Understanding patterns of bivalve vulnerability and resilience to ocean acidification

Abstract

Anthropogenic greenhouse gas emissions, including carbon dioxide, are causing an unprecedented rate of global warming. Carbon dioxide emissions are additionally causing ocean acidification; a process that decreases the pH and carbonate saturation state of seawater. Ocean acidification is particularly stressful for marine calcifiers; organisms that build calcium carbonate shells or skeletons. Marine bivalves build calcium carbonate shells that they use as a support for their growing tissues, and as protection from predation. Bivalves are osmoconformers, and have limited mobility, meaning that they are particularly susceptible to the impacts of thermal stress. Bivalve fisheries generate billions of dollars to the US economy in annual revenue, therefore understanding their response to these two global change stressors is crucial for helping the communities that rely on these fisheries plan for global change. The following studies explore the response of commercially important bivalve species to ocean acidification and warming. Chapter 2 describes an experiment in which the response of king scallops Pecten maximus to ocean acidification was measured under spring and summer temperature regimes. This chapter also introduces the role of calcification site chemistry in dictating the calcification response to ocean acidification. King scallops were exposed to three pCO2 and two temperature treatments for 74 days. Their calcification rates were measured over the experimental period, and the pH of their calcification site (the extrapallial fluid), and tissue condition index were measured at the end of the experiment. King scallop calcification and condition index were resilient to ocean acidification, but showed opposing trends under different seasonal temperatures, highlighting the energetic tradeoffs between these two biological processes, and the importance of temperature in influencing the timing of these processes. Calcification rate was correlated with extrapallial fluid pH, demonstrating the importance of the extrapallial fluid in facilitating calcification. In chapter 3, the full carbonate system of the extrapallial fluid was characterized under ocean acidification and warming in the Atlantic sea scallop Placopecten magellanicus. Additionally, calcification rates, respiration rates, and survivorship were quantified across these treatments. Increased dissolved inorganic carbon concentration in the extrapallial fluid under ocean acidification contributed to an increase in extrapallial fluid carbonate saturation state. However, calcification rates declined under ocean acidification. The sole aspect of the extrapallial fluid carbonate system that was correlated with calcification was pH, suggesting that pH homeostasis may be the most important factor in dictating calcification. Calcification rate was significantly impacted by the interactive effects of ocean acidification and warming, whereby individuals in the highest temperature and pCO2 treatments were the most negatively impacted. These treatments also had an additive negative effect on survivorship. This chapter highlights the importance of studying the combined effects of multiple climate change stressors, and shows that Atlantic sea scallops are highly vulnerable to global change. Chapter 4 builds on this finding by assessing the present day benthic carbonate chemistry and performance of Atlantic sea scallops across their Georges Bank habitat. Calcite saturation state ranged from 0.90 - 6.58, and both shell and tissue condition showed correlations with saturation state. The results of this chapter suggest that multiple aspects of Atlantic sea scallop biology may be negatively impacted by ocean acidification. However, the high regional heterogeneity in carbonate chemistry suggests that some areas within the Atlantic sea scallop fishing grounds may provide environmental conditions that are supportive of Atlantic sea scallop growth, and thus provide carbonate chemistry refugia for future populations of Atlantic sea scallops. Chapter 5 provides an in-depth characterization of the extrapallial fluid carbonate chemistry and elemental composition of four marine (Arctica islandica; Crassostrea virginica; Mya arenaria; Placopecten magellanicus) and one freshwater (Elliptio complanata) bivalve species under ambient seawater conditions. This chapter shows that bivalves have tight control over calcification site chemistry, and demonstrates that bivalves may use this control over calcification site chemistry to dictate shell mineralogy. This chapter shows that several elements are typically depleted in the extrapallial fluid compared to the marine/freshwater environment, including toxic metals and divalent ions that can substitute for calcium in the bivalve shell crystal lattice.