Description: Benthic foraminifera are unicellular eukaryotes inhabiting sediments of aquatic environments. Several species were shown to store and use nitrate for complete denitrification, a unique energy metabolism among eukaryotes. The population of benthic foraminifera reaches high densities in oxygen-depleted marine habitats, where they play a key role in the marine nitrogen cycle. However, the mechanisms of denitrification in foraminifera are still unknown, and the possibility of a contribution of associated bacteria is debated. Here, we present evidence for a novel eukaryotic denitrification pathway that is encoded in foraminiferal genomes. Large-scale genome and transcriptomes analyses reveal the presence of a denitrification pathway in foraminifera species of the genus Globobulimina. This includes the enzymes nitrite reductase (NirK) and nitric oxide reductase (Nor) as well as a wide range of nitrate transporters (Nrt). A phylogenetic reconstruction of the enzymes' evolutionary history uncovers evidence for an ancient acquisition of the foraminiferal denitrification pathway from prokaryotes. We propose a model for denitrification in foraminifera, where a common electron transport chain is used for anaerobic and aerobic respiration. The evolution of hybrid respiration in foraminifera likely contributed to their ecological success, which is well documented in palaeontological records since the Cambrian period.

Description: 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.

Description: 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.

Description: 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.

Description: Die Meeresstrategie-Rahmenrichtlinie (MSRL) will durch gezielte Maßnahmen bis 2021 den guten Umweltzustand in den europäischen Meeren erreichen. Dazu sind die Kosten und die Nutzen derartiger Schutzmaßnahmen zu ermitteln und abzuwägen. Die Ziele des Forschungsprojektes waren deshalb zweierlei: zum einen der Frage nachzugehen, welche ökonomischen Nutzen durch Maßnahmen zur Belastungsreduktion entstehen, und zum anderen zu untersuchen, wie die Nutzen einer Maßnahme zur Verbesserung der Meeresumwelt nach heutigem Wissensstand quantifiziert werden können. Mit der Kostenseiten befasst sich das Vorhaben nicht. Um die genannten Ziele zu erreichen, wurden im Projekt methodische Grundlagen und darauf basierend ein Mengengerüst zur Monetarisierung von ökonomischen Nutzen durch maritime Schutzmaßnahmen im Rahmen der MSRL-Implementierung entwickelt. Dieses methodische Vorgehen ist daraufhin in zwei Fallstudien (zur Müllreduzierung in der Nordsee und zur Eutrophierungsreduzierung in der Ostsee) auf seine Praktikabilität und Einfachheit hin getestet worden, um die Ergebnisse in die Entwicklung einer praktikablen Handlungsanleitung einfließen zu lassen. Flankierend wurde im Rahmen des Projekts eine Zahlungsbereitschaftsanalyse zur Eutrophierungsreduktion in der Ostsee durchgeführt, deren Ergebnisse in die Arbeiten des internationalen Forschungsnetzwerks BalticSTERN sowie in einer der o.g. Fallstudien eingeflossen sind. Die Ergebnisse des Vorhabens waren demnach eine Abschätzung der Nutzen durch Reduktionsmaßnahmen der Belastungen "Mariner Abfall" und "Eutrophierung", sowie eine Diskussion der damit verbundenen Unsicherheiten und Datenlücken. Außerdem ist über die Zahlungsbereitschaftsanalyse die Wertschätzung der deutschen Bevölkerung für eine Reduzierung der Eutrophierung der Ostsee erhoben worden. Die Erkenntnisse, die im Rahmen des Projektes gesammelt wurden, sind schließlich in die Handlungsanleitung eingeflossen.

Description: 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 〈7.5 are encountered during summer and autumn, average pCO2 values are ~70 Pa (~700 μatm). In contrast to previously described naturally CO2 enriched sites that have suggested a progressive displacement of calcifying auto- and heterotrophic species, the macrobenthic community in Kiel Fjord is dominated by calcifying invertebrates. We show that blue mussels from Kiel Fjord can maintain control rates of somatic and shell growth at a pCO2 of 142 Pa (1400 μatm, pHNBS = 7.7). Juvenile mussel recruitment peaks during the summer months, when high water pCO2 values of ~100 Pa (~1000 μatm) prevail. Our findings indicate that calcifying keystone species may be able to cope with surface ocean pHNBS values projected for the end of this century when food supply is sufficient. However, owing to non-linear synergistic effects of future acidification and upwelling of corrosive water, peak seawater pCO2 in Kiel Fjord and many other productive estuarine habitats could increase to values 〉400 Pa (〉4000 μatm). These changes will most likely affect calcification and recruitment, and increase external shell dissolution.

Description: Brachiopods present a key fossil group for Phanerozoic palaeo-environmental and palaeo-oceanographical reconstructions, owing to their good preservation and abundance in the geological record. Yet to date, hardly any geochemical proxies have been calibrated in cultured brachiopods and only little is known on the mechanisms that control the incorporation of various key elements into brachiopod calcite. To evaluate the feasibility and robustness of multiple Element/Ca ratios as proxies in brachiopods, specifically Li/Ca, B/Ca, Na/Ca, Mg/Ca, Sr/Ca, Ba/Ca, as well as Li/Mg, we cultured Magellania venosa, Terebratella dorsata and Pajaudina atlantica under controlled experimental settings over a period of more than two years with closely monitored ambient conditions, carbonate system parameters and elemental composition of the culture medium. The experimental setup comprised of two control aquariums (pH0 = 8.0 and 8.15, T = 10 °C) and treatments where pCO2−pH (pH1 = 7.6 and pH2 = 7.35), temperature (T = 16 °C) and chemical composition of the culture medium were manipulated. Our results indicate that the incorporation of Li and Mg is strongly influenced by temperature, growth effects as well as carbonate chemistry, complicating the use of Li/Ca, Mg/Ca and Li/Mg ratios as straightforward reliable proxies. Boron partitioning varied greatly between the treatments, however without a clear link to carbonate system parameters or other environmental factors. The partitioning of both Ba and Na varied between individuals, but was not systematically affected by changes in the ambient conditions. We highlight Sr as a potential proxy for DIC, based on a positive trend between Sr partitioning and carbonate chemistry in the culture medium. To explain the observed dependency and provide a quantitative framework for exploring elemental variations, we devise the first biomineralisation model for brachiopods, which results in a close agreement between modelled and measured Sr distribution coefficients. We propose that in order to sustain shell growth under increased DIC, a decreased influx of Ca2+ to the calcifying fluid is necessary, driving the preferential substitution of Sr2+ for Ca2+ in the crystal lattice. Finally, we conducted micro-computed tomography analyses of the shells grown in the different experimental treatments. We present pore space – punctae – content quantification that indicates that shells built under increased environmental stress, and in particular elevated temperature, contain relatively more pore space than calcite, suggesting this parameter as a potential novel proxy for physiological stress and even environmental conditions.

Description: Highlights • Records of hard-bottom communities show regional differences in community dynamics. • Regionally, signs of regime shift were detected. • Shift can be explained by the decline of the foundation species Mytilus sp. • Modelling process revealed three environmental variables explaining the decline. • Regional differences in larval dispersal could explain contrary Mytilus recoveries. Abstract Ecological processes modulate ecosystem functioning and services. Foundation species are those exerting intense control on such processes as both their existence and loss have profound implications on the structure of ecological communities. For the distinction between random fluctuations and directional regime shifts in community composition, long-term records are of strategic need. In this study we present the monitoring of benthic hard-bottom communities over 11 years along seven stations in the SW Baltic Sea. Regional differences were found between the communities of Kiel and Lübeck bights, with the former area displaying signs of regime shift. The decline and near disappearance of the foundational species Mytilus edulis from settlement panels deployed in Kiel Bight correlated with three environmental variables: sea surface temperature, water current speed and chlorophyll a concentration. Thus, low spring temperatures, in some cases reinforced by local maxima of chlorophyll a, correlated with reduced recruitment of Mytilus. Moreover, regional differences of larval dispersal and population connectivity could explain the rapid recovery after disturbance of the mussel populations in Lübeck Bight in contrast to Kiel Bight. Our findings underscore the relevance of long-term monitoring programmes to detect the interactive impacts of global climatic and regional environmental drivers.

Description: CO2-induced ocean acidification and associated decrease of seawater carbonate saturation state contributed to multiple environmental crises in Earth’s history, and currently poses a major threat for marine calcifying organisms. Owing to their high abundance and good preservation in the Phanerozoic geological record, brachiopods present an advantageous taxon of marine calcifiers for palaeo-proxy applications as well as studies on biological mechanism to cope with environmental change. To investigate the geochemical and physiological responses of brachiopods to prolonged low-pH conditions we cultured Magellania venosa, Terebratella dorsata and Pajaudina atlantica under controlled experimental settings over a period of more than two years. Our experiments demonstrate that brachiopods form their calcite shells under strong biological control, which enables them to survive and grow under low-pH conditions and even in seawater strongly undersaturated with respect to calcite (pH = 7.35, Ωcal = 0.6). Using boron isotope (δ11B) systematics including MC-ICP-MS as well as SIMS analyses, validated against in vivo microelectrode measurements, we show that this resilience is achieved by strict regulation of the calcifying fluid pH between the epithelial mantle and the shell. We provide a culture-based δ11B−pH calibration, which as a result of the internal pH regulatory mechanisms deviates from the inorganic borate ion to pH relationship, but confirms a clear yet subtle pH dependency for brachiopods. At a micro-scale level, the incorporation of 11B appears to be principally driven by a physiological gradient across the shell, where the δ11B values of the innermost calcite record the internal calcifying fluid pH while the composition of the outermost layers is also influenced by seawater pH. These findings are of consequence to studies on biomineralisation processes, physiological adaptations as well as past climate reconstructions.

Description: Climate change is driving compositional shifts in ecological communities directly by affecting species and indirectly through changes in species interactions. For example, competitive hierarchies can be inversed when competitive dominants are more susceptible to climate change. The brown seaweed Fucus vesiculosus is a foundation species in the Baltic Sea, experiencing novel interactions with the invasive red seaweed Gracilaria vermiculophylla, which is known for its high tolerance to environmental stress. We investigated the direct and interactive effects of warming and co-occurrence of the two algal species on their performance, by applying four climate change-relevant temperature scenarios: 1) cooling ) 2 °C below ambient – representing past conditions), 2) ambient summer temperature (18 °C), 3) IPCC RCP2.6 warming scenario (1 °C above ambient), and 4) RCP8.5 warming (3 °C above ambient) for 30 days and two compositional levels (mono and co-cultured algae) in a fully-crossed design. The RCP8.5 warming scenario increased photosynthesis, respiration, and nutrients' uptake rates of mono- and co-cultured G. vermiculophylla while growth was reduced. An increase in photosynthesis and essential nutrients' uptake and, at the same time, a growth reduction might result from increasing stress and energy demand of G. vermiculophylla under warming. In contrast, the growth of mono-cultured F. vesiculosus significantly increased in the highest warming treatment (+3 °C). The cooling treatment (−2 °C) exerted a slight negative effect only on co-cultured F. vesiculosus photosynthesis, compared to the ambient treatment. Interestingly, at ambient and warming (RCP2.6 and RCP8.5 scenarios) treatments, both F. vesiculosus and G. vermiculophylla appear to benefit from the presence of each other. Our results suggest that short exposure of F. vesiculosus to moderate or severe global warming scenarios may not directly affect or even slightly enhance its performance, while G. vermiculophylla net performance (growth) could be directly hampered by warming.