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Cortical growth marks reveal extended juvenile development in New Zealand moa

Abstract

Cyclical growth marks in cortical bone, deposited before attainment of adult body size, reflect osteogenetic changes caused by annual rhythms and are a general phenomenon in non-avian ectothermic and endothermic tetrapods1. However, the growth periods of ornithurines (the theropod group including all modern birds) are usually apomorphically shortened to less than a year2,3, so annual growth marks are almost unknown in this group4,5,6. Here we show that cortical growth marks are frequent in long bones of New Zealand's moa (Aves: Dinornithiformes), a recently extinct ratite order. Moa showed the exaggerated K-selected life-history strategy formerly common in the New Zealand avifauna, and in some instances took almost a decade to attain skeletal maturity. This indicates that reproductive maturity in moa was extremely delayed relative to all extant birds. The two presently recognized moa families (Dinornithidae and Emeidae) also showed different postnatal growth rates, which were associated with their relative differences in body size. Both species of giant Dinornis moa attained their massive stature (up to 240 kg live mass) by accelerating their juvenile growth rate compared to the smaller emeid moa species, rather than by extending the skeletal growth period.

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Figure 1: Reconstructions of dinornithid and emeid moa species. A 1.8-m tall person is used as a scale.
Figure 2: Transverse undemineralized diaphyseal thin sections through moa long bones.
Figure 3: Ratite phylogeny and histology.

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References

  1. Hall, B. K. (ed.) Bone Vol. 7 (CRC Press, Boca Raton, 1993)

  2. Padian, K., de Ricqlès, A. & Horner, J. R. Dinosaurian growth rates and bird origins. Nature 412, 405–408 (2001)

    Article  ADS  CAS  Google Scholar 

  3. Davies, S. J. J. F. Ratites and Tinamous (Oxford Univ. Press, Oxford, 2002)

    Google Scholar 

  4. Chinsamy, A. in Mesozoic Birds. Above the Heads of Dinosaurs (eds Chiappe, L. M. & Witmer, L. M.) 421–431 (Univ. of California Press, Berkeley, 2002)

    Google Scholar 

  5. de Ricqlès, A., Padian, K. & Horner, J. R. in New Perspectives on the Origin and Early Evolution of Birds. Proceedings of the International Symposium in Honor of John H. Ostrom (eds Gauthier, J. & Gall, L. F.) 411–426 (Peabody Museum of Natural History, Yale Univ., New Haven, 2001)

    Google Scholar 

  6. Starck, J. M. & Chinsamy, A. Bone microstructure and developmental plasticity in birds and other dinosaurs. J. Morphol. 254, 232–246 (2002)

    Article  Google Scholar 

  7. de Margerie, E. et al. Assessing a relationship between bone microstructure and growth rate: a fluorescent labelling study in the king penguin chick (Aptenodytes patagonicus). J. Exp. Biol. 207, 869–879 (2004)

    Article  CAS  Google Scholar 

  8. Enlow, D. H. & Brown, S. O. A comparative histological study of fossil and recent bone tissues. Part II. Tex. J. Sci. 9, 186–214 (1957)

    Google Scholar 

  9. Houde, P. Histological evidence for the systematic position of Hesperornis (Odontornithes: Hesperornithiformes). Auk 104, 125–129 (1987)

    Article  Google Scholar 

  10. Klomp, N. I. & Furness, R. W. A technique which may allow accurate determination of the age of adult birds. Ibis 134, 245–249 (1992)

    Article  Google Scholar 

  11. Broughton, J. M., Rampton, D. & Holanda, K. A test of an osteologically based age determination technique in the double-crested cormorant Phalacrocorax auritus. Ibis 144, 143–146 (2002)

    Article  Google Scholar 

  12. Holdaway, R. N. & Jacomb, C. Rapid extinction of the moas (Aves: Dinornithiformes): model, test and implications. Science 287, 2250–2254 (2000)

    Article  ADS  CAS  Google Scholar 

  13. Lydekker, R. Catalogue of the Fossil Birds in the British Museum (Natural History) (British Museum (Nat. Hist.), London, 1891)

    Google Scholar 

  14. Bunce, M. et al. Extreme reversed sexual size dimorphism in the extinct New Zealand moa Dinornis. Nature 425, 172–175 (2003)

    Article  ADS  CAS  Google Scholar 

  15. Huynen, L., Millar, C. D., Scofield, R. P. & Lambert, D. M. Nuclear DNA sequences detect species limits in ancient moa. Nature 425, 175–178 (2003)

    Article  ADS  CAS  Google Scholar 

  16. Worthy, T. H. & Holdaway, R. N. The Lost World of the Moa (Indiana Univ. Press, Bloomington, 2002)

    Google Scholar 

  17. Chinsamy, A. Histological perspectives on growth in the birds Struthio camelus and Sagittarius serpentarius. Courier Forsch.-Inst. Senckenberg 181, 317–323 (1995)

    Google Scholar 

  18. Chinsamy, A., Rich, T. & Vickers-Rich, P. Polar dinosaur bone histology. J. Vert. Paleontol. 18, 385–390 (1998)

    Article  Google Scholar 

  19. Castanet, J., Curry Rogers, K., Cubo, J. & Boisard, J.-J. Periosteal bone growth rates in extant ratites (ostriche and emu). Implications for assessing growth in dinosaurs. Comptes Rendus Acad. Sci. Paris, Sciences de la vie 323, 543–550 (2000)

    ADS  CAS  Google Scholar 

  20. Castanet, J., Grandin, A., Abourachid, A. & de Ricqlès, A. Expression de la dynamique de croissance dans la structure de l'os périostique chez Anas platyrhynchos. Comptes Rendus Acad. Sci. Paris, Sciences de la vie 319, 301–308 (1996)

    CAS  Google Scholar 

  21. Amprino, R. La structure du tissue osseux envisage comme expression de differences dans la vitesse de l'accroissement. Arch. Biol. (Paris) 58, 315–330 (1947)

    Google Scholar 

  22. Padian, K., Horner, J. R. & de Ricqlès, A. Growth in small dinosaurs and pterosaurs: the evolution of archosaurian growth strategies. J. Vert. Paleontol. 24, 555–571 (2004)

    Article  Google Scholar 

  23. Erickson, G. M. et al. Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430, 772–775 (2004)

    Article  ADS  CAS  Google Scholar 

  24. Sander, P. M. et al. Adaptive radiation in sauropod dinosaurs: bone histology indicates rapid evolution of giant body size through acceleration. Org. Div. Evol. 4, 165–173 (2004)

    Article  Google Scholar 

  25. Cracraft, J. Phylogeny and evolution of the ratite birds. Ibis 116, 494–521 (1974)

    Article  Google Scholar 

  26. Cooper, A. et al. Complete mitochondrial genome sequences of two extinct moas clarify ratite evolution. Nature 409, 704–707 (2001)

    Article  ADS  CAS  Google Scholar 

  27. Bennett, P. M. & Owens, I. P. F. Evolutionary Ecology of Birds (Oxford Univ. Press, Oxford, 2002)

    Google Scholar 

  28. Owens, I. P. F. & Bennett, P. M. Ecological basis of extinction risk in birds: habitat loss versus human persecution and introduced predators. Proc. Natl Acad. Sci. USA 97, 12144–12148 (2000)

    Article  ADS  CAS  Google Scholar 

  29. Johnson, C. N. Determinants of loss of mammal species during the Late Quaternary ‘megafauna’ extinctions: life history and ecology, but not body size. Proc. R. Soc. Lond. B 269, 2221–2227 (2002)

    Article  CAS  Google Scholar 

  30. Horner, J. R., de Ricqlès, A. & Padian, K. Variation in dinosaur skeletochronology indicators: implications for age assessment and physiology. Paleobiology 25, 295–304 (1999)

    Article  Google Scholar 

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Acknowledgements

We are grateful to R. P. Scofield, H. A. Schlumpf, N. Carson, A. J. D. Tennyson, J. A. Bartle, M. Bunce, T. H. Worthy, L. J. Shorey, T. Robinson, R. Spiers, M. Giesen, S. Veldhuizen, A. Chinsamy-Turan, J. Horner, P. Houde and K. Padian. Funding was provided by a Banks Alecto postdoctoral fellowship from the Royal Society of London (S.T.T.) and the New Zealand Foundation for Research, Science and Technology (R.N.H.).

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Correspondence to Samuel T. Turvey.

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Turvey, S., Green, O. & Holdaway, R. Cortical growth marks reveal extended juvenile development in New Zealand moa. Nature 435, 940–943 (2005). https://doi.org/10.1038/nature03635

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