Temperature‐Oxygen Interactions and the Evolution of Giant Antarctic Sea Spiders

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For more than a hundred years, scientists have known that many marine invertebrate taxa grow to unusually large size in polar waters. This biogeographic pattern has become known as polar gigantism, and it occurs in taxa as diverse as glass sponges, ctenophores, foraminiferans, polychaete annelids, isopod crustaceans, copepods, amphipod crustaceans, and pycnogonids. Despite being common, polar gigantism remains a physiological and evolutionary mystery; how and why do polar taxa grow to such large sizes? Using Antarctic sea spiders (pycnogonids), we tested one of the leading physiological hypotheses about polar gigantism—the oxygen hypothesis, proposed by Chapelle and Peck, which states that polar giants are permitted in very cold water by high levels of oxygen supply coupled to low metabolic demand for that oxygen. We measured whole‐body metabolic rates spanning three orders of magnitude in body size. Metabolic rate scaled to body mass with an exponent of 0.9, indicating that giant sea spiders do not require unusually low metabolic rates. Using oxygen electrodes and dye‐tracer experiments, we examined the details of oxygen transport across the cuticle and of oxygen levels and transport in the hemocoel. Oxygen is taken up across the cuticle (there is no distinct respiratory organ), and the cuticle is a much greater barrier to oxygen movement than is the mix of fluids and tissues inside the legs and trunk. Oxygen levels in the hemocoel were high everywhere in the body, but were consistently highest in distal parts of the legs and lowest in the trunk. In addition, larger sea spiders had lower central levels of oxygen. Our dye tracer experiments suggested that contractions of the heart and muscles in the legs drive relatively rapid blood circulation, especially between the trunk and proximal parts of the legs. This indicates that sea spiders use their proximal leg segments as respiratory surfaces. Building on these physiological details, we constructed a mathematical model of oxygen transport and consumption, which we applied to the range of body sizes we studied in Antarctica. The model accurately predicted measured levels of oxygen in the blood. We then used the model along with realistic Q10s for key oxygen processes to simulate how polar sea spiders would perform in warmer water. These simulations strongly suggest that gigantic forms would not obtain oxygen rapidly enough in warm water to support their higher metabolic rates. Thus, together our empirical and theoretical studies support the oxygen hypothesis: it appears that the giant forms found in the Ross Sea can balance their oxygen budgets only because supply is so high and demand is so low.Support or Funding InformationNational Science Foundation grant 1341476