Polar and K/Pg nonavian dinosaurs were low-metabolic rate reptiles vulnerable to cold-induced extinction, rather than more survivable tachyenergetic bird relatives: comment on an obsolete hypothesis

Discussion

Abstract

The great majority of researchers concur that the presence of dinosaurs near the poles of their time are part of a large body of evidence that all Cretaceous dinosaurs had elevated metabolic rates more like their avian subbranch and mammals than low-energy reptiles. Yet a few still propose that nonavian dinosaurs were bradyenergetic ectothermic reptiles, and migrated away from the polar winters. The latter is not biologically possible because land animals cannot and never undertake very long seasonal migrations because the cost of ground locomotion is too high even for long limbed, tachyenergetic mammals to do so, much less low-energy reptiles. Nor was it geographically possible because marine barriers barred some polar dinosaurs from moving towards the winter sun. The presence of external insulation on some dinosaurs both strongly supports their being tachyenergetic endotherms and helps explain their ability to survive polar winters that included extended dark, chilling rains, sharp frosts, and blizzards so antagonistic to reptiles that the latter are absent from some locations that preserve dinosaurs including birds and mammals. The hypothesis that nonavian dinosaurs failed to survive the K/Pg crisis because they had reptilian energetics is illogical not only because they did not have such metabolisms, but because many low-energy reptiles did survive the crisis. The global super chill that apparently plagued K/Pg dinosaurs should have seriously impacted dinosaurs at all latitudes, but does not entirely readily explain their loss because some avian dinosaurs and other land tetrapods did survive. High- as well as low-latitude dinosaurs add to the growing evidence that high-energy endothermy has been a common adaptation in a wide variety of vertebrates and flying insects since the late Paleozoic.

Keywords

Dinosaurs Alaskan Australian Polar Winters Energetics Physiology Migration Cretaceous 

References

  1. Amiot R, Lecuyer C, Buffetaut E, Escarguel G, Fluteau F, Martineau F (2006) Oxygen isotopes from biogenic apatites suggest widespread endothermy in Cretaceous dinosaurs. Earth Planet Sci Lett 246:41–54CrossRefGoogle Scholar
  2. Amiot R, Xu W, Zhinge Zm Xiaolin W, Buffataut Em Lecuyer C, Zhongli D, Fluteau F, Tsuyoshi H, Nao K, Jinyao M, Suteethorn V, Yauanging W, Xing X, Fusong Z (2011) Oxygen isotopes of east Asian dinosaurs reveal exceptionally cold Early Cretaceous climates. Proc Natl Acad Sci USA 108:5179–5183CrossRefGoogle Scholar
  3. Bakker R (1968) The superiority of dinosaurs. Discovery 3:11–22Google Scholar
  4. Bakker R (1971) Dinosaur physiology and the origin of mammals. Evolution 25:636–658CrossRefGoogle Scholar
  5. Bakker R (1972) Anatomical and ecological evidence of endothermy in dinosaurs. Nature 238:81–85CrossRefGoogle Scholar
  6. Bakker R (1975) Dinosaur renaissance. Sci Amer 232(4):58–78CrossRefGoogle Scholar
  7. Bakker R, Zoehfeld K, Temple D, Flis C (2016) Endothermy acquired: tracks and productivity efficiency show elevated energy consumption during origin of dinosaurs and advanced therapsids. In: Soc Vert Paleont 76th Ann Meet Abstracts, p. 91Google Scholar
  8. Barrick R, Stoskopf M, Showers W (1997) Oxygen isotopes in dinosaur bone. In: Farlow J, Brett-Surman M (eds) The complete dinosaur. Indiana University Press, Bloomington, pp 474–490Google Scholar
  9. Bell P, Snively E (2008) Polar dinosaurs on parade: a review of dinosaur migration. Alcheringa 32:271–284CrossRefGoogle Scholar
  10. Bernal D, Donley M, Shadwick R, Syme D (2005) Mammal-like muscles power swimming in a cold-water shark. Nature 437:1349–1352CrossRefGoogle Scholar
  11. Bernard A, Lécuye C, Vincent P, Amiot R, Bardet N, Buffetaut E, Cuny G, Fourel F, Martineau F, Mazin Q, Prieur A (2010) Regulation of body temperature by some Mesozoic marine reptiles. Science 328:1379–1382CrossRefGoogle Scholar
  12. Brill R, Bushnell P (2001) The cardiovascular system of tunas. Fish Physiol 19:79–120CrossRefGoogle Scholar
  13. Brouwers E, Clemens W, Spicer R, Ager T, Carter L, Sliter W (1987) Dinosaurs on the North Slope, Alaska: high latitude, latest Cretaceous environments. Science 237:1608–1610CrossRefGoogle Scholar
  14. Brugger J, Feulner G, Petri S (2017) Baby, it’s cold outside: climate model simulations of the effects of the asteroid impact at the end of the Cretaceous. Geophys Res Lett 44:419–427CrossRefGoogle Scholar
  15. Carrier D, Farmer C (2000) The evolution of pelvic aspiration in archosaurs. Paleobiology 26:271–293CrossRefGoogle Scholar
  16. Chinsamy A, Thomas D, Tumarkan-Deratzian A, Fiorillo A (2012) Hadrosaurs were perennial polar residents. Anat Rec 295:610–614CrossRefGoogle Scholar
  17. Clarke A (2013) Dinosaur energetics: setting the bounds on feasible physiologies and ecologies. Am Nat 182:283–297CrossRefGoogle Scholar
  18. Clemens WA, Nelms LG (1993) Paleoecological implications of Alaskan terrestrial vertebrate fauna in latest Cretaceous time at high paleolatitudes. Geology 21(6):503–506CrossRefGoogle Scholar
  19. Constantine A, Chinsamy A, Vickers-Rich P, Rich T (1998) Periglacial environments and polar dinosaurs. S Afr J Sci 94:137–141Google Scholar
  20. Crichton M (1990) Jurassic park. Knopf, New YorkGoogle Scholar
  21. Desmond A (1976) The hot-blooded dinosaurs. The Dial Press, New YorkGoogle Scholar
  22. Eagle R, Tutken T, Martin T, Tripati A, Fricke H, Connely M, Cifelli R, Eiler J (2011) Dinosaur body temperatures determined from isotopic ordering in fossil biominerals. Science 333:443–445CrossRefGoogle Scholar
  23. Erickson G, Brochu C (1999) How the ‘terror crocodile’ grew so big. Nature 398:205–206CrossRefGoogle Scholar
  24. Erickson G, Druckenmiller P (2011) Longevity and growth rate estimates for a polar dinosaur: a Pachyrhinosaurus specimen from the North Slope of Alaska showing a complete developmental record. Hist Biol 23:327–334CrossRefGoogle Scholar
  25. Erickson G, Curry Rogers K, Yerby S (2001) Dinosaurian growth patterns and rapid avian growth rates. Nature 412:429–433CrossRefGoogle Scholar
  26. Erickson G, Makovicky P, Inouye B, Chang-Fu Z, Ke-Qin G (2009a) A life table for Psittacosaurus lujiatuensis: initial insights into ornithischian population biology. Anat Rec 292:1514–1521CrossRefGoogle Scholar
  27. Erickson G, Rauhut O, Zhou Z, Turner A, Inouye B, Ho D, Norell M (2009b) Was dinosaurian physiology inherited by birds? Reconciling slow growth in Archaeopteryx. PLoS ONE 4:e7390CrossRefGoogle Scholar
  28. Erickson G, Zelenitsky D, Kay D, Norell M (2017) Dinosaur incubation periods directly determined from growth-line counts in embryonic teeth show reptilian-grade development. Proc Natl Acad Sci USA 114:540–545CrossRefGoogle Scholar
  29. Fancy S, Pank L, Whitten K, Regelin W (1989) Seasonal movements of caribou in Arctic Alaska as determined by satellite. Canad J Zool 67:644–650CrossRefGoogle Scholar
  30. Farmer C, Sander K (2010) Unidirectional airflow in the lungs of alligators. Science 327:338–340CrossRefGoogle Scholar
  31. Fiorillo A (2004) The dinosaurs of arctic Alaska. Sci Amer 291:84–91CrossRefGoogle Scholar
  32. Fiorillo A, Gangloff R (2001) The caribou migration model for Arctic hadrosaurs: a reassessment. Hist Biol 15:323–334CrossRefGoogle Scholar
  33. Fiorillo A, Tykoski R (2012) A new Maastrichtian species of the centrosaurine ceratopsid Pachyrhinosaurus form the North Slope of Alaska. Acta Palaeontol Pol 57:561–573CrossRefGoogle Scholar
  34. Fiorillo A, Tykoski R (2014) A diminutive new tyrannosaur from the top of the world. PLoS ONE 9:e91287CrossRefGoogle Scholar
  35. Fricke H, Rogers R (2000) Multiple taxon-multiple locality approach to providing oxygen isotope evidence for warm-blooded theropod dinosaurs. Geology 28:799–802CrossRefGoogle Scholar
  36. Gangloff R (2012) Dinosaurs under the aurora. Indiana University Press, BloomingtonGoogle Scholar
  37. Godefroit P, Golovneva L, Shchepetov S, Garcia G, Alekseev P (2008) The last polar dinosaurs in Russia. Naturwissen 96:459–501Google Scholar
  38. Grady J, Enquist B, Dettweller-Robinson E, Wright N, Smith F (2014) Evidence for mesothermy in dinosaurs. Science 344:1268–1272CrossRefGoogle Scholar
  39. Graham J, Dickson K (2004) Tuna comparative physiology. J Exp Biol 207:4015–4024CrossRefGoogle Scholar
  40. Grellet-Tinner G, Fiorelli L (2010) A new Argentinean nesting site showing neosauropod dinosaur reproduction in a Cretaceous hydrothermal environment. Nat Comm 1:32. doi:10.1038/ncomms1031 CrossRefGoogle Scholar
  41. Harrell T, Perez-Huerta A, Suarez C (2016) Endothermic mosasaurs? Possible thermoregulation of Late Cretaceous mosasaurs indicated by stable oxygen isotopes in fossil bioapatite marine fish and pelagic seabirds. Palaeont 59:351–363CrossRefGoogle Scholar
  42. Heinrich B (1993) The hot-blooded insects. Harvard University Press, CambridgeCrossRefGoogle Scholar
  43. Horner J, Padian K (2004) Age and growth dynamics of Tyrannosaurus rex. Proc R Soc Lond B 271:1875–1880CrossRefGoogle Scholar
  44. Huttenlocker A, Farmer C (2017) Bone microvasculature tracks red blood cell size diminution in Triassic mammal and dinosaur forerunners. Curr Biol 27:1–7CrossRefGoogle Scholar
  45. Kohler M, Marin-Moratalla N, Jordana X, Aanes R (2012) Seasonal bone growth and physiology in endotherms shed light on dinosaur physiology. Nature 487:358–361CrossRefGoogle Scholar
  46. Lewy Z (2015) How the Deccan vulcanism and the Chicxulub asteroid impact resulted in the biological crisis ending the Mesozoic era. J Geogr Environ Earth Sci Int 3:1–11CrossRefGoogle Scholar
  47. Lewy Z (2016) Dinosaur demise in light of their alleged perennial polar residency. Int J Earth Sci. doi:10.1007/s00531-016-1426-9 Google Scholar
  48. Martin A (2009) Dinosaur burrows in the Otway Group of Victoria, Australia, and their relation to Cretaceous polar environments. Cret Res 30:1223–1237CrossRefGoogle Scholar
  49. McNab B (2009) Resources and energetics determined dinosaur body size. Proc Natl Acad Sci USA 106:12188–12189CrossRefGoogle Scholar
  50. Molnar R, Wiffen J (1994) A Late Cretaceous polar dinosaur fauna from New Zealand. Cret Res 15:689–706CrossRefGoogle Scholar
  51. Organ C, Shedlock A, Meade A, Pagel M, Edwards S (2007) Origin of avian genome size and structure in non-avian dinosaurs. Nature 446:180–184CrossRefGoogle Scholar
  52. Ostrom J (1970) Terrestrial vertebrates as indicators of Mesozoic climates. N Am Paleontol Conv Proc D: 347-376Google Scholar
  53. Padian K, Ricqles A, Horner J (2001) Dinosaurian growth rates and bird origins. Nature 412:405–408CrossRefGoogle Scholar
  54. Paul G (1988) Physiological, migratorial, climatological, geophysical, survival and evolutionary implications of Cretaceous polar dinosaurs. J Palaeont 62:640–652CrossRefGoogle Scholar
  55. Paul G (1994) Physiology and migration of North Slope dinosaurs. In: Thurston D, Fujita K (eds) 1992 Proceedings International Conference on Arctic Margins. Anchorage: U.S. Department of the Interior, pp 405–408Google Scholar
  56. Paul G (2002) Dinosaurs of the air. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  57. Paul G (2012) Evidence for avian-mammalian aerobic capacity and thermoregulation in Mesozoic dinosaurs. In: Farlow J (ed) The complete dinosaur, 2nd edn. Indiana University Press, Bloomington, pp 819–872Google Scholar
  58. Paul G (2013) How far did dinosaurs really migrate? J Exp Biol 216:3762CrossRefGoogle Scholar
  59. Perry S, Christian A, Breuer T, Pajor N, Codd J (2009) Implications of an avian-style respiratory system for gigantism in sauropod dinosaurs. J Exp Zool 311A:600–610CrossRefGoogle Scholar
  60. Pontzer H, Allen V, Hutchinson J (2009) Biomenchanics of running indicates endothermy in bipedal dinosaurs. PLoS ONE 4:e7783CrossRefGoogle Scholar
  61. Priede I (1985) Metabolic scope in fishes. In: Tyler P, Calow P (eds) Fish energetics: new perspectives. The Johns Hopkins University Press, Baltimore, pp 33–64CrossRefGoogle Scholar
  62. Reid E (2012) “Intermediate” dinosaurs: the case updated. In: Farlow J (ed) The complete Dinosaur, 2nd edn. Indiana University Press, Bloomington, pp 873–921Google Scholar
  63. Rich T, Vickers-Rich P (2001) Dinosaurs of darkness. Indiana University Press, BloomingtonGoogle Scholar
  64. Rich P, Rich T, Wagstaff B, Mason J, Douthitt C, Gregory R, Felton E (1988) Evidence for low temperatures and biologic diversity in Cretaceous high latitudes of Australia. Science 242:1403–1406CrossRefGoogle Scholar
  65. Ricqles A (1976) On bone histology of fossil and living reptiles, with comments on its functional and evolutionary significance. In: Cox B, Bellairs A (eds) Morphology and biology of reptiles. Academic Press, London, pp 123–149Google Scholar
  66. Ricqles A, Padian K, Knoll F, Horner J (2008) On the origin of high growth rates in archosaurs and their ancient relatives: complementary histological studies on Triassic archosauriforms and the problem of a “phylogenetic signal” in bone histology. Ann Paleont 94:57–76CrossRefGoogle Scholar
  67. Ruben J, Jones T, Geist N, Hillenius W, Harwell A, Quick D (2012) Metabolic physiology of dinosaurs and early birds. In: Farlow J (ed) The complete dinosaur, 2nd edn. Indiana University Press, Bloomington, pp 785–818Google Scholar
  68. Russell D (1990) Mesozoic vertebrates of Arctic Canada. In: Harington C (ed) Canada’s missing dimension: science and history in the Canadian Arctic islands, vol 1. Canadian Museum of Nature, Ottawa, pp 81–90Google Scholar
  69. Sander P, Christian A, Clauss W, Fechner R, Gee C, Griebler E, Gunga H, Hummel J, Mallison H, Perry S, Preuschoft H, Rauhut O, Remes K, Tutken T, Wings O, Witzel U (2011) Biology of the sauropod dinosaurs: the evolution of gigantism. Biol Rev 86:117–155CrossRefGoogle Scholar
  70. Schweitzer M, Marshall C (2001) A molecular model for the evolution of endothermy in the theropod-bird lineage. J Exp Zool 291:317–338CrossRefGoogle Scholar
  71. Seymour R (2013) Maximal aerobic and anaerobic power generation in large crocodiles versus mammals: implications for dinosaur gigantothermy. PLoS ONE 8:e69361CrossRefGoogle Scholar
  72. Seymour R (2016) Cardiovascular physiology of dinosaurs. Physiology 31:430–441CrossRefGoogle Scholar
  73. Seymour R, Lillywhite H (2000a) Hearts, necks posture and metabolic intensity of sauropod dinosaurs. Proc Royal Soc Lond B 267:1883–1887CrossRefGoogle Scholar
  74. Seymour R, Lillywhite H (2000b) Hearts, neck posture and metabolic intensity of sauropod dinosaurs. Nature 264:664–666Google Scholar
  75. Seymour R, Bennett-Stamper C, Johnston S, Carrier D, Grigg G (2004) Evidence for endothermic ancestors of crocodiles at the stem of archosaur evolution. Physiol Biochem Zool 77:1051–1067CrossRefGoogle Scholar
  76. Seymour R, Smith S, White C, Henderson D, Schwarz-Wings D (2012) Blood flow to long bones indicates activity metabolism in mammals, reptiles and dinosaurs. Proc Biol Sci 279:451–456CrossRefGoogle Scholar
  77. Shelton C, Sander P (2017) Long bone histology of Ophiacodon reveals the geologically earliest occurrence of fibrolamellar bone in the mammalian stem lineage. Comptes Rend Palevol. doi:10.1016/j.crpv.2017.02.002 Google Scholar
  78. Spicer R, Herman A (2010) The Late Cretaceous environment of the Arctic: a quantitative reassessment based on plant fossils. Paleogeog Palaeoclim Palaeoecol 295:423–442CrossRefGoogle Scholar
  79. Spicer R, Herman A, Amiot R, Spicer T (2016) Environmental adaptations and constraints on latest Cretaceous Arctic dinosaurs. Global Geol 19:187–204Google Scholar
  80. Teitelbaum C et al (2015) How far to go? Determinants of migration distance of distance in land mammals. Ecol Lett 18:545–552CrossRefGoogle Scholar
  81. Thompson G (1995) Foraging patterns and behaviours, body postures and movement speed for Varanus gouldii, in a semi-urban environment. J Royal Soc Wes Aust 78:107–114Google Scholar
  82. Varricchio D, Jackson F (2016) Reproduction in Mesozoic birds and evolution of the modern avian reproductive mode. Auk 133:654–684CrossRefGoogle Scholar
  83. Vavrek M, Hills L, Currie P (2014) A hadrosaurid from the Late Cretaceous Kanguk Formation of Axel Heiberg Island, Nunavut, Canada, and its ecological and geographical implications. Arctic 67:1–9CrossRefGoogle Scholar
  84. Wegner NC, Snodgrass OE, Dewar H, Hyde JR (2015) Whole-body endothermy in a mesopelagic fish, the opah, Lampris guttatus. Science 348(6236):786–789CrossRefGoogle Scholar
  85. Xu X et al (2012) A gigantic feathered dinosaur from the Lower Cretaceous of China. Nature 484:92–95CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.BaltimoreUSA

Personalised recommendations