Oxygen in egg masses: interactive effects of temperature, age, and egg-mass morphology on oxygen supply to embryos

Embryos of many marine invertebrates are encased in gelatinous masses for part or all of development. Because gel and intervening embryos retard oxygen flux, such a life-history mode profoundly affects partial pressures of metabolic gases surrounding embryos. However, little is known about relationships between egg-mass structure and the opportunities and constraints imposed on structure by metabolic gas transport. We examined the effects of four factors (temperature, embryo age, embryo density and egg-mass size) on the metabolism of egg masses using both natural egg masses of a nudibranch and artificial egg masses made from sand dollar embryos and low-melting point agarose. Both temperature and embryo age strongly affected metabolic rates of nudibranch embryos. For embryos of a given age (stage), rates of oxygen consumption roughly doubled between 12 and 21 degrees C; from early cleavage to the veliger stage, consumption rose two- to fourfold, depending on temperature. Oxygen profiles in egg masses showed that advanced embryonic age, and to a lesser extent high temperature, both led to steeper oxygen gradients into egg masses. Egg masses containing advanced embryos at 21 C had very low central oxygen levels. Small-diameter artificial masses (2 mm diameter) had virtually no internal oxygen gradients regardless of embryo density or temperature, while medium (4 mm) and large diameter (10 mm) artificial masses had oxygen profiles that depended strongly and interactively on embryo density and temperature. Together, our data on natural and artificial egg masses suggest that (i) multiple factors have strong effects on metabolic rate; (ii) rates of oxygen transport are relatively invariant with temperature in simple, artificial systems but may vary more strongly with temperature in natural egg masses; and (iii) the four factors - temperature, embryo age, embryo density and egg-mass size - interact in important ways bearing on egg mass design. A simple mathematical model is developed to provide a quantitative means of estimating primary and interactive effects of the different factors. We also show that in T. diomedea the gel itself is the main barrier to oxygen transport into egg masses, and that the metabolic activity of embryos increases substantially when embryos are artificially released from the capsules that contain them within the gel mass.