Modeling Variable Phanerozoic Oxygen Effects on Physiology and Evolution.

Geochemical approximation of Earth's atmospheric O2 level over geologic time prompts hypotheses linking hyper- and hypoxic atmospheres to transformative events in the evolutionary history of the biosphere. Such correlations, however, remain problematic due to the relative imprecision of the timing and scope of oxygen change and the looseness of its overlay on the chronology of key biotic events such as radiations, evolutionary innovation, and extinctions. There are nevertheless general attributions of atmospheric oxygen concentration to key evolutionary changes among groups having a primary dependence upon oxygen diffusion for respiration. These include the occurrence of Devonian hypoxia and the accentuation of air-breathing dependence leading to the origin of vertebrate terrestriality, the occurrence of Carboniferous-Permian hyperoxia and the major radiation of early tetrapods and the origins of insect flight and gigantism, and the Mid-Late Permian oxygen decline accompanying the Permian extinction. However, because of variability between and error within different atmospheric models, there is little basis for postulating correlations outside the Late Paleozoic. Other problems arising in the correlation of paleo-oxygen with significant biological events include tendencies to ignore the role of blood pigment affinity modulation in maintaining homeostasis, the slow rates of O2 change that would have allowed for adaptation, and significant respiratory and circulatory modifications that can and do occur without changes in atmospheric oxygen. The purpose of this paper is thus to refocus thinking about basic questions central to the biological and physiological implications of O2 change over geological time.

Spiracular air breathing in polypterid fishes and its implications for aerial respiration in stem tetrapods.

The polypterids (bichirs and ropefish) are extant basal actinopterygian (ray-finned) fishes that breathe air and share similarities with extant lobe-finned sarcopterygians (lungfishes and tetrapods) in lung structure. They are also similar to some fossil sarcopterygians, including stem tetrapods, in having large paired openings (spiracles) on top of their head. The role of spiracles in polypterid respiration has been unclear, with early reports suggesting that polypterids could inhale air through the spiracles, while later reports have largely dismissed such observations. Here we resolve the 100-year-old mystery by presenting structural, behavioural, video, kinematic and pressure data that show spiracle-mediated aspiration accounts for up to 93% of all air breaths in four species of Polypterus. Similarity in the size and position of polypterid spiracles with those of some stem tetrapods suggests that spiracular air breathing may have been an important respiratory strategy during the fish-tetrapod transition from water to land.

Atmospheric oxygen levels affect mudskipper terrestrial performance: implications for early tetrapods.

The Japanese mudskipper (Periophthalmus modestus), an amphibious fish that possesses many respiratory and locomotive specializations for sojourns onto land, was used as a model to study how changing atmospheric oxygen concentrations during the middle and late Paleozoic Era (400-250 million years ago) may have influenced the emergence and subsequent radiation of the first tetrapods. The effects of different atmospheric oxygen concentrations (hyperoxia = 35%, normoxia = 21%, and hypoxia = 7% O2) on terrestrial performance were tested during exercise on a terrestrial treadmill and during recovery from exhaustive exercise. Endurance and elevated post-exercise oxygen consumption (EPOC; the immediate O2 debt repaid post-exercise) correlated with atmospheric oxygen concentration indicating that when additional oxygen is available P. modestus can increase oxygen utilization both during and following exercise. The time required post-exercise for mudskippers to return to a resting metabolic rate did not differ between treatments. However, in normoxia, oxygen consumption increased above hyperoxic values 13-20 h post-exercise suggesting a delayed repayment of the incurred oxygen debt. Finally, following exercise, ventilatory movements associated with buccopharyngeal aerial respiration returned to their rest-like pattern more quickly at higher concentrations of oxygen. Taken together, the results of this study show that P. modestus can exercise longer and recover quicker under higher oxygen concentrations. Similarities between P. modestus and early tetrapods suggest that increasing atmospheric oxygen levels during the middle and late Paleozoic allowed for elevated aerobic capacity and improved terrestrial performance, and likely led to an accelerated diversification and expansion of vertebrate life into the terrestrial biosphere.