Local ecosystem processes modulate ocean acidification and its effect on benthic foundation species
Lowe, Alexander Trent
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Ocean acidification poses serious threats to coastal ecosystem services, yet few empirical studies have investigated how feedbacks from local ecological processes may modulate global trends of pH from rising atmospheric CO2. Just as microclimatic influences cause departures from long-term warming trends in temperature, local processes may decouple local marine environments from the increased anthropogenic CO2 that dissolves in seawater and reduces pH. Seawater pH has been shown to be an important factor regulating physiological processes of many aquatic organisms, including valuable aquaculture species like Pacific oysters. Understanding 1) whether long-term ocean acidification varies spatially due to local ecological processes, 2) which environmental factors or ecological processes drive variation in seawater pH, and 3) the effects of this pH variation on marine organisms are critical research needs for climate change adaptation and management of important marine resources. In this dissertation, I found that pH exhibits high variability across spatial and temporal scales in the Salish Sea, exhibiting location-specific long-term changes driven by differences in net ecosystem metabolism (Chapter 1). By mapping pH in important shellfish aquaculture regions of Washington state, I showed that shallow-water environments over tidal flats are more variable in pH than surface waters over deeper channels, associated with bentho-pelagic coupling of organic matter production and decomposition, in addition to characteristic physical changes of temperature and salinity up-estuary (Chapter 2). Using interactions with an autotrophic foundation species (eelgrass Zostera marina) along estuarine gradients, I found that growth of two species of oyster were most strongly positively correlated to differences in stable isotope and fatty acid biomarkers of food availability both from river to ocean along the estuarine gradient and in association with eelgrass (Chapter 3). Shell strength, a putative indicator of pH stress, showed a positive response to eelgrass for the native, but negative response for the non-native oyster. Small differences in growth and shell strength were observed in association with eelgrass, but mortality related to predation was much higher in eelgrass. Collectively, these results support the adoption of an ecosystem perspective to ocean acidification as well as other stressors in productive aquatic habitats. Chapter 1: Patterns of pH variability were quantified as a function of atmospheric CO2 and local physical and biological processes at 83 sites over 25 years in the Salish Sea and two NE Pacific estuaries. Mean seawater pH decreased significantly at -0.009 ± 0.0005 pH yr-1 (0.22 pH over 25 years), with spatially variable rates ranging up to 10 times greater than atmospheric CO2-driven ocean acidification. Dissolved oxygen saturation (%DO) decreased by -0.24 ± 0.036% yr-1, with site-specific trends similar to pH. Mean pH shifted from <7.6 in winter to >8.0 in summer concomitant with the seasonal shift from heterotrophy (%DO <100) to autotrophy (%DO>100) and dramatic shifts in aragonite saturation state critical to shell-forming organisms (probability of undersaturation was >80% in winter, but <20% in summer). At multiple scales, %DO overwhelmed the influence of atmospheric CO2, temperature and salinity on pH, providing strong evidence that local ecosystem processes modulate ocean acidification. Chapter 2: I mapped surface water pH using a Durafet sensor in seven important aquaculture regions in the Salish Sea, including over intertidal flats that were not generally the focus of sampling efforts collated in Chapter 1. Surveys were repeated in late summer and early spring to investigate seasonal differences in nearshore oceanography. Spatial variation in pH within bays was greater in summer than late spring, and summer surveys also documented greater area experiencing low pH. The areas with low pH tended to be in shallow water. Temperature, salinity, dissolved oxygen and the ratio of chlorophyll to total suspended solids (Chl:TSS) were important factors explaining variation in pH. The strong correlation of pH variability with Chl:TSS provides a mechanistic hypothesis linking food web dynamics and pH stress in coastal areas through the production and decomposition of suspended organic matter. Factors controlling food quality and quantity (primary production, detrital abundance and decomposition) were correlated to pH, indicating pH and food stress to suspension feeders are likely often co-occurring. Chapter 3: I investigated the effects of an autotrophic foundation species (eelgrass, Zostera marina) on intertidal native (Ostrea lurida) and non-native oysters (Crassostrea gigas) across a range of estuarine conditions in Willapa Bay and Padilla Bay, Washington. I analyzed morphological (growth and shell strength), demographic (survival), and physiological responses (stable isotope and fatty acid signatures) to determine the relative influence of mechanisms by which foundation species affect associated species. Hypothesized mechanisms include top-down and bottom-up food web interactions, and amelioration of pH associated with net photosynthesis (CO2 uptake) in eelgrass. Eelgrass interactions significantly influenced top-down effects, reducing survival at many sites through provision of habitat for predators. Fatty acid concentration and stable isotope signatures were significant predictors of growth for both species, providing strong evidence of bottom-up effects, including potential fatty acid limitation in native oysters, related to environmental context and modified by eelgrass. Effects of eelgrass on pH stress were inconclusive: Eelgrass had positive effects on growth of both oyster species at down-estuary sites, which is not where pH was likely lowest; also, shell strength in eelgrass increased for native oysters but decreased for non-native oysters. Trade-offs between growth rate and survival were observed at the habitat-scale but to a lesser extent than along the environmental gradient.
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