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

Sensitivity of A. islandica and M. edulis towards environmental change: a threat to the bivalves - an opportunity for palaeo-climatology?

As a major green house gas, CO2 causes global warming which further induces changes in other climate parameters like precipitation and salinity. Additionally as about one-third of the atmospheric CO2 is absorbed by surface waters, the oceans become acidified. Bivalve shell production is costly and should therefore be sensitive to environmental stress. Water pCO2, salinity and temperature changes may be factors that increase physiological stress and thus, can reduce fitness, muscle strength, shell growth, shell stability and finally the bivalves’ ecological performance. The improvement of climate models requires a better understanding of climate history. The ratios of stable Ca isotopes and of divalent substituents of Ca (e.g. Mg and Sr) in bivalve shells depend on seawater temperatures and can therefore theoretically be used as archives of past seawater climates. In two 2-factorial experimental approaches (temperature vs. salinity, temperature vs. pCO2), this work investigates the influence of water temperature, salinity and pCO2 on shell growth, mortality, condition index (Ci = soft tissue weight / shell weight), lipofuscin content in the soft tissue (by fluorometry), shell stability (with a texture analyzer), shell Mg / Ca and Sr / Ca ratios (by optical emission spectrometry) and shell Ca isotope fractionation (Δ44/40Ca, by mass spectrometry) of the two bivalve species Arctica islandica and Mytilus edulis. Additionally, in a feeding assay, we tested the defence capability of M. edulis towards predation by starfish Asterias rubens. Lipofuscin accumulation, growth rates and mortalities indicate that M. edulis is rather an estuarine than a fully marine species. Independent of the respective salinity, however, condition and growth of this species are strongly controlled by temperature. In the Baltic Sea, a positive temperature effect on shell stability will presumably be stronger than a negative salinity effect. A. islandica is a species adapted to high salinity and low temperatures. This could be shown by mortalities and growth rates (salinity) on the one hand and by lipofuscin accumulation, condition index and shell stability (temperature) on the other hand. Both bivalve species that were under investigation in this thesis are largely insensitive to acidifications up to a water pCO2 of about 1400 μatm. Also, the starfish A. rubens did not change its feeding behaviour on M. edulis that were cultured under acidic conditions. Increasing temperature and decreasing salinity, in summary, will most likely shift distributions of M. edulis and A. islandica in the Baltic Sea towards the higher-saline and cooler North-Western areas. It became obvious that most of the shell chemistry characteristics investigated in this study can only be explained by a tightly biologically controlled shell formation. The DSr proxy for seawater Sr / Ca ratios (M. edulis) respectively for salinity (A. islandica) is applicable in both species. The Ca isotope (Δ44/40Ca)-temperature proxy in A. islandica has a shallow slope but is independent of salinity. Δ44/40Ca in M. edulis shells, with regard to our results cannot be used as a temperature proxy. Mg / Ca in M. edulis calcite, however, increases very consistently and exponentially with temperature, though Mg / Ca is influenced by salinity and water pCO2, too

Wochenbericht R.V. Littorina L19-10

02.09. bis 06.09.201

Sensitivität von A. islandica und M. edulis gegenüber Umweltveränderungen: Eine Gefahr für die Muscheln - eine Chance für die Paläoklimatologie?

As a major green house gas, CO2 causes global warming which further induces changes in other climate parameters like precipitation and salinity. Additionally as about one-third of the atmospheric CO2 is absorbed by surface waters, the oceans become acidified. Bivalve shell production is costly and should therefore be sensitive to environmental stress. Water pCO2, salinity and temperature changes may be factors that increase physiological stress and thus, can reduce fitness, muscle strength, shell growth, shell stability and finally the bivalves’ ecological performance. The improvement of climate models requires a better understanding of climate history. The ratios of stable Ca isotopes and of divalent substituents of Ca (e.g. Mg and Sr) in bivalve shells depend on seawater temperatures and can therefore theoretically be used as archives of past seawater climates. In two 2-factorial experimental approaches (temperature vs. salinity, temperature vs. pCO2), this work investigates the influence of water temperature, salinity and pCO2 on shell growth, mortality, condition index (Ci = soft tissue weight / shell weight), lipofuscin content in the soft tissue (by fluorometry), shell stability (with a texture analyzer), shell Mg / Ca and Sr / Ca ratios (by optical emission spectrometry) and shell Ca isotope fractionation (Δ44/40Ca, by mass spectrometry) of the two bivalve species Arctica islandica and Mytilus edulis. Additionally, in a feeding assay, we tested the defence capability of M. edulis towards predation by starfish Asterias rubens. Lipofuscin accumulation, growth rates and mortalities indicate that M. edulis is rather an estuarine than a fully marine species. Independent of the respective salinity, however, condition and growth of this species are strongly controlled by temperature. In the Baltic Sea, a positive temperature effect on shell stability will presumably be stronger than a negative salinity effect. A. islandica is a species adapted to high salinity and low temperatures. This could be shown by mortalities and growth rates (salinity) on the one hand and by lipofuscin accumulation, condition index and shell stability (temperature) on the other hand. Both bivalve species that were under investigation in this thesis are largely insensitive to acidifications up to a water pCO2 of about 1400 μatm. Also, the starfish A. rubens did not change its feeding behaviour on M. edulis that were cultured under acidic conditions. Increasing temperature and decreasing salinity, in summary, will most likely shift distributions of M. edulis and A. islandica in the Baltic Sea towards the higher-saline and cooler North-Western areas. It became obvious that most of the shell chemistry characteristics investigated in this study can only be explained by a tightly biologically controlled shell formation. The DSr proxy for seawater Sr / Ca ratios (M. edulis) respectively for salinity (A. islandica) is applicable in both species. The Ca isotope (Δ44/40Ca)-temperature proxy in A. islandica has a shallow slope but is independent of salinity. Δ44/40Ca in M. edulis shells, with regard to our results cannot be used as a temperature proxy. Mg / Ca in M. edulis calcite, however, increases very consistently and exponentially with temperature, though Mg / Ca is influenced by salinity and water pCO2, too.Als bedeutendes Treibhausgas verursacht CO2 globale Klimaerwärmung, die wiederum Veränderungen von anderen Klimaparametern wie Niederschlag und Salinität nach sich zieht. Zusätzlich versauern die Meere, da etwa ein Drittel des atmosphärischen CO2 vom Oberflächenwasser absorbiert wird. Für Muscheln ist die Schalenbildung ein ressourcenaufwändiger Prozess, der folglich empfindlich auf umweltbedingten Stress reagieren sollte. Veränderung des pCO2 , der Salinität und der Temperatur des Wassers könnten als physiologische Stressoren wirken und Fitness, Muskelstärke, Schalenwachstum und -stabilität, also letztendlich die ökologische Performance der Muschel verringern. Zur Verbesserung von Klimamodellen muss die Klimageschichte verstanden werden. Das Verhältnis stabiler Kalzium (Ca)-Isotope und divalenter Ca-Substituenten (z.B. Mg und Sr) in Muschelschalen ist abhängig von Wassertemperaturen und könnte deshalb theoretisch als Archiv vergangener Meerwasserklimata genutzt werden. In zwei 2-faktoriellen Experimenten (Temperatur vs. Salinität, Temperatur vs. pCO2) wurde in dieser Arbeit der Einfluss von Wassertemperatur, Salinität und pCO2 auf Schalenwachstum, Mortalität, Verfassung (Condition Index = Weichkörpergewicht / Schalengewicht), Lipofuszingehalt des Weichkörpers (per Fluorometrie), Schalenstabilität (per Texture Analyzer) sowie auf das Verhältnis von Mg / Ca und Sr / Ca (per optischer Emissionsspektrometrie) und Kalziumisotopenfraktionierung (Δ44/40Ca, per Massenspektrometrie) in Muschelschalen der beiden Arten Arctica islandica und Mytilus edulis untersucht. Zudem wurde die Verteidigungsfähigkeit von M. edulis gegen Prädation durch den Seestern Asteria rubens in einem Fütterungsexperiment getestet. Lipofuszinakkumulation, Wachstums- und Sterblichkeitsraten zeigen an, dass es sich bei M. edulis eher um eine Brackwasserart handelt. Unabhängig von der jeweiligen Salinitätsstufe hängen Verfassung und Wachstum dieser Art aber stark von der Temperatur ab. Bezüglich der Schalenstabilität von M. edulis wird in der Ostsee voraussichtlich ein positiver Temperatureffekt über einen negativen Salinitätseffekt überwiegen. A. islandica ist eine an hohe Salinitäten und niedrige Temperaturen angepasste Art. Dies konnte einerseits durch Mortalität und Wachstumsraten (Salinität) und Lipofuszinakkumulation, Verfassung und Schalenstabilität (Temperatur) gezeigt werden. Beide in dieser Arbeit untersuchten Muschelarten sind äußerst unempfindlich gegenüber Versauerung bis zu einem pCO2 von etwa 1400 μatm. Zudem änderte der Seestern A. rubens sein Fraßverhalten gegenüber unter sauren Bedingungen gehälterten Muscheln nicht. In der Summe werden steigende Temperaturen und sinkende Salinitäten voraussichtlich die Verbreitungsgrenzen von M. edulis und A. islandica in Richtung stärker saliner und kälterer Bereiche in der westlichen Ostsee verschieben. Die meisten in dieser Arbeit untersuchten Muschelschalen-Charakteristika können nur mit einer streng biologisch kontrollierten Schalenbildung erklärt werden. Der DSr-Proxy für Meerwasser Sr / Ca -Verhältnisse (M. edulis) bzw. für Salinitäten (A. islandica) ist bei beiden Arten anwendbar. Der Δ44/40Ca-Temperaturproxy weist bei A. islandica eine flache Steigung auf, jedoch unabhängig von der Salinität. Δ44/40Ca in M. edulis Schalen kann unseren Ergebnissen zu Folge nicht als Temperaturproxy verwendet werden. Das Mg / Ca-Verhältnis im Kalzit von M. edulis steigt sehr stetig und exponentiell mit steigender Temperatur an, wird aber zusätzlich von Salinität und pCO2 des Wassers beeinflusst

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