Letter | Published:

Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology

Nature volume 487, pages 358361 (19 July 2012) | Download Citation

Abstract

Cyclical growth leaves marks in bone tissue that are in the forefront of discussions about physiologies of extinct vertebrates1. Ectotherms show pronounced annual cycles of growth arrest that correlate with a decrease in body temperature and metabolic rate; endotherms are assumed to grow continuously until they attain maturity because of their constant high body temperature and sustained metabolic rate1,2. This apparent dichotomy has driven the argument that zonal bone denotes ectotherm-like physiologies, thus fuelling the controversy on dinosaur thermophysiology and the evolution of endothermy in birds and mammal-like reptiles1,2,3,4. Here we show, from a comprehensive global study of wild ruminants from tropical to polar environments, that cyclical growth is a universal trait of homoeothermic endotherms. Growth is arrested during the unfavourable season concurrently with decreases in body temperature, metabolic rate and bone-growth-mediating plasma insulin-like growth factor-1 levels, forming part of a plesiomorphic thermometabolic strategy for energy conservation. Conversely, bouts of intense tissue growth coincide with peak metabolic rates and correlated hormonal changes at the beginning of the favourable season, indicating an increased efficiency in acquiring and using seasonal resources. Our study supplies the strongest evidence so far that homeothermic endotherms arrest growth seasonally, which precludes the use of lines of arrested growth as an argument in support of ectothermy. However, high growth rates are a distinctive trait of mammals, suggesting the capacity for endogenous heat generation. The ruminant annual cycle provides an extant model on which to base inferences regarding the thermophysiology of dinosaurs and other extinct taxa.

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Acknowledgements

We thank Th. Kaiser for permission to cut femora of skeletons from the Oboussier collections and from zoological material housed at the Zoological Institute and Museum of the University of Hamburg; W. Arnold for providing alpine red deer material, and A. Kübber for preparing and sending it; R. García González for providing red deer femora from Jaca (Spanish Pyrenees) and Capra ibex from Alfarc (Tarragona, Spain); all the people that helped collect the Svalbard material, and R. García for preparation of the thin sections; and J. Horner, H. Woodward, S. Moyà-Solà, T. Bromage and J. Cubo for comments on the manuscript. This work was supported by the Spanish Ministry of Science and Innovation (CGL2008-06204/BTE, 2012: CGL2011-24685, M.K.; BES-2009-02641, N.M.-M.; JCI-2010-08157, X.J.); the work was partly funded by the Norwegian Research Council (NORKLIMA 178561/S30, R.A.). The material is tabulated in the Supporting Online Material and archived at the Institut Català de Paleontologia, Catalonia, Spain.

Author information

Affiliations

  1. ICREA at the Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain

    • Meike Köhler
  2. Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain

    • Nekane Marín-Moratalla
    •  & Xavier Jordana
  3. Norwegian Polar Institute, Fram Centre, NO-9296 Tromsø, Norway

    • Ronny Aanes
  4. Norwegian Directorate for Nature Management, NO-7047 Trondheim, Norway

    • Ronny Aanes

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Contributions

M.K. designed the study and wrote the manuscript. R.A. gathered the Svalbard material and was involved in discussions about the biology of Svalbard reindeer. M.K., N.M.-M. and X.J. analysed data and discussed the results and implications at all stages.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Meike Köhler.

Supplementary information

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    Supplementary Information

    This file contains Supplementary Figures 1-2, Supplementary Methods, additional references, Supplementary Table 1 and Supplementary Materials.

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DOI

https://doi.org/10.1038/nature11264

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