Phenotypic plasticity in economically and ecologically important bivalves in response to changing environments

Marine bivalves are ecologically important, providing ecosystem services like filtering water, stabilizing substrate, and creating hard structure for epibionts. Cultured bivalves are also economically important, supporting thousands of aquaculture jobs nationwide and providing valuable protein sources for our growing human population. However, recent shifts in the environment such as temperature, ocean acidification, hypoxia, and extreme environmental variation have greatly affected bivalve physiology, reproduction, and survival across multiple lifestages. Bivalves in the Northeast Pacific are increasingly vulnerable climate change related stressors like intensifying upwelling and weather extremes, defined stratification, and unique geography which causes distinct spatial and seasonal variation. I seek to investigate if higher degrees of phenotypic plasticity and parental carryover will have the potential to improve bivalve’s fitness and tolerance as climate change progresses. My goal is to evaluate plastic capacity by taking a multi-method approach to assessing the physiological metrics of several important bivalve species, using both field and laboratory experiments. Early lifestages are greatly influenced by parental environmental history leading to carryover effects, favoring phenotypes that have a higher likelihood of surviving. In addition to natural selection in the wild, commercial and restoration aquaculturists may select for beneficial phenotypes in adults and offspring which would yield the most desirable characteristics. In our experiment, I focus on three different species: the purple-hinge rock scallop Crassadoma gigantea, the Mediterranean mussels Mytilus galloprovincialis, and the Olympia oyster Ostrea lurida. By choosing a suite of native and non-native, inter- and subtidal species, I hope to obtain a broad snapshot of physiological responses to help restore vulnerable species and maximize quality of farmed product. Chapter 1 examines physiological responses of the scallop C. gigantea to climate change related stressors in the laboratory. I conducted a full factorial laboratory experiment, manipulating pCO2 and temperature to mimic current and future ocean acidification and warming levels. After six weeks of acclimation, I found that stressors reduced shell strength and periostracum (outer shell layer) density. Only acidification affected lipids, and fatty acid content varied between treatments. I was the first to quantify microbial composition of a bivalve under multiple stressors and I found differences in the microbiome, especially with temperature stress. Chapter 2 explores physiological responses of C. gigantea and M. galloprovincialis in a six-month field acclimatation experiment. Shellfish were deployed in cages in Puget Sound, Washington at either 5 or 30 m below the surface. I found that environmental gradients varied seasonally and spatially and affected growth, shell strength, and isotopic signatures. There were differences between the two species, namely with shell strength and δ13C. I found that no one depth or time period yielded the most desirable traits for culturing, and I highlight the concerning patterns in Puget Sound’s most productive region. In Chapter 3, I took my research one step further by introducing a spatial component to a one-year field experiment. I outplanted O. lurida in cages at 5 m depth in three different locations in Puget Sound, one of which also had a 20 m depth. Each of these locations had an oceanographic monitoring buoy which allowed me to couple physiological data with high-resolution environmental data. I spawned the oysters to test parental carryover and found evidence in growth rates of larvae, which when acclimated to high temperatures, mirrored their parents. Interestingly, larval survival did not coincide with growth, and through respirometry, I found that 20°C may be a bottleneck for this lifestage. Adult oyster growth, isotopic signatures, and gametogenesis were affected by both seasonal and spatial field conditions. Metabolic responses to pH and temperature depending on recent acclimatization history. This research shows evidence of strong adaptive plasticity which was demonstrated by energetic trade-offs and parental carryover. Chapter 4 acclimatized M. galloprovincialis in the field in a similar fashion to O. lurida. Growth, shell strength, and isotopes were all affected by season and site. Similar to oysters, acute metabolic rate of each site and season was affected differently between pH and temperature. Shellfish covered in Chapter 3/4 have a high degree of plasticity and results are useful to restoration (oyster) and commercial (mussel) aquaculturists to create selective breeding programs that will withstand climate change. Results of this dissertation demonstrate the rapid degree of phenotypic plasticity and capacity for parental carryover in field and laboratory setting though a wide array of physiological analysis. Outcomes of this research add to the limited but growing body of literature about multiple-stressors and field experiments, and indents to assist aquaculturists as climate change progresses.

Alma, L., 2022. Phenotypic plasticity in economically and ecologically important bivalves in response to changing environments. PhD thesis, University of Washington. Thesis (restricted access).

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