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The evolution of nasal turbinates and mammalian endothermy

Published online by Cambridge University Press:  08 February 2016

Willem J. Hillenius
Willem J. Hillenius*
Affiliation:
Department of Zoology, Cordley 3029, Oregon State University, Corvallis, Oregon 97331-2914
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Abstract

Complex nasal turbinal bones are associated with reduction of respiratory water loss in desert mammals and have previously been described as an adaptation to xeric conditions. However, complex turbinates are found in virtually all mammals. Experimental data presented here indicate that turbinates also substantially reduce respiratory water loss in five species of small mammals from relatively mesic environments. The data support the conclusion that turbinates did not evolve primarily as an adaptation to particular environmental conditions, but in relation to high ventilation rates, typical of all mammals. Complex turbinates appear to be an ancient attribute of mammals and may have originated among the therapsid ancestors of mammals, in relation to elevated ventilation rates and the evolution of endothermy.

Type
Articles
Information
Paleobiology , Volume 18 , Issue 1 , Winter 1992 , pp. 17 - 29
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Anthony, R.L.F., and Iliesco, G. M. 1926. Etude sur les cavités nasales des carnassiers. Proceedings of the Zoological Society (London) 1926:989–1015.CrossRefGoogle Scholar
Baker, M. A. 1982. Brain cooling in endotherms in heat and exercise. Annual Review of Physiology 44:85–96.CrossRefGoogle ScholarPubMed
Bang, B. G. 1961. The surface pattern of the nasal mucosa and its relation to mucous flow—a study of chicken and herring gull nasal mucosae. Journal of Morphology 109:57–72.CrossRefGoogle ScholarPubMed
Bang, B. G. 1964. The nasal organs of the black and turkey vultures; a comparative study of the cathartid species Coragyps atratus atratus and Cathartes aura septentrionalis (with notes on Cathartes aura falklandica, Pseudogyps bengalensis, and Neophron percnopterus). Journal of Morphology 115:153–184.CrossRefGoogle ScholarPubMed
Bang, B. G. 1966. The olfactory apparatus of tubenosed birds (Procellariformes). Acta Anatomica 65:391–415.CrossRefGoogle Scholar
Bang, B. G. 1968. Olfaction in Rallidae (Gruiformes), a morphological study of thirteen species. Journal of Zoology, London 156:97–107.CrossRefGoogle Scholar
Bennett, A. F. 1972. The effect of activity on oxygen consumption, oxygen debt, and heart rate in the lizards Varanus gouldii and Sauromalus hispidus. Journal of Comparative Physiology 79:259–280.CrossRefGoogle Scholar
Bennett, A. F. 1973. Ventilation in two species of lizards during rest and activity. Comparative Biochemistry and Physiology 46A:653–671.CrossRefGoogle Scholar
Bennett, A. F., and Dawson, W. R. 1976. Metabolism. Pp. 127–223In Gans, C. and Dawson, W. R., eds. Biology of the reptilia, vol. 5. Academic Press, London.Google Scholar
Bennett, A. F., and Ruben, J. A. 1979. Endothermy and activity in vertebrates. Science (Washington, D.C.) 206:649–654.CrossRefGoogle ScholarPubMed
Bennett, A. F., and Ruben, J. A. 1986. The metabolic and thermoregulatory status of therapsids. Pp. 207–218in Hotton et al. 1986.Google Scholar
Berger, M., Hart, J. S., and Roy, O. Z. 1971. Respiratory water and heat loss of the black duck during flight at different ambient temperatures. Canadian Journal of Zoology 49:767–774.CrossRefGoogle ScholarPubMed
Bernstein, M. H., and Schmidt-Nielsen, K. 1974. Ventilation and oxygen extraction in the crow. Respiration Physiology 21:393–401.CrossRefGoogle ScholarPubMed
Bintz, G. L., and Roesbery, H. W. 1978. Evaporative water loss by control and starved laboratory rats and Spermophilus richardsoni. Comparative Biochemistry and Physiology 59A:275–278.CrossRefGoogle Scholar
Blix, A. S., and Johnsen, H. K. 1983. Aspects of heat exchange in resting reindeer. Journal of Physiology 340:445–454.CrossRefGoogle ScholarPubMed
Brink, A. S. 1956. Speculations on some advanced mammalian characteristics in the higher mammal-like reptiles. Paleontologia Africana 4:77–95.Google Scholar
Broom, R. 1926. On the organ of Jacobson and some other structures in the nose of Caenolestes. Proceedings of the Zoological Society (London) 1926:419–424.Google Scholar
Caputa, M. 1979. Temperature gradients in the nasal cavity of the rabbit. Journal of Thermal Biology 4:283–286.CrossRefGoogle Scholar
Caputo, M. V., and Crowell, J. C. 1985. Migration of glacial centers across Gondwana during the Paleozoic Era. Geological Society of America Bulletin 96:1020–1036.2.0.CO;2>CrossRefGoogle Scholar
Carroll, R. L. 1988. Vertebrate paleontology and evolution. W. H. Freeman, New York.Google Scholar
Colbert, E. H. 1986. Therapsids in Pangaea and their contemporaries and competitors. Pp. 133–145in Hotton et al. 1986.Google Scholar
Cole, P. 1953. Further observations on the conditioning of respiratory air. Journal of Laryngology and Otology 67:669–681.CrossRefGoogle ScholarPubMed
Collins, J. C., Pilkington, T. C., and Schmidt-Nielsen, K. 1971. A model of respiratory heat transfer in a small mammal. Biophysical Journal 11:886–914.CrossRefGoogle Scholar
Condie, K. C. 1982. Plate tectonics and crustal evolution, 2d ed. Pergamon Press, New York.Google Scholar
Crompton, A. W., and Jenkins, F. A. Jr. 1979. Origin of mammals. Pp. 59–73In Lillegraven, J. A., Kielan-Jaworowska, Z., and Clemens, W. A., eds. Mesozoic mammals, the first two-thirds of mammalian history. University of California Press, Berkeley.Google Scholar
Crowley, T. J., Hyde, W. T., and Short, D. H. 1989. Seasonal cycle variations on the supercontinent of Pangaea. Geology 17:257–260.2.3.CO;2>CrossRefGoogle Scholar
Dawson, T. J., and Hulbert, A. J. 1970. Standard metabolism, body temperature and surface areas of Australian marsupials. American Journal of Physiology 218:1233–1238.CrossRefGoogle ScholarPubMed
Depocas, F. J., and Hart, J. S. 1957. Use of the Pauling oxygen analyzer for measurement of oxygen consumption in open circuit systems and in a short-lag, closed circuit apparatus. Journal of Applied Physiology 10:388–392.CrossRefGoogle Scholar
Edwards, R. M., and Haines, H. 1978. Effects of water vapor pressure and temperature on evaporative water loss in Peromyscus maniculatus and Mus musculus. Journal of Comparative Physiology 128:177–184.CrossRefGoogle Scholar
Folkow, L. P., and Blix, A. S. 1987. Nasal heat exchange in gray seals. American Journal of Physiology 253:R883-R889.Google ScholarPubMed
Fourie, S. 1974. The cranial morphology of Thrinaxodon liorhinus Seeley. Annals of the South African Museum 65:337–400.Google Scholar
Getz, L. L. 1968. Relationships between ambient temperature and respiratory water loss of small mammals. Comparative Biochemistry and Physiology 24:335–342.CrossRefGoogle ScholarPubMed
Guyton, A. C. 1991. Textbook of medical physiology, 8th ed.Saunders, Philadelphia.Google Scholar
Hill, R. W. 1978. Exhalant air temperatures in the Virginia opossum. Journal of Thermal Biology 3:219–221.CrossRefGoogle Scholar
Hopson, J. A. 1969. The origin and adaptive radiation of mammal-like reptiles and non-therian mammals. Annals of the New York Academy of Sciences 167:199–216.CrossRefGoogle Scholar
Hotton, N., MacLean, P. D., Roth, J. J., and Roth, E. C., eds. 1986. The ecology and biology of mammal-like reptiles. Smithsonian Institution Press, Washington, D.C.Google Scholar
Huey, R. B. 1982. Temperature, physiology, and the ecology of reptiles. Pp. 25–91In Gans, C. and Pough, F. H., eds. Biology of the reptilia, vol. 12. Academic Press, London.Google Scholar
Huey, R. B., and Slatkin, M. 1976. Cost and benefits of lizard thermoregulation. Quarterly Review of Biology 51:363–384.CrossRefGoogle ScholarPubMed
Hulbert, A. J. 1980. The evolution of energy metabolism in mammals. Pp. 129–139In Schmidt-Nielsen, K., Bolis, L., Taylor, C. R., Bentley, P. J., and Stevens, C. E., eds. Comparative physiology: primitive mammals. Cambridge University Press, Cambridge.Google Scholar
Huntley, A. C., Costa, D. P., and Rubin, R. D. 1984. The contribution of countercurrent heat exchange to water balance in the northern elephant seal. Journal of Experimental Biology 113:447–454.CrossRefGoogle ScholarPubMed
Ingelstedt, S. 1956. Studies on the conditioning of air in the respiratory tract. Acta Oto-Laryngologica 131(suppl.):1–79.Google ScholarPubMed
Jackson, D. C., and Schmidt-Nielsen, K. 1964. Countercurrent heat exchange in the respiratory passages. Proceedings of the National Academy of Sciences, USA 51:1192–1197.CrossRefGoogle ScholarPubMed
Jenkins, F. A. Jr. 1970. Cynodont postcranial anatomy and the “prototherian” level of mammalian organization. Evolution 24:230–252.Google ScholarPubMed
Jenkins, F. A. Jr. 1990. Monotremes and the biology of Mesozoic mammals. Netherlands Journal of Zoology 40:5–31.CrossRefGoogle Scholar
Johnsen, H. K., Blix, A. S., Mercer, J. B., and Bolz, K. D. 1987. Selective cooling of the brain in reindeer. American Journal of Physiology 253:R848-R853.Google ScholarPubMed
Kamau, J.M.Z., Maina, J. N., and Maloiy, G.M.O. 1984. The design and the role of the nasal passages in the temperature regulation in the dik-dik antelope (Rhynchotragus kirkii) with observations on the carotid rete. Respiration Physiology 56:183–194.CrossRefGoogle ScholarPubMed
Kemp, T. S. 1969. On the functional morphology of the gorgonopsid skull. Philosophical Transactions of the Royal Society of London B256:1–83.Google Scholar
Kemp, T. S. 1979. The primitive cynodont Procynosuchus: functional anatomy of the skull and relationships. Philosophical Transactions of the Royal Society of London B285:73–122.Google Scholar
Kemp, T. S. 1980. Aspects of the structure and functional anatomy of the Middle Triassic cynodont Luangwa. Journal of Zoology, London 191:193–239.CrossRefGoogle Scholar
Kemp, T. S. 1982. Mammal-like reptiles and the origin of mammals. Academic Press, London.Google Scholar
Kermack, K. A., Mussett, F., and Rigney, H. W. 1981. The skull of Morganucodon. Zoological Journal of the Linnean Society 71:1–158.CrossRefGoogle Scholar
Kutzbach, J. E., and Gallimore, R. G. 1989. Pangaean climates: megamonsoons on the megacontinent. Journal of Geophysical Research 94(D3):3341–3357.CrossRefGoogle Scholar
Langman, V. A. 1985. Nasal heat exchange in a northern ungulate, the reindeer (Rangifer tarandus). Respiration Physiology 59:279–287.CrossRefGoogle Scholar
Langman, V. A., Maloiy, G.M.O., Schmidt-Nielsen, K., and Schroter, R. C. 1978. Respiratory water and heat loss in camels subjected to dehydration. Journal of Physiology 278:35P.Google ScholarPubMed
Langman, V. A., Maloiy, G.M.O., Schmidt-Nielsen, K., and Schroter, R. C. 1979. Nasal heat exchange in the giraffe and other large mammals. Respiration Physiology 37:325–333.CrossRefGoogle ScholarPubMed
Lasiewski, R. C., and Calder, W. A. 1971. A preliminary allometric analysis of respiratory variables in resting birds. Respiration Physiology 11:152–166.CrossRefGoogle ScholarPubMed
Lasiewski, R. C., Acosta, A. L., and Bernstein, M. H. 1966. Evaporative water loss in birds. I. Characteristics of the open flow method of determination, and their relation to estimates of thermoregulatory ability. Comparative Biochemistry and Physiology 19:445–457.Google Scholar
Macmillen, R. E. 1972. Water economy of nocturnal desert rodents. Pp. 147–174in Maloiy, G.M.O., ed. Comparative physiology of desert animals. Symposia of the Zoological Society of London. 31.Google Scholar
Macmillen, R. E., and Hinds, D. S. 1983. Water regulatory efficiency in heteromyid rodents: a model and its application. Ecology 64:152–164.CrossRefGoogle Scholar
Miao, D. 1988. Skull morphology of Lambdopsalis bulla (Mammalia, Multituberculata) and its implications to mammalian evolution. University of Wyoming, Contributions to Geology, Special Paper 4.Google Scholar
Moore, W. J. 1981. The mammalian skull. Cambridge University Press, Cambridge.Google Scholar
Murrish, D. E. 1973. Respiratory heat and water exchange in penguins. Respiration Physiology 19:262–270.CrossRefGoogle ScholarPubMed
Murrish, D. E., and Schmidt-Nielsen, K. 1970. Exhaled air temperature and water conservation in lizards. Respiration Physiology 10:151–158.CrossRefGoogle ScholarPubMed
Negus, V. 1958. Comparative anatomy and physiology of the nose and paranasal sinuses. F. and S. Livingstone, Edinburgh.Google Scholar
Parrish, J. M., Parrish, J. T., and Ziegler, A. M. 1986. Permian-Triassic paleogeography and paleoclimatology and implications for therapsid distribution. Pp. 109–131in Hotton et al. 1986.Google Scholar
Parsons, T. S. 1967. Evolution of the nasal structure in the lower tetrapods. American Zoologist 7:397–413.CrossRefGoogle Scholar
Piiper, J. 1989. Gas-exchange efficiency of fish gills and bird lungs. Pp. 159–171In Paganelli, C. V. and Farhi, L. E., eds. Physiological function in special environments. Springer, Berlin.CrossRefGoogle Scholar
Proctor, D. F., Andersen, I., and Lundqvist, G. R. 1977. Human nasal mucosal function at controlled temperatures. Respiration Physiology 30:109–124.CrossRefGoogle ScholarPubMed
Robinson, P. L. 1973. Palaeoclimatology and continental drift. Pp. 451–476In Tarling, D. H. and Runcorn, S. K., eds. Implications of Continental Drift to earth sciences, vol. 1. Academic Press, New York.Google Scholar
Romer, A. S., and Parsons, T. S. 1986. The vertebrate body, 6th ed.Saunders College, Philadelphia.Google Scholar
Schmid, W. D. 1976. Temperature gradients in the nasal passage of some small mammals. Comparative Biochemistry and Physiology 54A:305–308.CrossRefGoogle Scholar
Schmidt-Nielsen, K. 1964. Desert animals. Oxford University Press, Oxford.Google Scholar
Schmidt-Nielsen, K. 1969. The neglected interface: the biology of water as a liquid-gas system. Quarterly Review of Biophysiology 2:283–304.CrossRefGoogle ScholarPubMed
Schmidt-Nielsen, K. 1970. Energy metabolism, body size and problems of scaling. Federation Proceedings 29:1524–1532.Google ScholarPubMed
Schmidt-Nielsen, K. 1972a. How animals work. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Schmidt-Nielsen, K. 1972b. Recent advances in the comparative physiology of desert animals. Pp. 371–382in Maloiy, G.M.O., ed. Comparative physiology of desert animals. Symposia of the Zoological Society of London. 31.Google Scholar
Schmidt-Nielsen, K. 1981. Countercurrent systems in animals. Scientific American 244:118–128.CrossRefGoogle ScholarPubMed
Schmidt-Nielsen, K. 1984. Scaling. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Schmidt-Nielsen, K. 1990. Animal physiology; adaptation and environment, 4th ed.Cambridge University Press, Cambridge.Google Scholar
Schmidt-Nielsen, K., Bretz, W. L., and Taylor, C. R. 1970a. Panting in dogs: unidirectional air flow over evaporative surfaces. Science (Washington, D.C.) 169:1102–1104.CrossRefGoogle ScholarPubMed
Schmidt-Nielsen, K., Hainsworth, F. R., and Murrish, D. E. 1970b. Counter-current heat exchange in the respiratory passages: effect on water and heat balance. Respiration Physiology 9:263–276.CrossRefGoogle ScholarPubMed
Schmidt-Nielsen, K., Schroter, R. C., and Shkolnik, A. 1981. Desaturation of exhaled air in camels. Proceedings of the Royal Society of London B211:305–319.Google Scholar
Schroter, R. C., and Watkins, N. V. 1989. Respiratory heat exchange in mammals. Respiration Physiology 78:357–368.CrossRefGoogle ScholarPubMed
Schroter, R. C., Robertshaw, D., Baker, M. A., Shoemaker, V. H., Holmes, R., and Schmidt-Nielsen, K. 1987. Respiration in heat stressed camels. Respiration Physiology 70:97–112.CrossRefGoogle ScholarPubMed
Schroter, R. C., Robertshaw, D., and Zine Filali, R. 1989. Brain cooling and respiratory heat exchange in camels during rest and exercise. Respiration Physiology 78:95–105.CrossRefGoogle ScholarPubMed
Stahl, W. R. 1967. Scaling of respiratory variables in mammals. Journal of Applied Physiology 22:453–460.CrossRefGoogle ScholarPubMed
Szalay, F. S. 1990. Evolution of the tarsal complex in Mesozoic mammals. Journal of Vertebrate Paleontology 10(suppl. to no. 3):45A.Google Scholar
Taylor, C. R., and Lyman, C. P. 1972. Heat storage in running antelopes: independence of brain and body temperatures. American Journal of Physiology 222:114–117.CrossRefGoogle ScholarPubMed
Thomason, J. J., and Russell, A. P. 1986. Mechanical factors in the evolution of the mammalian secondary palate: a theoretical analysis. Journal of Morphology 189:199–213.CrossRefGoogle ScholarPubMed
Tracy, C. R. 1982. Biophysical modeling in reptilian physiology and ecology. Pp. 275–314In Gans, C. and Pough, F. H., eds. Biology of the reptilia, vol. 12. Academic Press, London.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 et al. 1986.Google Scholar
Verzar, F., Keith, J., and Parchet, V. 1953. Temperatur und Feuchtigheit der Luft in den Atemwegen. Pflueger's Archiv fuer die gesamte Physiologie 257:400–416.CrossRefGoogle Scholar
Walker, J.E.C., Wells, R. E., and Merrill, E. W. 1961. Heat and water exchange in the respiratory tract. American Journal of Medicine 30:259–267.CrossRefGoogle ScholarPubMed
Watson, D.M.S. 1913. Further notes on the skull, brain and organs of special sense of Diademodon. Annals and Magazine of Natural History. Ser. 8. 12:217–228.CrossRefGoogle Scholar
Watson, D.M.S. 1931. On the skeleton of a bauriamorph reptile. Proceedings of the Zoological Society of London 1931:1163–1205.CrossRefGoogle Scholar
Welch, W. R. 1984. Temperature and humidity of expired air: interspecific comparisons and significance for loss of respiratory heat and water from endotherms. Physiological Zoology 57:366–375.CrossRefGoogle Scholar
Withers, P. C., Casey, T. M., and Casey, K. K. 1979a. Allometry of respiratory and haematological parameters of arctic mammals. Comparative Biochemistry and Physiology 64A:343–350.CrossRefGoogle Scholar
Withers, P. C., Lee, A. K., and Martin, R. W. 1979b. Metabolism, respiration and evaporative water loss in the Australian hopping-mouse Notomys alexis (Rodentia: Muridae). Australian Journal of Zoology 27:195–204.CrossRefGoogle Scholar