Intense pCO2 and [O2] Oscillations in a Mussel-Seagrass Habitat: Implications for Calcification

Numerous studies have been conducted on the effect of ocean acidification on calcifiers inhabiting nearshore benthic habitats, such as the blue mussel Mytilus edulis. The majority of these experiments was performed under stable CO2 partial pressure (pCO2), carbonate chemistry and oxygen (O2) levels, reflecting present or expected future open ocean conditions. Consequently, levels and variations occurring in coastal habitats, due to biotic and abiotic processes, were mostly neglected, even though these variations largely override global long-term trends. To highlight this hiatus and guide future research, state-of-the-art technologies were deployed to obtain high-resolution time series of pCO2 and [O2] on a mussel patch within a Zostera marina seagrass bed, in Kiel Bay (western Baltic Sea) in August and September 2013. Combining the in situ data with results of discrete sample measurements, a full seawater carbonate chemistry was derived using statistical models. An average pCO2 more than 50 % (~ 640 µatm) higher than current atmospheric levels was found right above the mussel patch. Diel amplitudes of pCO2 were large: 765 ± 310 (mean ± SD). Corrosive conditions for calcium carbonates (Ωarag and Ωcalc < 1) centered on sunrise were found, but the investigated habitat never experienced hypoxia throughout the study period. It is estimated that mussels experience conditions limiting calcification for 12–15 h per day, based on a regional calcium carbonate concentration physiological threshold. Our findings call for more extensive experiments on the impact of fluctuating corrosive conditions on mussels. We also stress the complexity of the interpretation of carbonate chemistry time series data in such dynamic coastal environments

Seagrass beds as ocean acidification refuges for mussels? High resolution measurements of pCO2 and O2 in a Zostera marina and Mytilus edulis mosaic habitat

It has been speculated that macrophytes beds might act as a refuge for calcifiers from ocean acidification. In the shallow nearshores of the western Kiel Bay (Baltic Sea), mussel and seagrass beds are interlacing, forming a mosaic habitat. Naturally, the diverse physiological activities of seagrasses and mussels are affected by seawater carbonate chemistry and they locally modify it in return. Calcification by shellfishes is sensitive to seawater acidity; therefore the photosynthetic activity of seagrasses in confined shallow waters creates favorable chemical conditions to calcification at daytime but turn the habitat less favorable or even corrosive to shells at night. In contrast, mussel respiration releases CO2, turning the environment more favorable for photosynthesis by adjacent seagrasses. At the end of summer, these dynamics are altered by the invasion of high pCO2/low O2 coming from the deep water of the Bay. However, it is in summer that mussel spats settle on the leaves of seagrasses until migrating to the permanent habitat where they will grow adult. These early life phases (larvae/spats) are considered as most sensitive with regard to seawater acidity. So far, the dynamics of CO2 have never been continuously measured during this key period of the year, mostly due to the technological limitations. In this project we used a combination of state-of-the-art technologies and discrete sampling to obtain high-resolution time-series of pCO2 and O2 at the interface between a seagrass and a mussel patch in Kiel Bay in August and September 2013. From these, we derive the entire carbonate chemistry using statistical models. We found the monthly average pCO2 more than 50 % (approx. 640 μatm for August and September) above atmospheric equilibrium right above the mussel patch together with large diel variations of pCO2 within 24 h: 887 ± 331 μatm in August and 742 ± 281 μatm in September (mean ± SD). We observed important daily corrosiveness for calcium carbonates (Ωarag and Ωcalc < 1) centered on sunrise. On the positive side, the investigated habitat never suffered from hypoxia during the study period. We emphasize the need for more experiments on the impact of these acidic conditions on (juvenile) mussels with a focus on the distinct day-night variations observed

Macroalgae may mitigate ocean acidification effects on mussel calcification by increasing pH and its fluctuations

Ocean acidification (OA) is generally assumed to negatively impact calcification rates of marine organisms. At a local scale however, biological activity of macrophytes may generate pH fluctuations with rates of change that are orders of magnitude larger than the long-term trend predicted for the open ocean. These fluctuations may in turn impact benthic calcifiers in the vicinity. Combining laboratory, mesocosm and field studies, such interactions between OA, the brown alga Fucus vesiculosus, the sea grass Zostera marina and the blue mussel Mytilus edulis were investigated at spatial scales from decimetres to 100s of meters in the western Baltic. Macrophytes increased the overall mean pH of the habitat by up to 0.3 units relative to macrophyte-free, but otherwise similar, habitats and imposed diurnal pH fluctuations with amplitudes ranging from 0.3 to more than 1 pH unit. These amplitudes and their impact on mussel calcification tended to increase with increasing macrophyte biomass to bulk water ratio. At the laboratory and mesocosm scales, biogenic pH fluctuations allowed mussels to maintain calcification even under acidified conditions by shifting most of their calcification activity into the daytime when biogenic fluctuations caused by macrophyte activity offered temporal refuge from OA stress. In natural habitats with a low biomass to water body ratio, the impact of biogenic pH fluctuations on mean calcification rates of M. edulis was less pronounced. Thus, in dense algae or seagrass habitats, macrophytes may mitigate OA impact on mussel calcification by raising mean pH and providing temporal refuge from acidification stress

The influence of temperature and seawater carbonate saturation state on 13C–18O bond ordering in bivalve mollusks

© The Author(s), 2013. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Biogeosciences 10 (2013): 4591-4606, doi:10.5194/bg-10-4591-2013.The shells of marine mollusks are widely used archives of past climate and ocean chemistry. Whilst the measurement of mollusk δ18O to develop records of past climate change is a commonly used approach, it has proven challenging to develop reliable independent paleothermometers that can be used to deconvolve the contributions of temperature and fluid composition on molluscan oxygen isotope compositions. Here we investigate the temperature dependence of 13C–18O bond abundance, denoted by the measured parameter Δ47, in shell carbonates of bivalve mollusks and assess its potential to be a useful paleothermometer. We report measurements on cultured specimens spanning a range in water temperatures of 5 to 25 °C, and field collected specimens spanning a range of −1 to 29 °C. In addition we investigate the potential influence of carbonate saturation state on bivalve stable isotope compositions by making measurements on both calcitic and aragonitic specimens that have been cultured in seawater that is either supersaturated or undersaturated with respect to aragonite. We find a robust relationship between Δ47 and growth temperature. We also find that the slope of a linear regression through all the Δ47 data for bivalves plotted against seawater temperature is significantly shallower than previously published inorganic and biogenic carbonate calibration studies produced in our laboratory and go on to discuss the possible sources of this difference. We find that changing seawater saturation state does not have significant effect on the Δ47 of bivalve shell carbonate in two taxa that we examined, and we do not observe significant differences between Δ47-temperature relationships between calcitic and aragonitic taxa.This work was funded by National Science Foundation grants ARC-1215551 to R. A. Eagle and A. K. Tripati, EAR-1024929 to R. A. Eagle and J. M. Eiler, and EAR-0949191 to A. K. Tripati. A. K. Tripati is also supported by the Hellman Fellowship program. Culture of bivalves in Kiel, Germany, was funded by the German Science Foundation (DFG Ei272/21-1, to Anton Eisenhauer) and the European Science Foundation (ESF) Collaborative Research Project CASIOPEIA (04 ECLIM FP08). Determination of bivalve mineralogy by J. B. Ries was funded by National Science Foundation grant OCE-1031995

Calcifying invertebrates succeed in a naturally CO2 enriched coastal habitat but are threatened by high levels of future acidification

CO2 emissions are leading to an acidification of the oceans. Predicting marine community vulnerability towards acidification is difficult, as adaptation processes cannot be accounted for in most experimental studies. Naturally CO2 enriched sites thus can serve as valuable proxies for future changes in community structure. Here we describe a natural analogue site in the Western Baltic Sea. Seawater pCO2 in Kiel Fjord is elevated for large parts of the year due to upwelling of CO2 rich waters. Peak pCO2 values of >230 Pa (>2300 μatm) and pHNBS values of 400 Pa (>4000 μatm). These changes will most likely affect calcification and recruitment, and increase external shell dissolution

Disentangling the Biological and Environmental Control of M. edulis Shell Chemistry

Blue mussel individuals (Mytilus edulis) were cultured at four different salinities (17, 20, 29, and 34). During the course of the experiment, temperature was gradually increased from 6°C to 14°C. Mg/Ca and Sr/Ca ratios of the shell calcite portions produced during the 9 weeks of experimental treatment as well parts that were precipitated before the treatment phase were measured by laser ablation–multicollector–inductively coupled plasma–mass spectrometry. Mg/Ca ratios show a positive correlation with temperature for individuals cultured at salinity 29 and 34 (Mg/Ca (mmol/mol) ∼ (0.2–0.3)*T (°C)), while for individuals cultured at low salinities (17, 20) no trend was observed. Sr/Ca ratios were not affected by temperature but strongly by salinity. The data show very strong biological influence (“individual differences” and “physiological variability”) on elemental ratios (79% on Mg/Ca and 41% on Sr/Ca) in M. edulis calcite. The results challenge the use of blue mussel shell data as environmental proxies

A new mesocosm system to study the effects of environmental variability on marine species and communities

Climate change will shift mean environmental conditions and also increase the frequency and intensity of extreme events, exerting additional stress on ecosystems. While field observations on extremes are emerging, experimental evidence of their biological consequences is rare. Here, we introduce a mesocosm system that was developed to study the effects of environmental variability of multiple drivers (temperature, salinity, pH, light) on single species and communities at various temporal scales (diurnal - seasonal): the Kiel Indoor Benthocosms (KIBs). Both, real-time offsets from field measurements or various dynamic regimes of environmental scenarios, can be implemented, including sinusoidal curve functions at any chosen amplitude or frequency, stochastic regimes matching in situ dynamics of previous years and modeled extreme events. With temperature as the driver in focus, we highlight the strengths and discuss limitations of the system. In addition, we examined the effects of different sinusoidal temperature fluctuation frequencies on mytilid mussel performance. High-frequency fluctuations around a warming mean (+2°C warming, ± 2°C fluctuations, wavelength = 1.5 d) increased mussel growth as did a constant warming of 2°C. Fluctuations at a lower frequency (+2 and ± 2°C, wavelength = 4.5 d), however, reduced the mussels’ growth. This shows that environmental fluctuations, and importantly their associated characteristics (such as frequency), can mediate the strength of global change impacts on a key marine species. The here presented mesocosm system can help to overcome a major short-coming of marine experimental ecology and will provide more robust data for the prediction of shifts in ecosystem structure and services in a changing and fluctuating world

Decreased depth distribution of Fucus vesiculosus (Phaeophyceae) in the Western Baltic: effects of light deficiency and epibionts on growth and photosynthesis

For many coastal areas of the world, a decrease in abundance and depth penetration of perennial macroalgae and seagrasses has been documented and attributed to eutrophication. A surplus of nutrients impairs perennial seaweeds in at least two ways: increased phytoplankton densities reduce the depth penetration of light and in addition filamentous seaweeds and microalgae growing epiphytically shade their perennial hosts. A reduction of depth limit and total abundance has also been observed for the brown seaweed Fucus vesiculosus at many sites in the Baltic Sea. However, in most cases the mechanistic reason for the loss of Fucus has been deduced from observations rather than from experimental evidence. Here, we present results of a two-factorial (water depth/light supply and epibionts) experiment that was run in the Kiel Fjord, western Baltic, from August to October 2005. Performance of F. vesiculosus was recorded by growth and chlorophyll measurements, PI-curves and in situ measurements of the photosynthetic activity as the relative rate of electron transport (rETR). rETR and growth decreased with water depth. Chlorophyll a concentrations increased with reduced light intensities, but this apparently could not compensate for the light deficiency. Epibionts enhanced the negative effect of reduced light conditions on growth. According to these findings we estimated the physiological depth limit of F. vesiculosus in the Kiel Fjord to lie between 4 and 6 m water depth