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Unformatted text preview: Annu. Rev. Physiol. 2000. 62:135–55 Copyright q by Annual Reviews. All rights reserved 0066–4278/00/0315–0135$12.00 135 T HE E VOLUTIONARY P HYSIOLOGY OF A NIMAL F LIGHT : Paleobiological and Present Perspectives Robert Dudley Section of Integrative Biology, University of Texas, Austin, Texas, 78712 and Smithsonian Tropical Research Institute, P.O. Box 2072, Balboa, Republic of Panama; e-mail: [email protected] Key Words evolution, gigantism, hyperoxia, insect, oxygen Abstract Recent geophysical analyses suggest the presence of a late Paleozoic oxygen pulse beginning in the late Devonian and continuing through to the late Car- boniferous. During this period, plant terrestrialization and global carbon deposition resulted in a dramatic increase in atmospheric oxygen levels, ultimately yielding con- centrations potentially as high as 35% relative to the contemporary value of 21%. Such hyperoxia of the late Paleozoic atmosphere may have physiologically facilitated the initial evolution of insect flight metabolism. Widespread gigantism in late Paleo- zoic insects and other arthropods is also consistent with enhanced oxygen flux within diffusion-limited tracheal systems. Because total atmospheric pressure increases with increased oxygen partial pressure, concurrently hyperdense conditions would have augmented aerodynamic force production in early forms of flying insects. By the late Permian, evolution of decompositional microbial and fungal communities, together with disequilibrium in rates of carbon deposition, gradually reduced oxygen concen- trations to values possibly as low as 15%. The disappearance of giant insects by the end of the Permian is consistent with extinction of these taxa for reasons of asphyx- iation on a geological time scale. As with winged insects, the multiple historical origins of vertebrate flight in the late Jurassic and Cretaceous correlate temporally with periods of elevated atmospheric oxygen. Much discussion of flight performance in Archaeopteryx assumes a contemporary atmospheric composition. Elevated oxygen levels in the mid- to late Mesozoic would, however, have facilitated aerodynamic force production and enhanced muscle power output for ancestral birds, as well as for precursors to bats and pterosaurs. INTRODUCTION Today’s oxidizing atmosphere, with an oxygen concentration of about 21%, derives in part from the metabolic activity of photosynthetic organisms. Starting with the anoxic conditions and reducing atmosphere of the Archean and early Proterozoic eons, evolution of cyanobacteria, sulfide-oxidizing bacteria, and algae contributed to buildup of oxygen partial pressures by the beginning of the Cam- 136 DUDLEY brian (570 MYa) to values likely comparable to those of the present day (1–6)....
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