During the Palaeozoic some arthropod species grew to gigantic proportions. The rise of these giants strongly correlates with increased atmospheric oxygen concentrations (∼32% vs today's 21% O2). Among present day arthropods marine polar species show remarkable gigantism compared with lower latitude species. The size of these marine arthropods also correlates well with the increased oxygen solubility of the colder polar waters. These positive correlations of body size and oxygen availability form the basis of the `oxygen hypothesis', which states that increased oxygen concentrations facilitate improved oxygen supply to tissues, thereby allowing the evolution of larger body sizes. This hypothesis is intuitively attractive; however, very little experimental testing has been done to investigate whether the correlation between oxygen availability and size does indeed signify causation. Some data are available for short term developmental studies,mostly for Drosophila melanogaster, but stronger experimental tests of this hypothesis only recently started to appear in the peer reviewed literature.
Arthur Woods and colleagues report one such study in Proceedings of the Royal Society B, where they tested the performance during forced activity(self righting) of Antarctic pycnogonids from McMurdo Sound. In Antarctic waters pycnogonids (commonly known as sea-spiders) can reach colossal leg spans of 40 cm. Woods worked with 12 species with masses spanning three orders of magnitude. Using a 1000 l temperature controlled aquarium his team presented the specimens with 17% (low), 43% (medium) and 92% (high) air saturation oxygen levels. After brief equilibration they turned the pycnogonids on their backs and noted the time required to right themselves and the number of rightings in 1 h. They also measured body mass and leg diameter as leg diameter is an ideal metric to gauge oxygen diffusion to internal tissues. According to the oxygen hypothesis Woods predicted that larger pycnogonids would perform proportionally worse compared with smaller specimens– especially in lower oxygen levels. Alternatively, should the animals show symmorphosis – when their functional structure is developmentally and/or evolutionarily regulated to match, but not exceed, functional demand– both large and small specimens will perform equally when oxygen stressed.
Woods' team found that Antarctic pycnogonids' body surface areas scaled proportionally with mass, which suggests that the decreased surface area to mass ratios found in larger animals might cause increased oxygen sensitivity. Indeed, oxygen availability had a strong effect, with sea-spiders in high oxygen righting themselves more readily than those in low oxygen. However, it turned out that body size did not have a consistent effect on performance in relation to oxygen availability. Large pycnogonids' righting performance was only slightly worse than that of the smaller ones. Midsize specimens performed best with up to 160 rightings per hour, compared with ∼40 rightings for either size extremes. These results contradict the predictions of the oxygen hypothesis and also suggest that pycnogonids do not have wide oxygen safety margins. The team concluded that oxygen availability is unlikely to fully explain the evolution of large size in Antarctic pycnogonids.
One explanation Woods and colleagues offer for their data's consistency with symmorphosis is that millions of years of evolution in cold polar waters could have fine tuned the pycnogonids' oxygen delivery systems to these oxygen rich waters, leaving narrow safety margins. With this experimental approach Woods and colleagues illustrated that oxygen availability is still an important factor but is not the only important factor in attempts to explain the evolution of gigantism.
