Oxygen, animals and oceanic ventilation: an alternative view

Of all the components of biogeochemical cycles, few attract more attention than the waste product of oxygenic photosynthesis. Chemically unstable and biosynthetically dangerous, diatomic oxygen is the key ingredient in aerobic metabolism, and a prerequisite for the evolution of large complex organisms that define the modern biosphere. Exactly how much they require is only loosely constrained, but Catling et al . (2005) suggest something in the order of 10 3 –10 4 pascals [Pa] ( ≈ 1–10% atmospheric partial pressure [ p O 2 ]; ≈ 5–50% present atmospheric level [PAL]). Moreover, geochemical modelling indicates that p O 2 has fluctuated substantially over the course of the Phanerozoic: up to c . 35% in the late Palaeozoic, and down to perhaps 10% in the early Mesozoic (Falkowski et al ., 2005; Berner, 2006). Such shifts have been considered instrumental in directing the course of Phanerozoic evolution and extinction (Falkowski et al ., 2005; Huey & Ward, 2005; Ward et al ., 2006; Berner et al ., 2007), including the Ediacaran–Cambrian radiations of macroscopic life (Berkner & Marshall, 1965; Anbar & Knoll, 2002; Catling et al ., 2005; Holland, 2006; Canfield et al ., 2007). This is certainly a worthy hypothesis, and one that has gained an exceptionally wide following over the past decade – but a popular paradigm still needs to be tested and weighed against competing scenarios. In this editorial, I take critical look at the oxygen-evolution connection and discuss an alternative, biological explanation for geochemical signatures through the terminal Proterozoic. In the absence of direct measurements, the oxygen content of ancient atmospheres is inferred from a combination of geochemical proxies and modelling. These values, however, are accompanied by substantial error (see Berner et al ., 2007: fig. 1; Kump, 2008: fig. 2), and differing modelling assumptions yield conspicuously different results. For example, where Bergman et al . (2004) estimate the oxygen content of Mesozoic atmospheres to be continuously at or above PAL, Berner (2006) puts late Triassic/early Jurassic levels close to 50% PAL, followed by an early Cretaceous rise to more or less modern levels. Falkowski et al . (2005) also recognize an early Jurassic minimum, but with PAL not reached until the Eocene. All models are of course limited by the runaway wildfire induced at p O 2 > 35%, and lack of fire at p O 2 < 15% (Belcher & McElwain, 2008), neither of which have obtained for the past 420 million years (with the possible exception of a ‘charcoal gap’ in the late Devonian (Scott & Glasspool, 2006)). Atmospheric oxygen concentrations are more difficult to constrain in the absence of a land plant record, though the appearance of iron-retaining palaeosols at or around the 2.45 Ga ‘great oxygenation event’ marks the onset of p O 2 > 0.2% (1% PAL), and the rise of conspicuously macroscopic fossils from c . 575 Ma sets a Phanerozoic lower limit of c . 1% p O 2 or 5% PAL (Canfield, 2005; Catling et al ., 2005; Holland, 2006; Kump, 2008). Deep-sea geochemical proxies and modelling have been used to estimate an upper limit of c . 8% p O 2 (40% PAL) for most of the Proterozoic.