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

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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Figure 1: World map of Köppen-Geiger climate classification30, showing the climate zones of sample sites.
Figure 2: Climatic context of rest line formation.
Figure 3: A ruminant model for the correlation between bone tissue cycles and seasonal physiology.

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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.

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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.

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Correspondence to Meike Köhler.

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The authors declare no competing financial interests.

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Köhler, M., Marín-Moratalla, N., Jordana, X. et al. Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature 487, 358–361 (2012). https://doi.org/10.1038/nature11264

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