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


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.


  1. Fastovsky, D. E. & Weishampel, D. B. Dinosaurs. A Concise Natural History (Cambridge Univ. Press, 2009)

    Book  Google Scholar 

  2. Chinsamy, A. & Hillenius, J. in The Dinosauria 2nd edn (eds Weishampel, D., Dodson, B. P. & Osmolska, H. ) 643–659 (Univ. of California Press, 2004)

    Book  Google Scholar 

  3. Bennett, A. F. & Ruben, J. A. in The Ecology and Biology of Mammal-like Reptiles (eds Hotton, N.,, MacLean, P. D., Roth, J. J. & Roth, E. C. ) 207–218 (Smithsonian Institution Press, 1986)

    Google Scholar 

  4. Padian, K. & Horner, J. R. in The Dinosauria 2nd edn (eds Weishampel, D., Dodson, B. P. & Osmolska, H. ) 660–671 (Univ. of California Press, 2004)

    Book  Google Scholar 

  5. Klevezal, G. A. Recording Structures of Mammals. Determination of Age and Reconstruction of Life History (A.A. Balkema, 1996)

    Google Scholar 

  6. Reid, R. H. Primary bone and dinosaurian physiology. Geol. Mag. 121, 589–598 (1984)

    Article  ADS  Google Scholar 

  7. Sander, P. M. & Andrássy, P. Lines of arrested growth and long bone histology in Pleistocene large mammals from Germany: what do they tell us about dinosaur physiology? Palaeontographica A 277, 143–159 (2006)

    Google Scholar 

  8. Chinsamy, A., Thomas, D. B., Tumarkin-Dertzian, A. R. & Fiorillo, A. R. Hadrosaurs were perennial polar residents. Anat. Rec. 295, 610–614 (2012)

    Article  Google Scholar 

  9. Tyler, N. J. C. & Blix, A. S. Survival strategies in arctic ungulates. Rangifer 3, 211–230 (1990)

    Article  Google Scholar 

  10. McNab, B. Geographic and temporal correlations of mammalian size reconsidered: a resource rule. Oecologia 164, 13–23 (2010)

    Article  ADS  Google Scholar 

  11. Klein, N. & Sander, M. Ontogenetic stages in the long bone histology of sauropod dinosaurs. Paleobiology 34, 247–263 (2008)

    Article  Google Scholar 

  12. Gruber, A. & Levizzani, V. Assessment of Global Precipitation Products. A Project of the World Climate Research Programme Global Energy and Water Cycle Experiment (GEWEX) Radiation Panel (WCRP Report no. 128, WMO/TD no. 1430) (World Meteorological Organization, 2008)

    Google Scholar 

  13. de Margerie, E., Cubo, J. & Castanet, J. Bone typology and growth rate: testing and quantifying ‘Amprino’s rule’ in the mallard (Anas platyrhynchus). C. R. Biol. 325, 221–230 (2002)

    Article  Google Scholar 

  14. Reimers, E. Body composition and population regulation of Svalbard reindeer. Rangifer 4, 16–21 (1984)

    Article  Google Scholar 

  15. Aanes, R., Sæther, B.-E. & Øritsland, N. A. Fluctuations of an introduced population of Svalbard reindeer: the effects of density dependence and climatic variation. Ecography 23, 437–443 (2000)

    Article  Google Scholar 

  16. Ringberg, T. The Spitzbergen reindeer—a winter-dormant ungulate? Acta Physiol. Scand. 105, 268–273 (1979)

    Article  CAS  Google Scholar 

  17. Courtland, H.-W. et al. Serum IGF-1 affects skeletal acquisition in a temporal and compartment-specific manner. PLoS ONE 6, e14762 (2011)

    Article  ADS  CAS  Google Scholar 

  18. Bubenik, G. A. et al. Seasonal levels of metabolic hormones and substrates in male and female reindeer (Rangifer tarandus). Comp. Biochem. Physiol. 120, 307–315 (1998)

    CAS  Google Scholar 

  19. Turbill, C., Ruf, T., Mang, T. & Arnold, W. Regulation of heart rate and rumen temperature in red deer: effects of season and food intake. J. Exp. Biol. 214, 963–970 (2010)

    Article  Google Scholar 

  20. Arnold, W. et al. Nocturnal hypometabolism as an overwintering strategy of red deer (Cervus elaphus). Am. J. Physiol. Regul. Integr. Comp. Physiol. 286, R174–R181 (2004)

    Article  CAS  Google Scholar 

  21. Lawler, J. P. & White, R. G. Seasonal changes in metabolic rates in muskoxen following twenty-four hours of starvation. Rangifer 17, 135–138 (1997)

    Article  Google Scholar 

  22. Piccione, G., Giannetto, C., Casella, S. & Caola, G. Annual rhythms of some physiological parameters in Ovis aries and Capra hircus. Biol. Rhythm Res. 40, 455–464 (2009)

    Article  CAS  Google Scholar 

  23. Suttie, J. M. & Webster, J. R. Extreme seasonal growth in arctic deer: comparisons and control mechanisms. Am. Zool. 35, 215–221 (1995)

    Article  CAS  Google Scholar 

  24. Hetem, R. S. et al. Variation in the daily rhythm of body temperature of free-living Arabian oryx (Oryx leucoryx): does water limitation drive heterothermy? J. Comp. Physiol. 180, 1111–1119 (2010)

    Article  Google Scholar 

  25. Signer, C., Ruf, T. & Arnold, W. Hypometabolism and basking: the strategies of Alpine ibex to endure harsh over-wintering conditions. Funct. Ecol. 25, 537–547 (2011)

    Article  Google Scholar 

  26. Ostrowski, S., Mesochina, P. & Williams, J. B. Physiological adjustments of Sand Gazelles (Gazella subgutturosa) to a boom-or-bust economy: standard fasting metabolic rate, total evaporative water loss, and changes in the sizes of organs during food and water restriction. Physiol. Biochem. Zool. 79, 810–819 (2006)

    Article  Google Scholar 

  27. Todini, L. Thyroid hormones in small ruminants: effects of endogenous, environmental and nutritional factors. Animal 1, 997–1008 (2007)

    Article  CAS  Google Scholar 

  28. McNab, B. K. The Physiological Ecology of Vertebrates. A View from Energetics (Cornell Univ. Press, 2002)

    Google Scholar 

  29. Montes, L., Castanet, J. & Cubo, J. Relationship between bone growth rate and bone tissue organization in amniotes: first test of Amprino’s rule in a phylogenetic context. Animal Biol. 60, 25–41 (2010)

    Article  Google Scholar 

  30. Peel, M. C., Finlayson, B. L. & McMahon, T. A. Updated world map of the Köppen–Geiger climate classification. Hydrol. Earth Syst. Sci. Discuss. 11, 1633–1644 (2007)

    Article  ADS  Google Scholar 

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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).

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