Physiological response of shellfish native to the North American Pacific Coast to ocean acidification and warming

Following observations of shifting ocean conditions an enormous scientific effort has explored the response of marine species to ocean acidification and warming. Empirical data has established that many species are vulnerable to ocean conditions projected for this century, particularly calcifying invertebrates, affecting a range of physiological processes over the lifetime of an organism. However, these studies also indicate that biological responses are quite variable, related to an organism’s genetic and environmental ancestries. Some species are more tolerant to the effects of acidification than others, as are some populations within species. There is also evidence that transgenerational carryover effects may alleviate some negative effects by buffering future generations against challenging conditions. The future of marine ecosystems and food systems hinges in part upon our ability to identify, conserve, and invest in individuals that can tolerate shifting ocean conditions, and to understand the role of transgenerational carryover effects in shaping future populations.

The aim of this dissertation work is to examine the physiological and molecular responses of two invertebrate species native to the North American Pacific Coast, the Olympia oyster (Ostrea lurida) and Pacific geoduck (Panopea generosa), to ocean acidification and warming. Both species inhabit dynamic, heterogeneous estuarine environments that are influenced by coastal upwelling, and through adaptation and/or carryover effects may be relatively tolerant of ocean change. By testing multiple species, populations, life stages, and generations I provide evidence that these Pacific Coast natives are uniquely equipped for the effects of ocean acidification, and that warming will be a more impactful, but not necessarily negative, driver of physiological changes.

Chapter 1 characterizes the proteomes of Pacific geoduck in varying natural environments and habitat-specific pH conditions. Juvenile geoduck were deployed in eelgrass and adjacent unvegetated habitats for 30 days while pH, temperature, dissolved oxygen, and salinity were monitored. Across the four deployment locations pH was lower in unvegetated habitats compared to eelgrass habitats. While geoduck growth and proteomes were not affected by pH, they were sensitive to temperature and dissolved oxygen, but neither affected survival rates. Chapter 1 demonstrates that geoduck may be resilient to acidification in a natural setting and temperature may have a greater influence on geoduck physiology.

Chapter 2 examines the intra- and inter-generational carryover effects of ocean warming in the Olympia oyster. In many species reproductive and metabolic processes are tightly linked to the seasonal change from winter to spring, yet we know little about how these processes will shift as winters become milder. Therefore, in Chapter 2 I exposed adult Olympia oysters to elevated winter temperature and monitored effects to reproduction and offspring viability in spring. Parental exposure to warming did not affect overall larval production or survival, however it did increase the size and development of gametes, and the size of larval offspring. In the wild more developed gametes and larger larvae following milder winters could greatly impact recruitment patterns, possibly benefitting O. lurida populations. The results of Chapter 2 suggest that O. lurida is at minimum resilient to winter warming, and at best could benefit from it due to improved larval viability.

Chapter 3 continues exploring carryover effects in the Olympia oyster by examining the effects of combined ocean warming and acidification across three distinct O. lurida populations. Larval production was higher and began sooner following winter warming, was reduced by acidification, but was unaffected by combined stressors. Offspring of parents exposed to acidification, which were reared in common conditions for one year, had higher survival rates when tested in the field. Results of Chapter 3 indicate that altered recruitment patterns may follow warmer winters due to a prolonged reproductive season and/or increased production, but these effects may be masked by coincidental high pCO2. Furthermore, Olympia oysters may be more resilient in certain environments when progenitors are pre-conditioned in stressful conditions. This carryover effect demonstrates that parental conditions can have substantial ecologically relevant impacts that should be considered when predicting impacts of environmental change.

Chapter 4 further describes three O. lurida populations’ responses to acidification by examining growth, reproductive development, gene expression, and signals in offspring. Responses reveal energetic trade-offs that range from a robust transcriptional response in one population (Dabob Bay) without impacts to growth or reproduction, to no detectable transcriptional response but negative impacts to growth and reproduction in another (Oyster Bay). While exposure to acidification did not affect gene expression in the next generation’s larval stage, it did increase larval size in the Oyster Bay, which could partially alleviate negative effects of acidification in the wild in that population. Given the distinct transcriptional response of the Dabob Bay population to acidification and its high survival rates in previous studies, we identified genes unique to that population, which provide insight into the mechanisms behind a stress-tolerant oyster population. Chapter 4 provides the first description of molecular processes responsive to acidification in an Ostrea spp, and demonstrates that species inhabiting heterogeneous environments, even on small geographic scales, offer natural reservoirs of biodiversity.

This dissertation work reveals the resilience of bivalves native to the Northeast Pacific Ocean to ocean change, and suggests that that Olympia oyster and Pacific geoduck are good candidates for aquaculture investment and conservation efforts. Furthermore, population-specific responses and carryover effects observed in Olympia oyster suggests that both fine-scale genetic structure and parental priming can influence how an organism responds to ocean change, and should be considered by conservationists and managers, and in future studies.

Spencer L., 2021. Physiological response of shellfish native to the North American Pacific Coast to ocean acidification and warming. PhD thesis, University of Washington, 168 p. Thesis.

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