Hostname: page-component-7479d7b7d-pfhbr Total loading time: 0 Render date: 2024-07-11T21:14:25.907Z Has data issue: false hasContentIssue false
  • English
  • Français

Biophysical constraints on the thermal ecology of dinosaurs

Published online by Cambridge University Press:  08 April 2016

Michael P. O'Connor  and
Peter Dodson
Michael P. O'Connor
Affiliation:
Department of Bioscience and Biotechnology, Drexel University, Philadelphia, Pennsylvania 19104. E-mail: mike.oconnor@drexel.edu
Peter Dodson
Affiliation:
Department of Animal Biology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6045. E-mail: dodsonp@vet.upenn.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

A physical, model-based approach to body temperatures in dinosaurs allows us to predict what ranges of body temperatures and what thermoregulatory strategies were available to those dinosaurs. We argue that

  1. 1. The huge range of body sizes in the dinosaurs likely resulted in very different thermal problems and strategies for animals at either end of this size continuum.

  2. 2. Body temperatures of the smallest adult dinosaurs and of hatchlings and small juveniles would have been largely insensitive to metabolic rates in the absence of insulation. The smallest animals in which metabolic heating resulted in predicted body temperatures ≥ 2°C above operative temperatures (Te) weigh 10 kg. Body temperature would respond rapidly enough to changes in Te to make behavioral thermoregulation possible.

  3. 3. Body temperatures of large dinosaurs (>1000 kg) likely were sensitive to both metabolic rate and the delivery of heat to the body surface by blood flow. Our model suggests that they could adjust body temperature by adjusting metabolic rate and blood flow. Behavioral thermoregulation by changing microhabitat selection would likely have been of limited utility because body temperatures would have responded only slowly to changes in Te.

  4. 4. Endothermic metabolic rates may have put large dinosaurs at risk for overheating unless they had adaptations to shed the heat as necessary. This would have been particularly true for dinosaurs with masses > 10,000 kg, but simulations suggest that for animals as small as 1000 kg in the Tropics and in temperate latitudes during the summer, steady-state body temperatures would have exceeded 40°C. Slow response of body temperatures to changes in Te suggests that use of day-night thermal differences would have buffered dinosaurs from diel warming but would not have lowered body temperatures sufficiently for animals experiencing high mean daily Te.

  5. 5. Endothermic metabolism and metabolic heating might have been useful for intermediate and large-sized (100–3000 kg) dinosaurs but often in situations that demanded marked seasonal adjustment of metabolic rates and/or precise control of metabolism (and heat-loss mechanisms) as typically seen in endotherms.

Type
Articles
Information
Paleobiology , Volume 25 , Issue 3 , Summer 1999 , pp. 341 - 368
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Alexander, R. M. 1989. Dynamics of dinosaurs and other extinct giants. Columbia University Press, New York.Google Scholar
Anderson, R. A., and Karasov, W. H. 1981. Contrasts in energy intake and expenditure in sit-and-wait and widely foraging lizards. Oecologia 49:67–72.Google Scholar
Bailey, J. B. 1997. Neural spine elongation in dinosaurs: sailbacks or buffalo-backs? Journal of Paleontology 71:1124–1146.Google Scholar
Baker, L. A., and White, F. N. 1970. Redistribution of cardiac output in response to heating in Iguana iguana. Comparative Biochemistry and Physiology 35:253–262.CrossRefGoogle Scholar
Baker, L. A., Weathers, W. W., and White, F. N. 1972. Temperature induced peripheral blood flow changes in lizards. Journal of Comparative Physiology 80:313–323.CrossRefGoogle Scholar
Bakken, G. S., and Gates, D. M. 1975. Heat-transfer analysis of animals: some implications for field ecology, physiology, and evolution. Pp. 255–290in Gates, D. M. and Schmerl, R., eds. Perspectives in biophysical ecology. Springer, New York.Google Scholar
Bakken, G. S., Santee, W. R., and Erskine, D. J. 1985. Operative and standard operative temperature: tools for thermal energetic studies. American Zoologist 25:933–944.Google Scholar
Bakker, R. T. 1971. Dinosaur physiology and evolution of mammals. Evolution 25:636–658.Google Scholar
Bakker, R. T. 1972. Anatomical and ecological evidence of endothermy in dinosaurs. Nature 238:81–85.CrossRefGoogle Scholar
Bakker, R. T. 1975. Dinosaur renaissance. Scientific American 232:58–78.Google Scholar
Bakker, R. T. 1986. The dinosaur heresies: new theories unlocking the mysteries of the dinosaurs and their extinction. Willaim Morrow, New York.Google Scholar
Barrick, R. E., Stoskopf, M. K., and Showers, W. J. 1997. Oxygen isotopes in dinosaur bone. Pp. 474–490in Farlow, and Brett-Surman, 1997.Google Scholar
Bartholomew, G. A. 1982. Physiological control of body temperature. Pp. 167–211in Gans, C. and Pough, F. H., eds. Biology of the Reptilia, Vol. 12 Academic Press, London.Google Scholar
Beaupre, S. J. 1995. Effects of geographically variable thermal environment on bioenergetics of mottled rock rattlesnakes. Ecology 76:1655–1665.Google Scholar
Benedict, F.G. 1936. The physiology of the elephant. Publications of the Carnegie Institution No. 474:1–302.Google Scholar
Bennett, A. F. 1982. The energetics of reptilian activity. Pp. 155–199in Gans, C. and Pough, F. H., eds. Biology of the Reptilia, Vol. 13. Academic Press, London.Google Scholar
Bennett, A. F., and Dawson, W. R. 1976. Metabolism. Pp. 127–224in Gans, C. and Dawson, W. R., eds. Biology of the Reptilia, Vol. 5. Academic Press, New York.Google Scholar
Beyer, E. C., and Spotila, J. R. 1994. Seasonal variation in metabolic rates and maintenance costs of the eastern fence lizard, Sceloporus undulatus. Comparative Biochemistry and Physiology A 109A:1039–1047.CrossRefGoogle Scholar
Bonaparte, J. F., and Coria, R. A. 1993. Un nuevo y gigantesco sauropodo titanosaurio de la Formación Rio Limay (Albiano–Cenomanio) de la Provincia del Neuquen, Argentina. Ameghiniana 30:271–282.Google Scholar
Burness, G. P., Ydenberg, R. C., and Hochachka, P. W. 1998. Interindividual variability in body composition and resting oxygen consumption in breeding tree swallows, Tachycineta bicolor. Physiological Zoology 71:247–256.Google Scholar
Buss, I. O., and Estes, J. A. 1971. The functional significance of movements and positions of the pinnae of the African elephant, Loxodonta africana. Journal of Mammmalogy 52:21–27.Google Scholar
Calder, W. A. 1984. Size, function, and life history. Harvard University Press, Cambridge.Google Scholar
Cena, K., and Monteith, J. L. 1975. Transfer processes in animal coats: II. Conduction and Convection. Proceedings of the Royal Society of London B 188:395–411.Google Scholar
Chinsamy, A. 1990. Physiological implications of the bone histology of Syntarsus rhodesiensis (Saurischia: Theropoda). Paleontologia Africana 27:77–82.Google Scholar
Chinsamy, A. 1993. Bone histology and growth trajectory of the prosauropod dinosaur Massospondylatus carinatus (Owen). Modern Geology 18:319–329.Google Scholar
Chinsamy, A., and Dodson, P. 1995. Inside a dinosaur bone. American Scientist 83:174–180.Google Scholar
Chinsamy, A., Chiappe, L., and Dodson, P. 1994. Growth rings in Mesozoic birds. Nature 368:196–197.CrossRefGoogle Scholar
Chinsamy, A., Chiappe, L., and Dodson, P. 1995. Mesozoic avian bone microstructure: physiological implications. Paleobiology 21:561–574.Google Scholar
Cowles, R. B. 1958. Possible origin of dermal temperature regulation. Evolution 12:347–357.CrossRefGoogle Scholar
Crichton, M. 1990. Jurassic Park. Knopf, New York.Google Scholar
Crowley, T. J., and North, G. R. 1991. Chap. 8. Mid-Cretaceous climate. Pp. 155–170in Paleoclimatology. Oxford Monographs on Geology and Geophysics No. 16. Oxford University Press, New York.Google Scholar
Economos, A. C. 1983. Elastic and/or geometric similarity in mammalian design? Journal of Theoretical Biology 103:167–172.CrossRefGoogle ScholarPubMed
Farlow, J. O., and Brett-Surman, M. K., eds. 1997. The complete dinosaur. Indiana University Press, Indianapolis.Google Scholar
Farlow, J. O., Thompson, C. V., and Rosner, D. E. 1976. Plates of the dinosaur Stegosaurus: forced convection heat loss fins? Science 192:1123–1125.Google Scholar
Gates, D. M. 1980. Biophysical ecology. Springer, New York.CrossRefGoogle Scholar
Gatten, R.E. 1985. Activity metabolism of lizards after thermal acclimation. Journal of Thermal Biology 10:209–215.CrossRefGoogle Scholar
Gillette, D. D. 1991. Seismosaurus halli (n. gen., n. sp.) a new sauropod dinosaur from the Morrison Formation (Upper Jurrasic-Lower Cretaceous) of New Mexico, U.S.A. Journal of Vertebrate Paleontology 11:417–433.CrossRefGoogle Scholar
Grant, B. W. 1990. Trade-offs in activity time and physiological performance for thermoregulating desert lizards, Sceloporus merriami. Ecology 71:2323–2333.CrossRefGoogle Scholar
Grant, B. W., and Dunham, A. E. 1988. Thermally imposed time constraints on the activity of the desert lizard Sceloporus merriami. Ecology 69:167–176.Google Scholar
Grigg, G. C., Drane, C. R., and Courtice, G. P. 1979. Time constants of heating and cooling in the eastern water dragon, Physignathus leseurii, and some generalizations about heating and cooling in reptiles. Journal of Thermal Biology 4:95–103.Google Scholar
John-Alder, H. B. 1983. Effects of thyroxine supplementation on metabolic rate and aerobic capacity in a lizard. American Journal of Physiology 244:R659–R666.Google Scholar
John-Alder, H. B. 1990. Thyroid regulation of resting metabolic rate and intermediary metabolic enzymes in a lizard (Sceloporus occidentalis). General and Comparative Endocrinology 77:52–62.Google Scholar
Konarzewski, M., and Diamond, J. 1994. Peak sustained metabolic rate and its individual variation in cold-stressed mice. Physiological Zoology 67:1186–1212.CrossRefGoogle Scholar
McKay, G. M. 1973. Behavioral ecology of the Asiatic elephant in southeastern Ceylon. Smithsonian Contributions to Zoology 125:1–113.CrossRefGoogle Scholar
Mautz, W. J., and Nagy, K. A. 1987. Ontogenetic changes in diet, field metabolic rate, and water flux in the herbivorous lizard Dipsosaurus dorsalis. Physiological Zoology 60:640–658.CrossRefGoogle Scholar
Mitchell, J. W. 1976. Heat transfer from spheres and other animal shapes. Biophysical Journal 16:561–569.CrossRefGoogle Scholar
Monteith, J. J., and Unsworth, M. H. 1990. Principles of environmental physics. Edward Arnold, London.Google Scholar
Nagy, K. A. 1987. Field metabolic rates and food requirement scaling in mammals and birds. Ecological Monographs 57:111–128.Google Scholar
Nagy, K. A. 1989. Field bioenergetics: accuracy of models and methods. Physiological Zoology 62:237–252.Google Scholar
Nagy, K. A., Huey, R. B., and Bennett, A. F. 1984. Field energetics and foraging mode of Kalahari lacertid lizards. Ecology 65:588–596.Google Scholar
O'Connor, M. P. 1999. Physiological and ecological implications of a simple model of heating and cooling in reptiles. Journal of Thermal Biology (in press).Google Scholar
O'Connor, M. P., and Spotila, J. R. 1992. Consider a spherical animal: when do short cuts matter in biophysical models? American Zoologist 32:179–193.Google Scholar
Owen, R. 1842. Report on British fossil reptiles. Reports of the British Association for the Advancement of Science 11:60–204.Google Scholar
Padian, K. 1997. Physiology. Pp. 552–557in Currie, P. J. and Padian, K., eds. The encyclopedia of dinosaurs. Academic Press, San Diego.Google Scholar
Paladino, F. V., Spotila, J. R., and Dodson, P. 1997. A blueprint for giants: modeling the physiology of large dinosaurs. Pp. 491–504. in Farlow, and Brett-Surman, 1997.Google Scholar
Paul, G. S. 1991. The many myths, some old, some new, of dinosaurology. Modern Geology 16:69–99.Google Scholar
Peczkis, J. 1994. Implications of body-mass estimates for dinosaurs. Journal of Vertebrate Paleontology 14:520–533.Google Scholar
Porter, W. P., and Gates, D. M. 1969. Thermodynamic equilibria of animals with environment. Ecological Monographs 39:227–244.Google Scholar
Pough, F. H. 1980. The advantages of ectothermy for tetrapods. American Naturalist 115:92–112.Google Scholar
Reid, R. E. H. 1997. Dinosaurian physiology: the case for “intermediate” dinosaurs. Pp. 449–473in Farlow, and Brett-Surman, 1997.Google Scholar
Rosenberg, N. J. 1974. Microclimate: the biological environment. Wiley, New York.Google Scholar
Ruben, J., Hillenius, W. J., Geist, N. R., Leitch, A., Jones, T. D., Currie, P. J., Horner, J. R., and Espe, G. III. 1996. The metabolic status of some Late Cretaceous dinosaurs. Science 273:1204–1207.CrossRefGoogle Scholar
Ruben, J., Leitch, A., Hillenius, W., Geist, N., and Jones, T. 1997. New insights into the metabolic physiology of dinosaurs. Pp. 505–518in Farlow, and Brett-Surman, 1997.Google Scholar
Sereno, P. C., Forster, C. A., Rogers, R. R., and Monetta, A. M. 1993. Primitive dinosaur skeleton from Argentina and the early evolution of Dinosauria. Nature 361:64–66.CrossRefGoogle Scholar
Spotila, J. R. 1980. Constraints of body size and environment on the temperature regulation of dinosaurs. Pp. 233–252in Thomas, R. D. K. and Olson, E. C., eds. A cold look at warm-blooded dinosaurs. American Association for the Advancement of Sciences Symposium 28. Westview, Boulder, Colo.Google Scholar
Spotila, J. R., Lommen, P. W., Bakken, G. S., and Gates, D. M. 1973. A mathematical model for body temperatures of large reptiles: implications for dinosaur ecology. American Naturalist 107:391–404.Google Scholar
Spotila, J. R., O'Connor, M. P., Dodson, P., and Paladino, F. V. 1991. Hot and cold running dinosaurs: metabolism, body temperature, and migration. Modern Geology 16:203–227.Google Scholar
Spotila, J. R., O'Connor, M. P., and Bakken, G. S. 1992. The biophysics of heat and mass exchange in amphibians. Pp.59–80in Feder, M. E. and Burggren, W., eds. The ecological physiology of the amphibia. University of Chicago Press, Chicago.Google Scholar
Thomas, R. D. K., and Olson, E. C., eds. A cold look at warm-blooded dinosaurs. American Association for the Advancement of Sciences Symposium 28. Westview, Boulder, Colo.Google Scholar
Tracy, C. R. 1982. Biophysical modeling in reptilian physiology and ecology. Pp. 275–321in Gans, C. and Pough, F. H., eds. Biology of the Reptilia, Vol. 12 Academic Press, London.Google Scholar
Tracy, C. R., Turner, J. S., and Huey, R. B. 1986. A biophysical analysis of possible thermoregulatory adaptations in sailed pelycosaurs. Pp. 195–206in Hotton, N. III, MacLean, P. D., Roth, J. J., and Roth, E. C., eds. The ecology and biology of mammal-like reptiles. Smithsonian Institution Press, Washington, D.C.Google Scholar
Tsuji, J. S. 1988. Seasonal profiles of standard metabolic rate of lizards (Sceloporus occidentalis) in relation to latitude. Physiological Zoology 61:230–240.Google Scholar
Turner, J. S. 1987. The cardiovascular control of heat exchange: consequences of body size. American Zoologist 27:69–79.CrossRefGoogle Scholar
Turner, J. S., and Tracy, C. R. 1983. Blood flow to appendages and the control of heat exchange in American alligators. Physiological Zoology 56:195–200.Google Scholar
Turner, J. S., and Tracy, C. R. 1985. Body size and the control of heat exchange in alligators. Journal of Thermal Biology 10:9–11.Google Scholar
Turner, J. S., and Tracy, C. R. 1986. Body size, homeothermy and the control of heat exchange in mammal-like reptiles. Pp. 185–194in Hotton, N. III, MacLean, P. D., Roth, J. J., and Roth, E. C., eds. The ecology and biology of mammal-like reptiles. Smithsonian Institution Press, Washington, D.C.Google Scholar
Welch, W. R., and Tracy, C. R. 1977. Respiratory water loss: a predictive model. Journal of Theoretical Biology 65:253–265.Google Scholar
Wheeler, P. E. 1978. Elaborate CNS cooling structures in large dinosaurs. Nature 275:441–443.Google Scholar
White, F. M. 1984. Heat transfer. Addison-Wesley, Reading, Mass.Google Scholar
Williams, T. M. 1990. Heat transfer in elephants: thermal partitioning based on skin temperature profiles. Journal of Zoology 222:235–245.Google Scholar
Withers, P. C. 1992. Comparative animal physiology. Sunders College Publishing, Fort Worth, Tex.Google Scholar
Wright, P. G. 1984. Why do elephants flap their ears? South African Journal of Zoology 19:266–269.Google Scholar
Wright, P. G., and Luck, C. P. 1984. Do elephants need to sweat? South African Journal of Zoology 19:270–274.Google Scholar