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Origin and development of homoiothermy: A case study of avian energetics

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DOI: 10.4236/abb.2013.48A1001    4,064 Downloads   6,209 Views   Citations

ABSTRACT

The study is based on the results of the integrated measurement of the energy expenditure at rest and common activity in birds belonging to various systematic groups. Homeothermy has formed in birds and mammals independently and in different geological ages. However, in both groups it originated as a side effect of selection for aerobic metabolism improvement that provided a higher level of activity. Advantages of having high and stable body temperature, which were inevitably related with metabolism intensification, led to development of thermoregulatory adaptations such as fur and feathers. This made it possible to retain the metabolically generated heat and reduce heat absorption in hot environments. Emergence of homeothermy with aerobic supply of motion activity, possibilities to regulate the level of metabolism and thermal conductance, has opened a lot of opportunities for homoeothermic animals. Achieving such a level of energy utilization allowed them to maintain activity for a longer time, while its sensory support led to complication and diversification of birds’ behavioral repertoire (as well as that of mammals) facilitating the conquest of almost entire part of the biosphere that was suitable for living. This process was favored by the development of nurturing and passing on the information, collected throughout the life, to new generations. Formation of high levels of aerobic metabolism in birds and mammals was proceeding in parallel among different groups of reptilian ancestors. The level of homeothermy, at which aerobic metabolism was able to maintain prolonged activity, developed in birds and mammals in different ways: they had got dissimilar partitioning of venous and arterial networks, erythrocytes with or without a cell nucleus, different lungs design—but, at that, similar minimum metabolic power and rather close body temperatures which corresponded well to the environmental conditions on the Earth. Natural selection allowed animals with high energetic metabolism to increase their diversity and abundance, but only when homoeothermic animals could satisfy their demands for food resources, that had risen manifold. That happened in the middle of Cretaceous, in time with the appearance of angiosperms and expansion of related fauna of invertebrates.

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Gavrilov, V. (2013) Origin and development of homoiothermy: A case study of avian energetics. Advances in Bioscience and Biotechnology, 4, 1-17. doi: 10.4236/abb.2013.48A1001.

References

[1] Scholander, P.F., Hock, R., Walters, V. and Irving, L. (1950) Adaptation to cold in arctic and tropical mammals and birds in relation to body temperature insulation, and basal metabolic rate. Biological Bulletin, 99, 259-271. doi:10.2307/1538742
[2] Gavrilov, V.M. (2006) Environmental, physiological and thermodynamic prerequisites and consequences of homeothermy in birds. The Development of Modern Ornithology in Northern Eurasia: Proceedings of XII International Ornithology Conference of North Eurasia, Izd. Stavropol, 76-95.
[3] Gavrilov, V.M. (1997) Energetics and avian behavior. In: Turpaev, T.M., Ed., Physioogy and General Biology Reviews, Harwood Academy Publication GmbH, Amsterdam.
[4] Hemmingsen, A.M. (1960) Energy metabolism as related to body size and respiratory surface, and its evolution. Report of Steno Memorial Hospital (Copenhagen), 9, 1-110.
[5] Peters, P. (1983) Ecological implication of body size. Harvard University Press, Cambridge. doi:10.1017/CBO9780511608551
[6] Dolnik, V.R. (1995) Time and energy resources in birds in nature. Nauka, St. Petersburg.
[7] Darveau, C.A., Suarez, R.K., Andrews, R.D. and Hochachka, P.W. (2002) Allometric cascade as a unifying principle of body mass effects on metabolism. Nature, 417, 166-170. doi:10.1038/417166a
[8] Else, P.L., Turner, N. and Hulbert, A.J. (2004) The evolution of endothermy: Role for membranes and molecular activity. Physiological and Biochemical Zoology, 77, 950-958. doi:10.1086/422767
[9] Bennett, A.F. and Ruben, J.A. (1979) Endothermy and activity in vertebrates. Science, 206, 649-654. doi:10.1126/science.493968
[10] Bennett, A.F., Hicks, J.W. and Cullum, A.J. (2000) An experimental test of the thermoregulatory hypothesis for the evolution of endothermy. Evolution, 54, 1768-1773.
[11] Dolnik, V.R. (2003) Origin of homoiothermy: An unsolved problem. Zhurnal Obshchei Biologii, 64, 451-462.
[12] Bennett, A.F. (1976) Metabolism. In: Gens, C. and Dawson, W.R., Eds., Biology of the Reptilians, Academic Press, New York, 127-223.
[13] O’Conner, M.P. and Dodson, P. (1999) Biophysical constraints on the thermal ecology of dinosaurs. Paleobiology, 25, 341-346.
[14] Gillooly, J.F., Allen, A.P. and Charnov, E.L. (2006) Dinosaur fossils predict body temperatures. PLOS Biology, 4, 248-254. doi:10.1371/journal.pbio.0040248
[15] Barrick, R.E. and Showers, W.J. (1994) Thermophysiology of tyrannosaurus rex: Evidence from oxygen isotopes, Science, 265, 222-224. doi:10.1126/science.265.5169.222
[16] Fricke, H.C. and Rogers, R.R. (2000) Multiple taxon— Multiple locality approach to providing oxygen isotope evidence for warm-blooded theropod dinosaurs, Geology, 28, 799-802. doi:10.1130/0091-7613(2000)28<799:MTLATP>2.0.CO;2
[17] Seebacher, F. (2003) Dinosaur body temperatures: The occurrence of endothermy and ectothermy. Paleobiology, 29, 105-122. doi:10.1666/0094-8373(2003)029<0105:DBTTOO>2.0.CO;2
[18] Amiot, R., Wang, X., Zhou, Z., Wang, X., Buffetaut, E., Lecuyer, C., Ding, Z., Fluteau, F., Hibino, T., Kusuhashi, N., Mo, J., Suteethorn, V., Wang, Y., Xu, X. and Zhang, F. (2006) Oxygen isotopes from biogenic apatites suggest widespread endothermy in Cretaceous Dinosaurs. Earth Planet. Science Letters, 246, 41-48. doi:10.1016/j.epsl.2006.04.018
[19] Eagle, R.A., Tutken, T., Martin, T.S., Tripati, A.K., Fricke, H.C., Connely, M., Cifelli, R.L. and Eiler, J.M. (2010) Body temperatures of modern and extinct vertebrates from 13c-18o bond abundances in bioapatite. Proceedings of the National Academy of Sciences of USA, 107, 10377-10382. doi:10.1073/pnas.0911115107
[20] Eagle, R.A., Tutken, T., Martin, T.S., Tripati, A.K., Fricke, H.C., Connely, M., Cifelli, R.L. and Eiler, J.M. (2011) Dinosaur body temperatures determined from isotopic (13c-18o) ordering in fossil biominerals. Science, 333, 443-445. doi:10.1126/science.1206196
[21] McNab, B.K. (2009) Resources and energetics determined dinosaur maximal size. Proceedings of the National Academy of Sciences of USA, 106, 1-5. doi:10.1073/pnas.0904000106
[22] Pierson, D. (2009) The physiology of dinosaurs: Circulatory and respiratory function in the largest animals ever to walk the earth. Respiratory Care, 54, 887-911. doi:10.4187/002013209793800286
[23] Bennett, A.F. (1994) Exercise performance of reptiles. Advances in Veterinary Science and Comparative Medicine, 38B, 113-138.
[24] Bennett, A.F. and Lenski, R.E. (1999) Experimental evolution and its role in evolutionary physiology. American Zoologist, 39, 346-362.
[25] Bennett, A.F., Hicks, J.W. and Cullum, A.J. (2000) An experimental test of the thermoregulatory hypothesis for the evolution of endothermy. Evolution, 54, 1768-1773.
[26] Hicks, J.W., Wang, T. and Bennett, A.F. (2000) Patterns of cardiovascular and ventilatory response to elevated metabolic states in the lizard Varanus exanthematicus. Journal of Experimental Biology, 203, 2437-2445.
[27] Dolnik, V.R. (1998) The hypothesis of “warm-blooded” dinosaurs in the light of the energetics of modern animals. Uspekhi Sovremennoi Biologii, 118, 661-678.
[28] Dolnik, V.R. (1999) Allometric “arrangement” of reptile energetics. Zoologicheskii Zhurnal, 78, 1330-1339.
[29] Dolnik, V.R. (1999) Reconstruction of pterosaur energetics basing on the data on modern species energetics. Zhurnal Obshchei Biologii, 60, 359-375.
[30] Dolnik, V.R. (2002) Normal metabolism in vertebrates: What causes the differences between poikilothermic and homoiothermal classes? Zoologicheskii Zhurnal, 82, 643-654.
[31] Seymour, R.S., Smith, S.L., White, C.R., Henderson, D.M. and Schwarz-Wings, D. (2011) Blood flow to long bones indicates activity metabolism in mammals, reptiles and dinosaurs. Proceedings of the Royal Society B, 0968.
[32] Gavrilov, V.M. (1995) Maximum, potentially productive, and normal metabolic levels of existence of passerines and non-passerine birds. 1. Dependence on the temperature of the environment, the relationship with the body weight, seasonal variations, and the relationship with other levels of energy consumption. Zoologicheskii Zhurnal, 74, 102-122.
[33] Gavrilov, V.M. (1995) Maximum, potentially productive, and normal metabolic levels of existence of passerines and non-passerine birds. 2. Relationship with the external work: Energy and environmental consequences. Zoologicheskii Zhurnal, 74, 108-123.
[34] Gavrilov, V.M. (1996) Basal metabolism of homoiothermal animals. 1. Power ratings and fundamental characteristic of energetics. Zhurnal Obshchei Biologii, 57, 325-345.
[35] Gavrilov, V.M. (1996) Basal metabolism of homoiothermal animals. 2. The emergence in evolution, energy and environmental consequences. Zhurnal Obshchei Biologii, 57, 421-439.
[36] Gavrilov, V.M. (2000) How differences in basal metabolism affect energy expenditure on self-maintenance and energy efficiency in passeriformes and non-passeriformes. Doklady Biological Sciences, 371, 152-155.
[37] Gavrilov, V.M. (2000) What determines the mass-exponent factor of 3/4 in the allometric equations of basal metabolism in homoiothermal animals? Doklady Biological Sciences, 371, 172-175.
[38] Gavrilov, V.M. (2013) Ecological, functional, and thermodynamic prerequisites and consequences of the origin and development of homoiothermy: A case study of avian energetics. Biology Bulletin Reviews, 3, 27-48. doi:10.1134/S2079086413010040
[39] Zherikhin, V.V. (1978) Razvitie i smena melovykh i kainozoiskikh faunisticheskikh kompleksov (trakheinye i khelitserovye) (The development and change of the cretaceous and cenozoic faunal assemblages (tracheata and chelicerata). Trudy PIN AN SSSR, 165, 189-223.
[40] Rautian, A.S. and Zherikhin, V.V. (1997) Models of phylocenogenesis and the lessons of environmental crises of the geological past. Zhurnal Obshchei Biologii, 58, 20-47.
[41] Zherikhin, V.V. and Rautian, A.S. (2000) Crises in the biological evolution. Nauka, Moscow.
[42] Gavrilov, V.M. (2011) Energy expenditures for flight, aerodynamic quality, and colonization of forest habitats by birds. Biology Bulletin, 38, 779-788. doi:10.1134/S1062359011080024
[43] Gavrilov, V.M. (2012) The fundamental avian energetics: 2. The ability of birds to change heat loss and explanation of the mass exponent for basal metabolism in homeothermic animals. Biology Bulletin, 39, 659-671.
[44] Gavrilov, V.M. (1994) General consistent patterns of the effect of temperature on the energetics of a homoiothermal animal (a case study of the great tit Parus major, Passeriformes, Aves). Doklady Akademii Nauk, 334, 121-126.
[45] Gavrilov, V.M. (2001) Thermoregulation energetics of passerine and non-passerine birds. Ornitologiya, 29, 162-182.
[46] Gavrilov, V.M. (2004) Comparative energetics of passerine and non-passerine birds: Size limits, energetic capacity, and environmental consequences. Ornitologiya, 31, 92-107.
[47] Suarez, R.K. (1996) Upper limits to mass-specific metabolic rates. Annual Review of Physiology, 58, 583-590. doi:10.1146/annurev.ph.58.030196.003055
[48] Brody, G. (1945) Bioenergetics and growth. Reinhold, New York.
[49] Dolnik, V.R. (1969) Bioenergetics of a flying bird. Zhurnal Obshchei Biologii, 30, 273-291.
[50] Kirkwood, J.K. (1983) A limit to metabolisable energy intake in mammals and birds. Part A: Physiology, 75, 1-3. doi:10.1016/0300-9629(83)90033-6
[51] Hoppeler, H. and Weibel, E.R. (2005) Scaling functions to body size: Theories and facts. The Journal of Experimental Biology, 208, 1573-1574. doi:10.1242/jeb.01630
[52] Gavrilov, V.M. and Dolnik, V.R. (1985) Basal metabolic rate, thermoregulation and existence energy in birds: World data. Acta XVIII Congressus Internationalis Ornithologici, 1, 421-466.
[53] Yanshin, A.L. (1997) How the air composition changes? Vestnik Rossiiskoi Akademii Meditsinskikh Nauk, 67, 108-113.
[54] Ivanov, V.D. (2000) Cretaceous biocenotic crisis. Soros. Obrazovat. Zhurnal, 6, 69-75.
[55] Golubeva, T.B. (1997) Type of ontogeny and species-specific stimulation in the development of auditory sensitivity in birds. Physiology and General Biology Revue, 12, 1-106.
[56] Stark, J.M. and Ricklefs, R.E. (1998) Patterns of development: The altricial-precocial spectrum. Oxford University Press, Oxford.
[57] Iordanskii, N.N. (2001) Evolyutsiya zhizni (Evolution of life). Akademiya, Moscow.
[58] Budyko, M.I. (1982) Izmeneniya okruzhayushchei sredy i smeny posledovatel’nykh faun (Environmental changes and consecutive fauna succession). Gidrometeoizdat, Leningrad.
[59] Krasilov, V.A. (1985) Melovoi period. Evolyutsiya zemnoi kory i biosfery (Cretaceous period. The evolution of the earth’s crust and the biosphere). Nauka, Moscow.
[60] Zherikhin, V.V. (1984) Ecological crisis—A precedent in the Mesozoic. Energiya, 1, 54-61.
[61] Ivakhnenko, M.F., Golubev, V.K., Gubin, Y.M., Kalandadze, N.N., Novikov, I.V., Sennikov, A.G. and Rautian, A.S. (1997) Permian and triassic tetrapods of eastern Europe. Trudy Paleontological Institute, 268, 216.
[62] Lopatin A.V. (2004) Early miocene small mammals from the north Aral Region (Kazakhstan) with special reference to their biostratigraphic significance. Paleontologicheskii Zhurnal, 38, 217-323.
[63] Falkowski, P.G., Katz, M.E., Milligan, A.J., Fennel, K., Cramer, B.S., Aubr, M.P., Berner, R.A., Novacek, M.J., and Zapo, W.M. (2005) The rise of oxygen over the past 205 million years and the evolution of large placental mammals. Science, 309, 2202-2204. doi:10.1126/science.1116047
[64] Wible, J.R., Rougier, G.W., Novacek, M.J. and Asher, R.J. (2007) Cretaceous eutherians and laurasian origin for placental mammals near K/T boundary. Nature, 447, 1003-1006.
[65] Agadjanian, A.K. (1996) Models of phytohagy in mammals. Paleontological Journal, 30, 723-729.
[66] Rasnitsyn, A.P. (1988) The problem of global crisis of terrestrial biocenoses in the middle cretaceous. Nauka, Moscow.
[67] Ponomarenko, A.G. (1993) The key events in the evolution of the biosphere. Nauka, Moscow.
[68] Krasilov, V.A. (1985) Melovoi period. Evolyutsiya zemnoi kory i biosfery (Cretaceous period. The evolution of the earth’s crust and the biosphere). Nauka, Moscow.
[69] Zherikhin, V.V. (2003) Izbrannye trudy po paleoekologii i filotsenogenetike (Selected papers on paleoecology and phylocenogenetics). Tovar. Nauch. Izd. KMK, Moscow.
[70] Gorshkov, V.G. (1985) Stability of biogeochemical cycles. Ekologiya, 2, 3-12.
[71] Perfilova, O.Y. and Makhlaev, M.L. (2009) Geokhimiya biosfery (Geochemistry of the biosphere). Krasnoyarsk Federal University, Krasnoyarsk.
[72] Ponomarenko, A.G. (1998) Paleontology and balances of biogeochemical turnovers. In: Ponomarenko, A.G., Rosanov, A.Yu. and Fedonkin, M.A., Eds., Ecosystem Reorganizations and Evolution of the Biosphere, PIN, Moscow, 9-14.
[73] Plotnikov, V.V. (1979) Evolyutsiya struktury rastitel’nykh soobshchestv (Evolution of the structure of plant communities). Nauka, Moscow.
[74] Eskov, K.Y. (1999) Istoriya zemli i zhizni na nei (The history of the earth and life on it). MIROS, Moscow.
[75] Nagy, K.A. (2005) Field metabolic rate and body size. The Journal of Experimental Biology, 208, 1621-1625. doi:10.1242/jeb.01553
[76] Tatarinov, L.P. (1976) Morfologicheskaya evolyutsiya teriodontov i obshchie voprosy filogenetiki (Morphological evolution of theriodonts and general problems of phylogenetics). Nauka, Moscow.
[77] Kurochkin, E.N. (2006) Parallel evolution of theropod dinosaurs and birds. Journal of. Zoology, 85, 283-298.
[78] Kurochkin, E.N. (2001) Novye idei o proiskhozhdenii i rannei evolyutsii ptits. Dostizheniya i problemy ornitologii severnoi evrazii na rubezhe vekov (New ideas on the origin and early evolution of birds. Advances and challenges in ornithology in northern Eurasia at the turn of the century). Kazan State University, Kazan.
[79] Kurochkin, E.N. and Bogdanovich, I.A. (2008) On the origin of avian flight: Compromise and system approaches. Biology Bulletin, 35, 1-11. doi:10.1134/S1062359008010019
[80] Unwin, D.M. (2003) On the phylogeny and evolutionary history of pterosaurs. In: Buffetaut, E. and Mazin, J.-M., Eds., Evolution and Palaeobiology of Pterosaurs, Geological Society, London, 139-190.
[81] Lu, J.C., Azuma, Y., Dong, Z.M., Barsbold, R., Kobayashi, Y. and Lee, Y.N. (2009) New material of dsungaripterid pterosaurs (Reptilia: Pterosauria) from Western Mongolia and its palaeoecological implications. Geological Magazine, 146, 690-700. doi:10.1017/S0016756809006414
[82] Unwin, D.M. and Bakhurina, N.N. (2003) The age of dinosaurs in Russia and Mongolia. Cambridge University Press, Cambridge.
[83] Lu, J., Unwin, D.M., Jin, X., Liu, Y. and Ji, Q. (2010) Evidence for modular evolution in a long-tailed pterosaur with a pterodactyloid skull. Proceedings of the Royal Society B, 277, 383-389. doi:10.1098/rspb.2009.1603
[84] Severtsov, A.S., Kreslavskii, A.G. and Cherdantsev, V.G. (1993) Tri mekhanizma evolyutsii. Sovremennye problemy teorii evolyutsii (Three mechanisms of evolution. Modern problems of the theory of evolution). Nauka, Moscow.
[85] Zherikhin, V.V. (1980) Insects in terrestrial ecosystems: The historical development of the insect class. Trudy PIN AN SSSR, 75, 189-223.
[86] Gavrilov, V.M. (1999) Ecological phenomena of passeriformes as a derivative of their energetic. Acta Ornithologica, 34, 165-172.
[87] Nagy, K.A., Gavrilov, V.M., Kerimov, A.B. and Ivankina, E.V. (1999) Relationships between field metabolic rate, basal metabolic rate and territoriality in passerines. Proceedings of the 22nd International Ornithological Congress, University of Natal, Durban, 390-400.
[88] Gavrilov, V.M., Kerimov, A.B., Golubeva, T.B., Ivankina, E.V., Ilina, T.A., Karelin, D.V. and Kolyaskin, V.V. (1996) Energetics, morphophysiological heterogeneity of individuals, and the population structure in birds. 1. Energetics, morphophysiological heterogeneity, and population structure in the great tits in Moscow Oblast. Ornitologiya, 27, 34-73.
[89] Gavrilov, V.M., Kerimov, A.B., Aleksandrov, L.I., Golubeva, T.B., Ivankina, E.V., Ilina, T.A. and Shishkin, V.S. (1996) Energetics, morphophysiological heterogeneity of individuals, and the population structure in birds. 2. Energy, morphophysiological heterogeneity of individuals, and population structure in flycatchers. Ornitologiya, 27, 74-97.
[90] Bennett, A.F. (1991) The evolution of activity capacity. The Journal of Experimental Biology, 160, 1-23.
[91] Varricchio, D., Martin, A. and Katsura, Y. (2007) First trace and body fossil evidence of a burrowing, denning dinosaur. Proceedings of the Royal Society B: Biological Sciences, 274, 1361-1368.

  
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