N, Sander PM, Stein K, Le Loeuff J, Carballido JL, Buffetaut E (2012) Modified laminar bone in Ampelosaurus atacis and other titanosaurs (Sauropoda): Implications for life history and physiology. PLoS One 7(5): e36907. doi: 10.1371/journal.pone.0036907
  24. Köhler M, Moyà-Solà S (2009) Physiological and life history strategies of a fossil large mammal in a resource-limited environment. Proc Natl Acad Sci 106:20354–20358PubMedCentralPubMedCrossRefGoogle Scholar
  25. Köhler M, Marín-Moratalla N, Jordana X, Aanes R (2012) Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature 487:358–361PubMedCrossRefGoogle Scholar
  26. Legendre L, Le Roy N, Martinez-Maza C, Montes L, Laurin M, Cubo J (2013) Phylogenetic signal in bone histology of amniotes revisited. Zool Scr 42:44–53CrossRefGoogle Scholar
  27. Le Loeuff J (1995) Ampelosaurus atacis (nov. gen., nov. sp.), a new titanosaurid (Dinosauria, Sauropoda) from the Late Cretaceous of the Upper Aude Valley (France). CR Acad Sci Ser II 321:693–700Google Scholar
  28. Mayr G (2009) Paleogene fossil birds. Springer, BerlinCrossRefGoogle Scholar
  29. Padian K, Horner JR, Ricqlès A de (2004) Growth in small dinosaurs and pterosaurs: the evolution of archosaurian growth strategies. J Vertebr Paleontol 24:555–571Google Scholar
  30. Pereda-Suberbiola X (2009) Biogeographical affinities of Late Cretaceous continental tetrapods of Europe: a review. Bull Soc Geol Fr 180:57–71CrossRefGoogle Scholar
  31. Reid REH (1990) Zonal ‘growth rings’ in dinosaurs. Mod Geol 15:19–48Google Scholar
  32. Ricqlès A de, Meunier FJ, Castanet J, Francillon-Vieillot H (1991) Comparative microstructure of bone. In: Hall BK (ed) Bone. CRC, Boca Raton, pp 1–78Google Scholar
  33. Ricqlès A de, Padian K, Horner JR, Franchillon-Vieillot H (2000) Paleohistology of the bones of pterosaurs (Reptilia: Archosauria): anatomy, ontogeny, and biomechanical implications. Zool J Linnean Soc 129:349–385Google Scholar
  34. Starck JM, Chinsamy A (2002) Bone microstructure and developmental plasticity in birds and other dinosaurs. J Morphol 254:232–246PubMedCrossRefGoogle Scholar
  35. Steel L (2008) The palaeohistology of pterosaur bones: an overview. Zitteliana B28:109–125Google Scholar
  36. Steel L (2009) Bone Histology and skeletal pathology of two recently extinct flightless pigeons: Raphus cucullatus and Pezophaps solitaria. J Vertebr Paleontol 29(3):185AGoogle Scholar
  37. Stein K, Sander PM (2009) Histological core drilling: a less destructive method for studying bone histology. Lithodendron: The Occasional Papers of Petrified Forest National Park 1. Methods. In: Brown MA, Kane JF, Parker WG (ed) Fossil preparation: Proceedings of the First Annual Fossil Preparation and Collections Symposium, pp 69–80Google Scholar
  38. Turvey ST, Green OR, Holdaway RN (2005) Cortical growth marks reveal extended juvenile development in New Zealand moa. Nature 435:941–943CrossRefGoogle Scholar
  39. Varricchio DJ (1993) Bone microstructure of the Upper Cretaceous theropod dinosaur Troodon formosus. J Vertebr Paleontol 13:99–104CrossRefGoogle Scholar
  40. Worthy TH, Holdaway RN (2002) The lost world of the moa. Indiana University Press, BloomingtonGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Anusuya Chinsamy
    • 1
  • Eric Buffetaut
    • 2
  • Aurore Canoville
    • 1
  • Delphine Angst
    • 3
  1. 1.Department of Biological SciencesUniversity of Cape TownCape TownSouth Africa
  2. 2.Laboratoire de Géologie de l’Ecole Normale SupérieureCNRS (UMR 8538)Paris Cedex 05France
  3. 3.Laboratoire de Géologie de Lyon (UMR5276)Université Claude Bernard—Lyon 1Villeurbanne CedexFrance

Personalised recommendations