The Evolutionary Physiology of Animal Flight: Paleobiological and Present Perspectives

Abstract

Recent geophysical analyses suggest the presence of a late Paleozoic oxygen pulse beginning in the late Devonian and continuing through to the late Carboniferous. During this period, plant terrestrialization and global carbon deposition resulted in a dramatic increase in atmospheric oxygen levels, ultimately yielding concentrations 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 Paleozoic 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 concentrations 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 asphyxiation 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.

The effects of age and behavioral development on honey bee (Apis mellifera) flight performance

“…Across closely related hovering insects, n decreases with M b during hovering flight (Dillon and Dudley, 2004;Dudley, 2000), but this negative relationship does not always hold true for the few available datasets allowing intraspecific comparisons of n and M b . In honey bees, there is a slight negative relationship between n norm and M b , although this is unlikely to be due to resonance issues and an increase in the induced power required to move a larger wing (factors typically associated with the negative relationship between n and M b across similar species) because neither wing size nor thorax dimensions differ between foragers and nurses (J.T.V., unpublished observation).…”

Evolution on a Restless Planet: Were Environmental Variability and Environmental Change Major Drivers of Human Evolution?

“…For example, during the late Paleozoic, high oxygen concentrations in the atmosphere supported gigantic flying forms, including dragonflies a meter long and pterosaurs weighing perhaps 100 kg. (Graham et al 1995;Dudley 2000). Everyone accepts, we suppose, that external processes are important regulators of the rate and direction of evolution in the very long run, and everyone accepts that evolution is not an instantaneous process.…”

Ontogeny of tracheal system structure: A light and electron‐microscopy study of the metathoracic femur of the American locust, Schistocerca americana

“…The high capacity for oxygen delivery of the tracheal system is also indicated by the high safety margins for oxygen delivery in resting insects, which can commonly tolerate oxygen levels of 5 kPa or lower before demonstrating a drop in metabolic rate (Miller, 1964;Wegener, 1993;Harrison, 1998, 2004). However, recent suggestions that maximal insect body size is limited by atmospheric oxygen levels (Graham et al, 1995;Dudley, 1998Dudley, , 2000 raise the possibility that oxygen delivery may become more challenging for insects as they increase in size; or, more formally, that the ratio of tracheal oxygen delivery capacity to tissue oxygen consumption rate may decrease with size. In this study we conducted a partial test of this hypothesis by using quantitative light and electron microscopy to estimate the oxygen delivery capacity of the tracheal system within the metathoracic femur of 2nd instar and adult American locusts, Schistocerca americana.…”