Reconsidering the oxygen-temperature hypothesis of polar gigantism: Successes, failures, and nuance

“Polar gigantism” describes a biogeographic pattern in which many ectotherms in polar seas are larger than their warmer-water relatives. Although many mechanisms have been proposed, one idea-the oxygen-temperature hypothesis-has received significant attention because it emerges from basic biophysical principles and is appealingly straightforward and testable. Low temperatures depress metabolic demand for oxygen more than supply of oxygen from the environment to the organism. This creates a greater ratio of oxygen supply to demand, releasing polar organisms from oxygen-based constraints on body size. Here we review evidence for and against the oxygen-temperature hypothesis. Some data suggest that larger-bodied taxa live closer to an oxygen limit, or that rising temperatures can challenge oxygen delivery systems; other data provide no evidence for interactions between body size, temperature, and oxygen sufficiency. We propose that these findings can be partially reconciled by recognizing that the oxygen-temperature hypothesis focuses primarily on passive movement of oxygen, implicitly ignoring other important processes including ventilation of respiratory surfaces or internal transport of oxygen by distribution systems. Thus, the hypothesis may apply most meaningfully to organisms with poorly developed physiological systems (eggs, embryos, egg masses, juveniles, or adults without mechanisms for ventilating internal or external surfaces). Finally, most tests of the oxygen-temperature hypothesis have involved short-term experiments. Many organisms can mount effective responses to physiological challenges over short time periods; however, the energetic cost of doing so may have impacts that appear only in the longer term. We therefore advocate a renewed focus on long-term studies of oxygen-temperature interactions.