Comparative Oxygen Consumption of Gastropod Holobionts from Deep-Sea Hydrothermal Vents in the Indian Ocean

摘要

Physiological traits are the foundation of an organism's success in a dynamic environment, yet basic measurements are unavailable for many taxa and even ecosystems. We measured routine metabolism in two hydrothermal vent gastropods, Alviniconcha marisindica (n = 40) and the scaly-foot gastropod Chrysomallon squamiferum (n = 18), from Kairei and Edmond vent fields on the Central Indian Ridge (23-25 degrees S, about 3000 meter depth). No previous studies have measured metabolism in any Indian Ocean vent animals. After recovering healthy animals to the surface, we performed shipboard closed-chamber respirometry experiments to compare oxygen uptake at different temperatures (10, 16, and 25 degrees C) at surface pressure (1 atm). The physiology of these species is driven by the demands of their chemoautotrophic symbionts. Chrysomallon has very enlarged respiratory and circulatory systems, and endosymbionts are housed in its trophosome-like internal esophageal gland. By contrast, Alviniconcha has chemoautotrophic bacteria within the gill and less extensive associated anatomical adaptations. Thus, we predicted that routine oxygen consumption of Chrysomallon might be higher than that of Alviniconcha. However, oxygen consumption of Chrysomallon was not higher than that of Alviniconcha, and, further, Chrysomallon maintained a steady metabolic demand in two widely separated experimental temperatures, while Alviniconcha did not. We interpret that these findings indicate that (1) the trophosome does not fundamentally increase oxygen requirement compared to other gastropod holobionts, and (2) cold temperatures (10 degrees C) induce a stress response in Alviniconcha, resulting in aberrantly high uptake. While these two large gastropod species co-occur, differences in oxygen consumption may reflect the separate niches they occupy in the vent ecosystem.