Immovably flexible : spatial variation in emersion stress responses by Saccostrea cuccullata

Abstract

Saccostrea cuccullata is an intertidal oyster that dominates most sheltered hard shores around the Indo-Pacific Ocean. Due to their sessile nature, they act as ecosystem engineers, providing thermal refuges for a variety of species and thereby enhancing local diversity. These oysters experience stressful emersion periods every day as the tide recedes, which are further intensified during the summer season in Hong Kong. Unlike mobile species that can move to seek refuge, S. cuccullata are sessile and must adopt other strategies to survive these stressful periods. This study investigates the various strategies oysters adopt to persist in this dynamic and stressful habitat where resources are limited, and environmental factors vary at different spatial and temporal scale. Saccostrea cuccullata dominates most of the wave sheltered hard shore substrata around Hong Kong. Studies focused on three sheltered shores in the south of Hong Kong Island which, although all located in the same waters, varied in their local thermal regimes, physical and biological characteristics. Differences in thermal regimes also occurred between shore heights within the oyster bands, creating a complex mosaic at different spatial scales. These variations in thermal regimes and environmental factors are related to the life histories of oysters, as demonstrated by the differences in mortality and Gonadosomatic Index (GSI) recorded among oysters from different sites and shore heights. During emersion, the physiological responses of Saccostrea cuccullata were sensitive to their individual environments, where oysters showed different degrees of oxygen deprivation and hyperosmotic stress. Further investigation of physiological responses under controlled emersion (common garden) simulations showed variation in osmo-regulatory responses between oysters from different sites, despite their similar treatment, suggesting that the oysters may be locally acclimated to the stress regime of their occupying habitats. Local acclimation was further supported by the spatial variation in cellular heat shock responses (cellular HSR) of S. cuccullata. Oysters from different shore heights showed variation in cellular HSR before and after common garden acclimation, indicating that the spatial variation in cellular HSR occurred at different scales and was associated with individuals’ past thermal histories. While oysters did not display air-gaping behaviour during emersion, they did exhibit different magnitudes of valve closure, which varied spatially and temporally, implying that seasonal environmental variation may trigger different behaviour patterns. Saccostrea cuccullata also displayed spatial and temporal differences in gaping behaviour (i.e. feeding duration) when immersed, which, combined with the energetic trade-offs for stress responses at different thermal regimes, explained the variation in their energetic status and reproductive development measured throughout the summer. Overall, the spatial variation in the physiological and behavioural responses of Saccostrea cuccullata suggests that the oysters adopt varying strategies in response to their specific, residing thermal regimes, which leads to different life histories. Considering that the oysters are exposed to thermal regimes close to, and sometimes exceeding, their upper thermal limits (~47°C), the susceptibility of S. cuccullata to climate warming should be considered, taking into account potential synergistic effects from other stressors, which may affect the oysters’ future distribution and subsequent local biodiversity patterns.