Physiological response of the giant acorn barnacle, Balanus nubilus, to oxygen-limiting environments

Abstract

Sessile invertebrates in the nearshore coastal and rocky intertidal habitats can experience oxygen limitation during low tide air exposure and environmental hypoxia events. For some organisms, unique morphological characteristics may make these events especially challenging. The giant acorn barnacle, Balanus nubilus, has the largest muscle fibers in the animal kingdom (diameters can exceed 3 mm in adults). At these extreme sizes, muscle cells may already be at the brink of insufficient oxygen delivery owing to low SA:V ratios and long intracellular diffusion distances. We are interested in characterizing the internal oxygen dynamics of B. nubilus during air exposure and seawater anoxia so that we can better understand how they maintain function of their giant muscle fibers during environmentally-induced oxygen limitation. To this end, we examined the following: 1) hemolymph pO2, pCO2, pH and ion (Na+, Cl−, K+, Ca2+) concentrations across 9 h exposure to air emersion, anoxic immersion and normoxic immersion (control), 2) oxygen consumption rates (MO2) of barnacles held in water and air for 6 h (at 10, 15 and 20 °C), and 3) respiratory behaviors (e.g., % time operculum open or cirri extended, cirral beat frequency) of barnacles during acute (6 h) exposure to emersion, anoxic immersion and normoxic immersion. Our data revealed that hemolymph pO2 declined significantly (by 3 h) in the anoxic barnacles, whereas the air-exposed barnacles maintained hemolymph oxygen levels that were intermediate to the control and anoxia barnacles. We also found that MO2 values for B. nubilus were very similar in seawater and air at a common temperature. These results suggest that B. nubilus can effectively acquire oxygen and support aerobic metabolism while in the air. This assumption was corroborated by our behavioral data, which revealed that air exposed (and anoxic) barnacles spent significantly more time engaged in cirral beating than control barnacles. Such a behavioral preference should enhance oxygen delivery to the internal respiratory surfaces inside the shell. Finally, we found significantly higher hemolymph [K+] in the emersed and anoxic barnacles, which - when coupled to the relatively stable pH values we observed in all treatments - may suggest involvement of K+ ions in an effective acid-base buffering system. In sum, we predict that muscle function would be preserved in B. nubilus during periods of low tide emersion, whereas environmental hypoxia events, which are increasing in frequency and duration as global climates change, have the potential to diminish functionality of their giant muscle fibers.