Limits to Diffusive O2 Transport: Flow, Form, and Function in Nudibranch Egg Masses from Temperate and Polar Regions

Amy L Moran,H Arthur Woods,Craig R White

doi:10.1371/journal.pone.0012113

Abstract

BackgroundMany aquatic animals enclose embryos in gelatinous masses, and these embryos rely on diffusion to supply oxygen. Mass structure plays an important role in limiting or facilitating O2 supply, but external factors such as temperature and photosynthesis can play important roles as well. Other external factors are less well understood.Methodology/Principal FindingsWe first explored the effects of water flow on O2 levels inside nudibranch embryo masses and compared the effects of flow on masses from temperate and polar regions. Water flow (still vs. vigorously bubbled) had a strong effect on central O2 levels in all masses; in still water, masses were considerably more hypoxic than in bubbled water. This effect was stronger in temperate than in polar masses, likely due to the increased metabolic demand and O2 consumption of temperate masses. Second, we made what are to our knowledge the first measurements of O2 in invertebrate masses in the field. Consistent with laboratory experiments, O2 in Antarctic masses was high in masses in situ, suggesting that boundary-layer effects do not substantially limit O2 supply to polar embryos in the field.Conclusions/SignificanceAll else being equal, boundary layers are more likely to depress O2 in masses in temperate or tropical regions; thus, selection on parents to choose high-flow sites for mass deposition is likely greater in warm water. Because of the large number of variables affecting diffusive O2 supply to embryos in their natural environment, field observations are necessary to test hypotheses generated from laboratory experiments and mathematical modeling.

Highlights

Many marine and aquatic animals enclose embryos in gelatinous masses, and embryos in gel depend largely or entirely on diffusion to supply O2 for metabolism
Because O2 is fundamentally important to the metabolism that supports development, diffusive O2 supply is likely an overriding factor constraining the range of possible mass morphologies
Our data indicate that boundary layers strongly affect oxygen supply to embryos in gelatinous egg masses

Summary

Introduction

Many marine and aquatic animals enclose embryos in gelatinous masses, and embryos in gel depend largely or entirely on diffusion to supply O2 for metabolism. Egg masses, because they are simple compared to whole organisms, provide powerful systems for examining how constraints on oxygen diffusion shape the evolution of morphology, ecology, and behavior. External oxygen environments vary over many scales [18] and the result of this variation is likely to be intensification, or in some cases relaxation, of oxygen-related constraints on morphology.

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