George G. Waldbusser

Oyster Shell Dissolution Rates in Estuarine Waters: Effects of pH and Shell Legacy

ABSTRACT Oyster shell is a crucial component of healthy oyster reefs. Shell planting has been a main component of oyster restoration efforts in many habitats and has been carried out on scales from individual and grassroots efforts to multiagency efforts across entire estuaries. However, the cycling and lifetime of the shell that makes up the bulk of an oyster reef has only recently received attention, and most of the work to date has focused on the role of epi- and endobionts on shell degradation. Here we report findings from a laboratory study in which we manipulated pH in a flow-through control system using water from the mesohaline mouth of the Patuxent River to measure dissolution rates of intact oyster shell. Shells from the Eastern oyster (Crassostrea virginica Gmelin 1791) with three different legacies were exposed to 4 levels of pH that encompass a range typical of the mesohaline waters of the Chesapeake Bay (∼7.2–7.9 on the NBS scale). Mass loss over a 2-wk period was used to measure dissolution rate on 3 shell legacies: fresh, weathered, and dredged. We found that pH and shell legacy had significant effects on shell dissolution rate, with lower pH increasing dissolution rate. Fresh shell had the highest dissolution rate, followed by weathered then dredged shell. Dissolution rates were significantly different among all 4 pH treatments, except between the lowest (∼7.2) and the next lowest (∼7.4); however, shells lost mass even under noncorrosive conditions (∼7.9). We discuss the implications of our findings to ongoing efforts to understand shell budgets and cycling in oyster reef habitat, the interaction of biological and geochemical agents of shell degradation, and the complexity associated with shell carbonate cycling in the unique milieu of the oyster reef.

Ocean Acidification Has Multiple Modes of Action on Bivalve Larvae.

Ocean acidification (OA) is altering the chemistry of the world’s oceans at rates unparalleled in the past roughly 1 million years. Understanding the impacts of this rapid change in baseline carbonate chemistry on marine organisms needs a precise, mechanistic understanding of physiological responses to carbonate chemistry. Recent experimental work has shown shell development and growth in some bivalve larvae, have direct sensitivities to calcium carbonate saturation state that is not modulated through organismal acid-base chemistry. To understand different modes of action of OA on bivalve larvae, we experimentally tested how pH, PCO2, and saturation state independently affect shell growth and development, respiration rate, and initiation of feeding in Mytilus californianus embryos and larvae. We found, as documented in other bivalve larvae, that shell development and growth were affected by aragonite saturation state, and not by pH or PCO2. Respiration rate was elevated under very low pH (~7.4) with no change between pH of ~ 8.3 to ~7.8. Initiation of feeding appeared to be most sensitive to PCO2, and possibly minor response to pH under elevated PCO2. Although different components of physiology responded to different carbonate system variables, the inability to normally develop a shell due to lower saturation state precludes pH or PCO2 effects later in the life history. However, saturation state effects during early shell development will carry-over to later stages, where pH or PCO2 effects can compound OA effects on bivalve larvae. Our findings suggest OA may be a multi-stressor unto itself. Shell development and growth of the native mussel, M. californianus, was indistinguishable from the Mediterranean mussel, Mytilus galloprovincialis, collected from the southern U.S. Pacific coast, an area not subjected to seasonal upwelling. The concordance in responses suggests a fundamental OA bottleneck during development of the first shell material affected only by saturation state.

Ecosystem effects of shell aggregations and cycling in coastal waters: an example of Chesapeake Bay oyster reefs

Disease, overharvesting, and pollution have impaired the role of bivalves on coastal ecosystems, some to the point of functional extinction. An underappreciated function of many bivalves in these systems is shell formation. The ecological significance of bivalve shell has been recognized; geochemical effects are now more clearly being understood. A positive feedback exists between shell aggregations and healthy bivalve populations in temperate estuaries, thus linking population dynamics to shell budgets and alkalinity cycling. On oyster reefs a balanced shell budget requires healthy long-lived bivalves to maximize shell input per mortality event thereby countering shell loss. Active and dense populations of filter-feeding bivalves couple production of organic-rich waste with precipitation of calcium carbonate minerals, creating conditions favorable for alkalinity regeneration. Although the dynamics of these processes are not well described, the balance between shell burial and metabolic acid production seems the key to the extent of alkalinity production vs. carbon burial as shell. We present an estimated alkalinity budget that highlights the significant role oyster reefs once played in the Chesapeake Bay inorganic-carbon cycle. Sustainable coastal and estuarine bivalve populations require a comprehensive understanding of shell budgets and feedbacks among population dynamics, agents of shell destruction, and anthropogenic impacts on coastal carbonate chemistry.

Redox reactions and weak buffering capacity lead to acidification in the Chesapeake Bay

The combined effects of anthropogenic and biological CO2 inputs may lead to more rapid acidification in coastal waters compared to the open ocean. It is less clear, however, how redox reactions would contribute to acidification. Here we report estuarine acidification dynamics based on oxygen, hydrogen sulfide (H2S), pH, dissolved inorganic carbon and total alkalinity data from the Chesapeake Bay, where anthropogenic nutrient inputs have led to eutrophication, hypoxia and anoxia, and low pH. We show that a pH minimum occurs in mid-depths where acids are generated as a result of H2S oxidation in waters mixed upward from the anoxic depths. Our analyses also suggest a large synergistic effect from river–ocean mixing, global and local atmospheric CO2 uptake, and CO2 and acid production from respiration and other redox reactions. Together they lead to a poor acid buffering capacity, severe acidification and increased carbonate mineral dissolution in the USA’s largest estuary.The potential contribution of redox reactions to acidification in coastal waters is unclear. Here, using measurements from the Chesapeake Bay, the authors show that pH minimum occurs at mid-depths where acids are produced via hydrogen sulfide oxidation in waters mixed upward from anoxic depths.

The Carbonate Chemistry of the “Fattening Line,” Willapa Bay, 2011–2014

Willapa Bay has received a great deal of attention in the context of rising atmospheric CO2 and the concomitant effects of changes in bay carbonate chemistry, referred to as ocean acidification, and the potential effects on the bay’s naturalized Pacific oyster (Crassostrea gigas) population and iconic oyster farming industry. Competing environmental stressors, historical variability in the oyster settlement record, and the absence of adequate historical observations of bay-water carbonate chemistry all conspire to cast confusion regarding ocean acidification as the culprit for recent failures in oyster larval settlement. We present the first measurements of the aqueous CO2 partial pressure (PCO2) and the total dissolved carbonic acid (TCO2) at the “fattening line,” a location in the bay that has been previously identified as optimal for both larval oyster retention and growth, and collocated with a long historical time series of larval settlement. Samples were collected from early 2011 through late 2014. These measurements allow the first rigorous characterization of Willapa Bay aragonite mineral saturation state (Ωar), which has been shown to be of leading importance in determining the initial shell formation and growth of larval Crassostrea gigas. Observations show that the bay is usually below Ωar levels that have been associated with poor oyster hatchery production and with chronic effects noted in experimental work. Bay water only briefly rises to favorable Ωar levels and does so out of phase with optimal thermal conditions for spawning. Thermal and carbonate conditions are thus coincidentally favorable for early larval development for only a few weeks at a time each year. The limited concurrent exceedance of thermal and Ωar thresholds suggests the likelihood of high variability in settlement success, as seen in the historical record; however, estimates of the impact of elevated atmospheric CO2 suggest that pre-industrial Ωar conditions were more persistently favorable for larval development and more broadly coincident with thermal optima.

Coral Reefs and People in a High-CO2 World: Where Can Science Make a Difference to People?

Reefs and People at Risk Increasing levels of carbon dioxide in the atmosphere put shallow, warm-water coral reef ecosystems, and the people who depend upon them at risk from two key global environmental stresses: 1) elevated sea surface temperature (that can cause coral bleaching and related mortality), and 2) ocean acidification. These global stressors: cannot be avoided by local management, compound local stressors, and hasten the loss of ecosystem services. Impacts to people will be most grave where a) human dependence on coral reef ecosystems is high, b) sea surface temperature reaches critical levels soonest, and c) ocean acidification levels are most severe. Where these elements align, swift action will be needed to protect people’s lives and livelihoods, but such action must be informed by data and science. An Indicator Approach Designing policies to offset potential harm to coral reef ecosystems and people requires a better understanding of where CO2-related global environmental stresses could cause the most severe impacts. Mapping indicators has been proposed as a way of combining natural and social science data to identify policy actions even when the needed science is relatively nascent. To identify where people are at risk and where more science is needed, we map indicators of biological, physical and social science factors to understand how human dependence on coral reef ecosystems will be affected by globally-driven threats to corals expected in a high-CO2 world. Western Mexico, Micronesia, Indonesia and parts of Australia have high human dependence and will likely face severe combined threats. As a region, Southeast Asia is particularly at risk. Many of the countries most dependent upon coral reef ecosystems are places for which we have the least robust data on ocean acidification. These areas require new data and interdisciplinary scientific research to help coral reef-dependent human communities better prepare for a high CO2 world.

Perception and Response of the U.S. West Coast Shellfish Industry to Ocean Acidification: The Voice of the Canaries in the Coal Mine

ABSTRACT In the mid-2000s the U.S. west coast oyster industry experienced several years of significant production failures. This industry has been referred to as the “canary in a coal mine” for ocean acidification (OA). Industry-led collaboration with university and government scientists identified a relationship between elevated carbon dioxide in seawater and poor oyster seed production. This multiyear production slow-down resulted in significant economic losses to the industry and spurred state and regionally led initiatives to examine the current and potential future impacts of OA. To examine the perceptions and understanding of OA by the U.S. west coast shellfish industry, a regional survey of the industry was conducted, covering oyster, mussel, clam, geoduck, and abalone producers. The web-based survey addressed four general areas: experience, understanding, concern, and adaptability. There were 86 total respondents from industry, resulting in a response rate of 46% with 96% of respondents answering all 44 questions. Seventy percent of respondents were owners or managers of a shellfish business. Findings from the survey indicate that approximately half of the industry had personally experienced a negative impact from OA. This personal experience generally led to a higher level of concern about OA; however, self-reported level of understanding of OA resulted in slightly less concordance with the level of concern. Greater than 80% of the shellfish industry noted that OA will have consequences today, approximately four times higher than the U.S. publics perception of the threat. Finally, greater than 50% of the industry felt that they would be able to somewhat or definitely adapt to OA.

Evidence of infaunal effects on porewater advection and biogeochemistry in permeable sediments: A proposed infaunal functional group framework

Bioturbating infauna significantly modify reaction and transport processes in permeable sediments, though most studies to date are limited in the scope of species examined. We conducted a comparative field study measuring density-dependent effects of six common bioturbating species on porewater advection and biogeochemistry, across three intertidal permeable sediment habitats. The species in this study are; head-down like deposit feeders (Abarenicola pacifica and Balanoglossus aurantiacus), surface deposit feeders (Diopatra cuprea and Onuphis jenneri) and gallery diffusers (Upogebia pugettensis and Neotrypaea californiensis). Tracer loss from gel diffusers was used to assess relative differences in porewater advection among sites, and porewater peepers were used to measure solute concentrations of carbon, nitrogen, phosphate, and silicate in experimental plots. Characteristic surface features of different infauna were counted and used as a proxy for infaunal density. Density of surface features was then used in regression analyses as an explanatory variable affecting porewater transport and chemistry. Significant infaunal density effects on porewater transport or biogeochemistry were found in all but one species, D. cuprea. The species-specific attributes and mechanisms by which these infauna affect permeable sediment processes are explored. A process based functional group framework is presented for permeable sediments. Bulk granulometric properties also were assessed. There were little to no within-site effects of porosity, hydraulic conductivity, or organic matter on porewater transport and biogeochemistry. However, significant across-site differences in granulometry and site properties were found and these are addressed in relation to infaunal effects on porewater transport and chemistry.

Seagrass habitat metabolism increases short-term extremes and long-term offset of CO2 under future ocean acidification

Significance The impacts of ocean acidification in nearshore estuarine environments remain poorly characterized, despite these areas being some of the most ecologically important habitats in the global ocean. Here, we quantify how rising atmospheric CO2 from the years 1765 to 2100 alters high-frequency carbonate chemistry dynamics in an estuarine seagrass habitat. We find that increasing anthropogenic carbon reduces the ability of the system to buffer natural extremes in CO2. This reduced buffering capacity leads to preferential amplification of naturally extreme low pH and high pCO2(s.w.) events above changes in average conditions, which outpace rates published for atmospheric and open-ocean CO2 change. Seagrass habitat metabolism drives these short-term extreme events, yet ultimately reduces organismal exposure to harmful conditions in future high-CO2 scenarios. The role of rising atmospheric CO2 in modulating estuarine carbonate system dynamics remains poorly characterized, likely due to myriad processes driving the complex chemistry in these habitats. We reconstructed the full carbonate system of an estuarine seagrass habitat for a summer period of 2.5 months utilizing a combination of time-series observations and mechanistic modeling, and quantified the roles of aerobic metabolism, mixing, and gas exchange in the observed dynamics. The anthropogenic CO2 burden in the habitat was estimated for the years 1765–2100 to quantify changes in observed high-frequency carbonate chemistry dynamics. The addition of anthropogenic CO2 alters the thermodynamic buffer factors (e.g., the Revelle factor) of the carbonate system, decreasing the seagrass habitat’s ability to buffer natural carbonate system fluctuations. As a result, the most harmful carbonate system indices for many estuarine organisms [minimum pHT, minimum Ωarag, and maximum pCO2(s.w.)] change up to 1.8×, 2.3×, and 1.5× more rapidly than the medians for each parameter, respectively. In this system, the relative benefits of the seagrass habitat in locally mitigating ocean acidification increase with the higher atmospheric CO2 levels predicted toward 2100. Presently, however, these mitigating effects are mixed due to intense diel cycling of CO2 driven by aerobic metabolism. This study provides estimates of how high-frequency pHT, Ωarag, and pCO2(s.w.) dynamics are altered by rising atmospheric CO2 in an estuarine habitat, and highlights nonlinear responses of coastal carbonate parameters to ocean acidification relevant for water quality management.

Mechanisms to Explain the Elemental Composition of the Initial Aragonite Shell of Larval Oysters

Calcifying organisms face increasing stress from the changing carbonate chemistry of an acidifying ocean, particularly bivalve larvae that live in upwelling regions of the world, such as the coastal and estuarine waters of Oregon (USA). Arguably the first and most significant developmental hurdle faced by larval oysters is formation of their initial prodissoconch I (PDI) shell, upon which further ontological development depends. We measured the minor metal compositions (Sr/Ca, Mg/Ca) of this aragonitic PDI shell and of post-PDI larval Crassostrea gigas shell, as well as the water they were reared in, over ∼20 days for a May and an August cohort in 2011, during which time there was no period of carbonate under-saturation. After testing various methods, we successfully isolated the shell from organic tissue using a 5% active chlorine bleach solution. Elemental compositions (Sr, Mg, C, N) of the shells post treatment showed that shell Sr/Ca ranged from 1.55 to 1.82 mmol/mol; Mg/Ca from 0.60 to 1.11 mmol/mol, similar to the few comparable published data for larval oyster aragonite compositions. We compare these data in light of possible biomineralization mechanisms: an amorphous calcium carbonate (ACC) path, an intercellular path, and a direct-from-seawater path to shell formation via biologically induced inorganic precipitation of aragonite. The last option provides a mechanistic explanation for: 1) the accelerated precipitation rates of biogenic calcification in the absence of a calcifying fluid; 2) consistently elevated precipitation rates at varying ambient-water saturation states; and 3) the high Ca-selectivity of the early-larval calcification despite rapid precipitation rates.