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.

Acid sulfate soil induced acidification of estuarine areas used for the production of Sydney Rock oysters, Saccostrea glomerata

This study investigated estuarine acidification, associated with drainage and excavation of acid sulfate soils, in areas used for commercial cultivation of Sydney rock oysters (Saccostrea glomerata). Regular measurements of pH and electrical conductivity were collected in oyster cultivation areas and acidified reaches of the Hastings River estuary and Port Stephens estuary located on the mid north coast of New South Wales, Australia. Water quality information from acidified floodplain drains was also collected in the Hastings River following heavy rainfall. Both estuaries experienced acidification of tributaries following periods of heavy rainfall. Drain outflow waters were acidic (pH < 3.5); contained elevated concentrations of iron, aluminium, manganese and zinc; and polluted areas used for oyster production. The extent and duration of estuarine acidification events was capable of causing a variety of short- and long-term impacts to oysters as well as other aquatic organisms in affected areas.

Long-term trends in calcifying plankton and pH in the North Sea

Relationships between six calcifying plankton groups and pH are explored in a highly biologically productive and data-rich area of the central North Sea using time-series datasets. The long-term trends show that abundances of foraminiferans, coccolithophores, and echinoderm larvae have risen over the last few decades while the abundances of bivalves and pteropods have declined. Despite good coverage of pH data for the study area there is uncertainty over the quality of this historical dataset; pH appears to have been declining since the mid 1990s but there was no statistical connection between the abundance of the calcifying plankton and the pH trends. If there are any effects of pH on calcifying plankton in the North Sea they appear to be masked by the combined effects of other climatic (e.g. temperature), chemical (nutrient concentrations) and biotic (predation) drivers. Certain calcified plankton have proliferated in the central North Sea, and are tolerant of changes in pH that have occurred since the 1950s but bivalve larvae and pteropods have declined. An improved monitoring programme is required as ocean acidification may be occurring at a rate that will exceed the environmental niches of numerous planktonic taxa, testing their capacities for acclimation and genetic adaptation.

Impacts of ocean acidification on marine shelled molluscs

Over the next century, elevated quantities of atmospheric CO₂ are expected to penetrate into the oceans, causing a reduction in pH (−0.3/−0.4 pH unit in the surface ocean) and in the concentration of carbonate ions (so-called ocean acidification). Of growing concern are the impacts that this will have on marine and estuarine organisms and ecosystems. Marine shelled molluscs, which colonized a large latitudinal gradient and can be found from intertidal to deep-sea habitats, are economically and ecologically important species providing essential ecosystem services including habitat structure for benthic organisms, water purification and a food source for other organisms. The effects of ocean acidification on the growth and shell production by juvenile and adult shelled molluscs are variable among species and even within the same species, precluding the drawing of a general picture. This is, however, not the case for pteropods, with all species tested so far, being negatively impacted by ocean acidification. The blood of shelled molluscs may exhibit lower pH with consequences for several physiological processes (e.g. respiration, excretion, etc.) and, in some cases, increased mortality in the long term. While fertilization may remain unaffected by elevated pCO₂, embryonic and larval development will be highly sensitive with important reductions in size and decreased survival of larvae, increases in the number of abnormal larvae and an increase in the developmental time. There are big gaps in the current understanding of the biological consequences of an acidifying ocean on shelled molluscs. For instance, the natural variability of pH and the interactions of changes in the carbonate chemistry with changes in other environmental stressors such as increased temperature and changing salinity, the effects of species interactions, as well as the capacity of the organisms to acclimate and/or adapt to changing environmental conditions are poorly described.

A developmental and energetic basis linking larval oyster shell formation to acidification sensitivity

Acidified waters are impacting commercial oyster production in the U.S. Pacific Northwest and favorable carbonate chemistry conditions are predicted to become less frequent. Within 48 hours of fertilization, unshelled Pacific oyster (Crassostrea gigas) larvae precipitate roughly 90% of their body weight as calcium carbonate. We measured stable carbon isotopes in larval shell and tissue and in algal food and seawater dissolved inorganic carbon in a longitudinal study of larval development and growth. Using these data and measured biochemical composition of larvae we show that sensitivity of initial shell formation to ocean acidification results from diminished ability to isolate calcifying fluid from surrounding seawater, a limited energy budget dependent, and a strong kinetic demand for calcium carbonate precipitation. Our results highlight an important link between organism physiology and mineral kinetics in larval bivalves and suggest the consideration of mineral kinetics may improve understanding winners and losers in a high CO₂ world.

Early exposure of bay scallops (Argopecten irradians) to high CO2 causes a decrease in larval shell growth

Ocean acidification, characterized by elevated pCO₂ and the associated decreases in seawater pH and calcium carbonate saturation state (Ω), has a variable impact on the growth and survival of marine invertebrates. Larval stages are thought to be particularly vulnerable to environmental stressors, and negative impacts of ocean acidification have been seen on fertilization as well as on embryonic, larval, and juvenile development and growth of bivalve molluscs. We investigated the effects of high CO₂ exposure (resulting in pH = 7.39, Ω_ar = 0.74) on the larvae of the bay scallop Argopecten irradians from 12 h to 7 d old, including a switch from high CO₂ to ambient CO₂ conditions (pH = 7.93, Ω_ar = 2.26) after 3 d, to assess the possibility of persistent effects of early exposure. The survival of larvae in the high CO₂ treatment was consistently lower than the survival of larvae in ambient conditions, and was already significantly lower at 1 d. Likewise, the shell length of larvae in the high CO₂ treatment was significantly smaller than larvae in the ambient conditions throughout the experiment and by 7 d, was reduced by 11.5%. This study also demonstrates that the size effects of short-term exposure to high CO₂ are still detectable after 7 d of larval development; the shells of larvae exposed to high CO₂ for the first 3 d of development and subsequently exposed to ambient CO₂ were not significantly different in size at 3 and 7 d than the shells of larvae exposed to high CO₂ throughout the experiment.

Effects of seawater temperature and pH on the boring rates of the sponge Cliona celata in scallop shells

Warmer, more acidic water resulting from greenhouse gas emissions could influence ecosystem processes like bioerosion of calcifying organisms. Based on summer-maxima values (temperature = 26 °C; pH = 8.1) at a collection site in New York (40°56″ N, 72°30″ W), explants of the boring sponge Cliona celata Grant, 1826 were grown for 133 days on scallop shells in seawater ranging from current values to one scenario predicted for the year 2100 (T = 31 °C; pH = 7.8). High water temperature had little effect on sponge growth, survival, or boring rates. Lower pH slightly reduced sponge survival, while greatly influencing shell boring. At pH = 7.8, sponges bored twice the number of papillar holes and removed two times more shell weight than at pH = 8.1. Greater erosion resulted in weaker scallop shells. This study suggests that lower seawater pH may increase boring rates of C. celata in shellfish, with potentially severe implications for wild and farmed shellfish populations.

Predicting the response of molluscs to the impact of ocean acidification

Elevations in atmospheric carbon dioxide (CO₂) are anticipated to acidify oceans because of fundamental changes in ocean chemistry created by CO₂ absorption from the atmosphere. Over the next century, these elevated concentrations of atmospheric CO₂ are expected to result in a reduction of the surface ocean waters from 8.1 to 7.7 units as well as a reduction in carbonate ion (CO₃²⁻) concentration. The potential impact that this change in ocean chemistry will have on marine and estuarine organisms and ecosystems is a growing concern for scientists worldwide. While species-specific responses to ocean acidification are widespread across a number of marine taxa, molluscs are one animal phylum with many species which are particularly vulnerable across a number of life-history stages. Molluscs make up the second largest animal phylum on earth with 30,000 species and are a major producer of CaCO₃. Molluscs also provide essential ecosystem services including habitat structure and food for benthic organisms (i.e., mussel and oyster beds), purification of water through filtration and are economically valuable. Even sub lethal impacts on molluscs due to climate changed oceans will have serious consequences for global protein sources and marine ecosystems.

Short- and long-term consequences of larval stage exposure to constantly and ephemerally elevated carbon dioxide for marine bivalve populations (update)

While larval bivalves are highly sensitive to ocean acidification, the basis for this sensitivity and the longer-term implications of this sensitivity are unclear. Experiments were performed to assess the short-term (days) and long-term (months) consequences of larval stage exposure to varying CO₂ concentrations for calcifying bivalves. Higher CO₂ concentrations depressed both calcification rates assessed using ⁴⁵Ca uptake and RNA : DNA ratios in Mercenaria mercenaria and Argopecten irradians larvae with RNA : DNA ratios being highly correlated with larval growth rates (r²>0.9). These findings suggested that high CO₂ has a cascading negative physiological impact on bivalve larvae stemming in part from lower calcification rates. Exposure to elevated CO₂ during the first four days of larval development significantly depressed A. irradians larval survival rates, while a 10-day exposure later in larval development did not, demonstrating the extreme CO₂ sensitivity of bivalve larvae during first days of development. Short- (weeks) and long-term (10 month) experiments revealed that individuals surviving exposure to high CO₂ during larval development grew faster when exposed to normal CO₂ as juveniles compared to individuals reared under ambient CO₂ as larvae. These increased growth rates could not, however, overcome size differences established during larval development, as size deficits of individuals exposed to even moderate levels of CO₂ as larvae were evident even after 10 months of growth under normal CO₂ concentrations. This “legacy effect” emphasizes the central role larval stage CO₂ exposure can play in shaping the success of modern-day bivalve populations.

Environmental salinity modulates the effects of elevated CO2 levels on juvenile hard shell clams, Mercenaria mercenaria

Ocean acidification due to increasing atmospheric CO₂ concentrations results in a decrease in seawater pH and shifts in the carbonate chemistry that can negatively affect marine organisms. Marine bivalves such as the hard shell clams Mercenaria mercenaria serve as ecosystem engineers in estuaries and coastal zones of the western Atlantic and, as for many marine calcifiers, are sensitive to the impacts of ocean acidification. In estuaries, the effects of ocean acidification can be exacerbated by low buffering capacity of brackish waters, acidic inputs from freshwaters and land, and/or the negative effects of salinity on organisms’ physiology. We determined the interactive effects of 21 weeks of exposure to different levels of CO₂ (~395, 800 and 1500 µatm corresponding to pH of 8.2, 8.1 and 7.7 respectively) and salinity (32 vs. 16) on biomineralization, shell properties and energy metabolism of juveniles of the hard shell clam M. mercenaria. Low salinity had profound effects on survival, energy metabolism and biomineralization of hard shell clams and modulated their responses to elevated P_CO2. Negative effects of low salinity in juvenile clams were mostly due to the strongly elevated basal energy demand indicating energy deficiency that led to reduced growth, elevated mortality and impaired shell maintenance (evidenced by the extensive damage to the periostracum). The effects of elevated P_CO2 on physiology and biomineralization of hard shell clams were more complex. Elevated P_CO2 (~800-1500 µatm) had no significant effects on standard metabolic rates (indicative of the basal energy demand), but affected growth and shell mechanical properties in juvenile clams. Moderate hypercapnia (~800 µatm P_CO2) increased shell and tissue growth and reduced mortality of juvenile clams in high salinity exposures; however, these effects were abolished under the low salinity conditions or at high P_CO2 (~1500 µatm). Mechanical properties of the shell (measured as microhardness and fracture toughness of the shells) were negatively affected by elevated CO₂ alone or in combination with low salinity, which may have important implications for protection against predators or environmental stressors. Our data indicate that environmental salinity can strongly modulate responses to ocean acidification in hard shell clams and thus should be taken into account when predicting the effects of ocean acidification on estuarine bivalves.