Oyster larvae living in a multi-stressor world : vulnerabilities and potential for persistence

Abstract

Oysters are ecologically and economically important shellfish that have a complex life cycle involving several critical processes such as larval calcification and metamorphosis. Rising anthropogenic CO2 levels that cause ocean warming and ocean acidification are predicted to make coastal and surface oceans increasingly unsuitable for several calcifying marine invertebrates including oysters. Simultaneously, climate change-induced heavy precipitation in some parts of the world is expected to reduce ocean surface salinity. These multiple climate change stressors may not only reduce the calcification rate of marine calcifying species but also depress their metabolism. The impact of future climate change on the sensitive processes involved in the oyster’s complex life cycle, particularly metamorphosis, could be a bottleneck for population recruitment success. For example, in the U.S., oyster aquaculture is already failing to produce seeds due to climate change, providing evidence that oyster recruitment and populations may not be sustainable in future oceans. This is a stark warning to China, not only as a centre of oyster biodiversity, but also as the main producer of >80% of the world’s oysters. To avoid the possibility of future socioeconomic crisis and seafood insecurity, we need to assess how commercially important oyster species can tolerate future climate conditions. Therefore, the primary goal of this thesis is to understand how multiple climate change stressors, interactively and individually, can affect the economically and ecologically important edible oyster species, the Pacific oyster, at developmental, physiological, and molecular levels. The results demonstrated that long-term ocean acidification and exposure to multiple climate stressors had varying effects on the multiple life stages of larvae of the Chinese Pacific oyster. By analyzing multiple physical parameters (larval growth, respiration and feeding efficiency during metamorphosis, energy reserve for growth, metamorphosis success, early juvenile growth, shell composition and ultrastructure) and using multiple “omics” technologies (metabolomics and proteomics), we demonstrated the Chinese Pacific oyster had considerable tolerance and resistance to future moderate multiple stressor scenarios. Pacific oyster larvae when exposed to reduced seawater salinity and decreased pH appeared to be able to maintain an osmotic balance by shifting structural and storage lipid energy reserves, producing extra energy via saturated fatty acids, and homeoviscous adaptation. Similarly, larvae appeared to have adequate short-term proteomic plasticity to mitigate the negative effects of decreased pH by shifting energy forms, or by taking advantage of increased metabolic activity under elevated temperature. Larvae were also able to activate important ion channel protein NA+/H+ exchange regulatory cofactor NHE-RF1 to balance the cellular acid-base equilibrium in response to decreased pH. Moreover, wide alterations in the proteome, such as downregulated proteins involved in calcification, cytoskeleton, energy production, and metamorphosis-related pathways, reflected an altered energy allocation strategy that may enable the Pacific oyster to survive under decreased pH. Both proteomic and metabolomic results could explain the physiology performance of larvae living in ambient and treatment conditions, such as how they could have similar metamorphosis success and overall growth rate under these conditions. In summary, the research results not only have direct implications for oyster aquaculture and coastal management but also provide baseline data for climatic models to predict the ecological impact of projected climate change scenarios on coastal marine biodiversity, especially on shellfish.