Since early scientific expeditions to Antarctica, researchers have been aware that many Antarctic marine invertebrates are much larger than their relatives in warmer  regions of the world. This phenomenon is called ‘polar gigantism’ and despite over 100 years of work on Antarctic marine animals, the reasons behind polar gigantism are not well understood.

This work tested a leading physiological hypothesis for polar gigantism, the oxygen hypothesis. This hypothesis arises from observations about oxygen supply and demand in cold water. Cold water often holds high levels of oxygen, and cold temperatures depress metabolic rates of marine invertebrates. Thus, polar oceans create a situation in which oxygen is in high supply but low demand. Over evolutionary timescales, this may allow lineages to evolve larger body sizes without suffering from inadequate oxygen supply. Lineages are released from oxygen-related constraints on body size.

Intellectual Merit. Working at McMurdo Station for two field seasons, we tested this hypothesis using Antarctic sea spiders (Pycnogonida), a group that contains many striking examples of polar gigantism.  We measured, on a wide range of species, a number of aspects of oxygen physiology: how fast they use oxygen (their metabolic rates), the speed and paths by which oxygen gets into the body, and the internal distributions of oxygen. The results supported the oxygen hypothesis—by demonstrating that larger spiders had higher metabolic rates, more difficulty obtaining adequate oxygen, and, under some circumstances, lower levels of oxygen inside their bodies. We developed a mathematical model which allowed us to predict oxygen dynamics in individuals even larger than those we measured directly. The model suggested that there are upper limits to body size in sea spiders, and that the observed large body sizes likely are possible only because the water is so consistently cold.

Our work examined two additional aspects of gigantism. The first was to ask whether biomechanics constrains the evolution of better structures and physiologies for gaining oxygen. This possibility is suggested by potential conflicts between different functions of the exoskeleton (cuticle). Sea spiders gain most of their oxygen directly via the cuticle everywhere on the body. In principle, larger sea spiders could gain sufficient oxygen by evolving thinner, more porous cuticles, but the cuticle is also the weight-bearing skeleton, meaning there are structural limits to how thin or porous it can be. We examined this conflict by measuring differences in biomechanical properties across sea spiders having different body sizes. The results indicate that cuticle structure represents an evolutionary compromise between the competing functions of oxygen uptake and effective locomotion.

Second, we examined how water temperature affected oxygen uptake, oxygen utilization, and animal performance (all in the context of body size). We found that, like many other Antarctic invertebrates, sea spider metabolic rates were highly sensitive to temperature, rising dramatically with even a few degrees of warming above normal Antarctic sea temperatures (-1.5 °C).  We also found that warming strongly impacted performance; sea spider movement was slower at each incremental increase in temperature, and many animals were immobilized once temperatures reached 9°C.  To examine the potential consequences of thermal sensitivity, we built a mathematical model of oxygen movement across the legs and then used it to predict how rising temperatures affect internal oxygen concentrations. It suggested that higher water temperatures cause internal oxygen levels to decline sharply and that the largest-bodied individuals will be affected the most.  Interestingly, when we directly tested the combined effects of temperature and body size on movement and activity, we found that large- and small-bodied animals were equally impacted by warm temperatures.  Close examination of cuticle structure showed that within two species of sea spider, the porousness of the cuticle increases as animals grow.  Because sea spiders acquire oxygen through their cuticle pores, and larger animals have more porous cuticles, larger animals likely acquire oxygen more easily than do small ones.  Together these results suggest that although warming oceans will undoubtedly have profound impacts on all Antarctic species, sea spiders that display polar gigantism may be no more vulnerable than smaller animals.

Broader Impacts. The grant supported a wide array of broader impacts. It supported two PhD students (one of whom has successfully defended his dissertation and the other of whom is in process). The team engaged in significant outreach via the project website, many skype sessions with K-12 and college classrooms, and multiple articles and videos about our work in the popular press. In addition, the PIs gave multiple formal talks at scientific conferences and informal talks to local groups. Finally, we wrote a successful application to have a PolarTrec teacher (Tim Dwyer, K-12 teacher in Friday Harbor, WA) join us for one of the Antarctic seasons. He participated fully in all aspects of the project, maintained a blog of his experiences, and developed educational curricula for his class back in Washington.

Last Modified: 11/11/2018
Modified by: Bret W Tobalske