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The current increase in atmospheric CO2 concentration induces changes in the seawater carbonate system resulting in decreased pH and calcium carbonate saturation state, a phenomenon called ocean acidification (OA). OA has long been considered as a major threat to echinoderms because their extensive endoskeleton is made of high‑magnesium calcite, one of the most soluble forms of calcium carbonate. Numerous studies addressed this question in sea urchins, but very few questioned the impact of OA on the sea star skeleton, although members of this taxon do not compensate their extracellular pH, contrary to most sea urchins. In the present study, adults of the common sea star, Asterias rubens from Kiel Fjord, a site experiencing natural acidification events exceeding pCO2 levels of 2500 μatm, were chronically exposed to different levels of simulated ocean acidification (pHT-SW 8.0, 7.4, 7.2), encompassing present and future conditions, for the duration of 109 days. Corrosion and mechanical properties of skeletal elements were studied using scanning electron microscopy, three-point bending tests as well as nanoindentation. The spines were significantly corroded at pHT-SW 7.4 and below while the ambulacral plates were only affected at pHT-SW 7.2. Nanoindentation of newly formed spines and ambulacral plates did not reveal significant CO2-induced differences in skeleton hardness or elasticity across treatments. Results of three-point bending tests revealed significantly reduced characteristic strength and fracture force of ambulacral plates from the median arm segment at pHT-SW 7.4 and below. These plates are those supporting the tube feet involved in the opening of bivalves during feeding and in the animal attachment to the substrate. Under reduced seawater pH, this might result in fracture of sea star plates during predation on mussel. The present results predict a possible impact of ocean acidification on the skeletal integrity of a marine keystone predator.
Aim: Experimental simulation of near‐future ocean acidification (OA) has been demonstrated to affect growth and development of echinoderm larval stages through energy allocation towards ion and pH compensatory processes. To date, it remains largely unknown how major pH regulatory systems and their energetics are affected by trans‐generational exposure to near‐future acidification levels. Methods: Here, we used the common sea star Asterias rubens in a reciprocal transplant experiment comprising different combinations of OA scenarios, to study trans‐generational plasticity using morphological and physiological endpoints. Results: Acclimation of adults to pHT 7.2 (pCO2 3500 μatm) led to reductions in feeding rates, gonad weight and fecundity. No effects were evident at moderate acidification levels (pHT 7.4; pCO2 2000 μatm). Parental pre‐acclimation to pHT 7.2 for 85 days reduced developmental rates even when larvae were raised under moderate and high pH conditions, whereas pre‐acclimation to pHT 7.4 did not alter offspring performance. Microelectrode measurements and pharmacological inhibitor studies carried out on larval stages demonstrated that maintenance of alkaline gastric pH represents a substantial energy sink under acidified conditions that may contribute up to 30% to the total energy budget. Conclusion: Parental pre‐acclimation to acidification levels that are beyond the pH that is encountered by this population in its natural habitat (eg, pHT 7.2) negatively affected larval size and development, potentially through reduced energy transfer. Maintenance of alkaline gastric pH and reductions in maternal energy reserves probably constitute the main factors for a reduced juvenile recruitment of this marine keystone species under simulated OA.
Warming and acidification of the oceans as a consequence of increasing CO2-concentrations occur at large scales. Numerous studies have shown the impact of single stressors on individual species. However, studies on the combined effect of multiple stressors on a multi-species assemblage, which is ecologically much more realistic and relevant, are still scarce. Therefore, we orthogonally crossed the two factors warming and acidification in mesocosm experiments and studied their single and combined impact on the brown alga Fucus vesiculosus associated with its natural community (epiphytes and mesograzers) in the Baltic Sea in all seasons (from April 2013 to April 2014). We superimposed our treatment factors onto the natural fluctuations of all environmental variables present in the Benthocosms in so-called delta-treatments. Thereby we compared the physiological responses of F. vesiculosus (growth and metabolites) to the single and combined effects of natural Kiel Fjord temperatures and pCO2 conditions with a 5 °C temperature increase and/or pCO2 increase treatment (1100 ppm in the headspace above the mesocosms). Responses were also related to the factor photoperiod which changes over the course of the year. Our results demonstrate complex seasonal pattern. Elevated pCO2 positively affected growth of F. vesiculosus alone and/or interactively with warming. The response direction (additive, synergistic or antagonistic), however, depended on season and daylength. The effects were most obvious when plants were actively growing during spring and early summer. Our study revealed for the first time that it is crucial to always consider the impact of variable environmental conditions throughout all seasons. In summary, our study indicates that in future F. vesiculosus will be more affected by detrimental summer heat-waves than by ocean acidification although the latter consequently enhances growth throughout the year. The mainly negative influence of rising temperatures on the physiology of this keystone macroalga may alter and/or hamper its ecological functions in the shallow coastal ecosystem of the Baltic Sea.
Global change exposes brown algal Fucus vesiculosus populations to increasing temperature and pCO2, which may threaten individuals, in particular the early life-stages. Genetic diversity of F. vesiculosus populations is low in the Baltic compared to Atlantic populations. This might jeopardise their potential for adaptation to environmental changes. Here, we report on the responses of early life-stage F. vesiculosus to warming and acidification in a near-natural scenario maintaining natural and seasonal variation (spring 2013–2014) of the Kiel Fjord in the Baltic Sea, Germany (54°27ʹN, 10°11ʹW). We assessed how stress sensitivity differed among sibling groups and how genetic diversity of germling populations affected their stress tolerance. Warming increased growth rates of Fucus germlings in spring and in early summer, but led to higher photoinhibition in spring and decreased their survival in late summer. Acidification increased germlings' growth in summer but otherwise showed much weaker effects than warming. During the colder seasons (autumn and winter), growth was slow while survival was high compared to spring and summer, all at ambient temperatures. A pronounced variation in stress response among genetically different sibling groups (full-sib families) suggests a genotypic basis for this variation and thus a potential for adaptation for F. vesiculosus populations to future conditions. Corroborating this, survival in response to warming in populations with higher diversity was better than the mean survival of single sibling groups. We conclude that impacts on early life-stages depend on the combination of stressors and season and that genetic variation is crucial for the tolerance to global change stress.
About 30% of the anthropogenically released CO2 is taken up by the oceans; such uptake causes surface ocean pH to decrease and is commonly referred to as ocean acidification (OA). Foraminifera are one of the most abundant groups of marine calcifiers, estimated to precipitate ca. 50 % of biogenic calcium carbonate in the open oceans. We have compiled the state of the art literature on OA effects on foraminifera, because the majority of OA research on this group was published within the last three years. Disparate responses of this important group of marine calcifiers to OA were reported, highlighting the importance of a process-based understanding of OA effects on foraminifera. We cultured the benthic foraminifer Ammonia sp. under a range of carbonate chemistry manipulation treatments to identify the parameter of the carbonate system causing the observed effects. This parameter identification is the first step towards a process-based understanding. We argue that CO3 is the parameter affecting foraminiferal size-normalized weights (SNWs) and growth rates. Based on the presented data, we can confirm the strong potential of Ammonia sp. foraminiferal SNW as a CO3 proxy.
Seaweeds are key species of the Baltic Sea benthic ecosystems. They are the substratum of numerous fouling epibionts like bryozoans and tubeworms. Several of these epibionts bear calcified structures and could be impacted by the high pCO2 events of the late summer upwellings in the Baltic nearshores. Those events are expected to increase in strength and duration with global change and ocean acidification. If calcifying epibionts are impacted by transient acidification as driven by upwelling events, their increasing prevalence could cause a shift of the fouling communities toward fleshy species. The aim of the present study was to test the sensitivity of selected seaweed macrofoulers to transient elevation of pCO2 in their natural microenvironment, i.e. the boundary layer covering the thallus surface of brown seaweeds. Fragments of the macroalga Fucus serratus bearing an epibiotic community composed of the calcifiers Spirorbis spirorbis (Annelida) and Electra pilosa (Bryozoa) and the non-calcifier Alcyonidium hirsutum (Bryozoa) were maintained for 30 days under three pCO2 conditions: natural 460±59 µatm, present-day upwelling1193±166 µatm and future upwelling 3150±446 µatm. Only the highest pCO2 caused a significant reduction of growth rates and settlement of S. spirorbis individuals. Additionally, S. spirorbis settled juveniles exhibited enhanced calcification of 40% during daylight hours compared to dark hours, possibly reflecting a day-night alternation of an acidification-modulating effect by algal photosynthesis as opposed to an acidification-enhancing effect of algal respiration. E. pilosa colonies showed significantly increased growth rates at intermediate pCO2 (1193 µatm) but no response to higher pCO2. No effect of acidification on A. hirsutum colonies growth rates was observed. The results suggest a remarkable resistance of the algal macro-epibionts to levels of acidification occurring at present day upwellings in the Baltic. Only extreme future upwelling conditions impacted the tubeworm S. spirorbis, but not the bryozoans.
The brown algae Fucus serratus is one of the major meadow forming algae of the Western Baltic Sea nearshore ecosystem. At the end of summer, those meadows are exposed to local upwelling suddenly increasing the pCO2 and DIC up to 2500 µatm and 2250 µmol/kg resp., for period of days to weeks. This study investigates the growth response of summer's vegetative Fucus serratus to elevated pCO2 (1350 and 4080 µatm) during a 40 days laboratory incubation. After 10 days, increases of growth rates of 20 % and 47 % of the control were observed in the 1350 and 4080 µatm pCO2 treatments respectively. Beyond 20 days, the growth rates collapsed in all treatments due to nutrients shortage, as demonstrated by high C:N ratios (95:1) and low N tissue content (0.04 % of dry weight). The collapse occurs faster at higher pCO2. On day 30, growth rates were reduced by 40 % and 100 % relative to the control at 1350 and 4080 µatm respectively. These results are consistent with a fertilizing effect of elevated pCO2 on Fucus serratus presumably linked to the transition from active HCO3- to passive CO2(aq) uptake. This positive effect is limited by nutrients resources, low seawater dissolved inorganic N and P and shortage of the nutrients reserves accumulated over the previous autumn and winter.
Calcifying foraminifera are expected to be endangered by ocean acidification; however, the response of a complete community kept in natural sediment and over multiple generations under controlled laboratory conditions has not been constrained to date. During 6 months of incubation, foraminiferal assemblages were kept and treated in natural sediment with pCO2-enriched seawater of 430, 907, 1865 and 3247 µatm pCO2. The fauna was dominated by Ammonia aomoriensis and Elphidium species, whereas agglutinated species were rare. After 6 months of incubation, pore water alkalinity was much higher in comparison to the overlying seawater. Consequently, the saturation state of Omega calc was much higher in the sediment than in the water column in nearly all pCO2 treatments and remained close to saturation. As a result, the life cycle (population density, growth and reproduction) of living assemblages varied markedly during the experimental period, but was largely unaffected by the pCO2 treatments applied. According to the size-frequency distribution, we conclude that foraminifera start reproduction at a diameter of 250 µm. Mortality of living Ammonia aomoriensis was unaffected, whereas size of large and dead tests decreased with elevated pCO2 from 285 µm (pCO2 from 430 to 1865 µatm) to 258 µm (pCO2 3247 µatm). The total organic content of living Ammonia aomoriensis has been determined to be 4.3% of CaCO3 weight. Living individuals had a calcium carbonate production rate of 0.47 g/m**2/a, whereas dead empty tests accumulated a rate of 0.27 g /m**2/a. Although Omega calc was close to 1, approximately 30% of the empty tests of Ammonia aomoriensis showed dissolution features at high pCO2 of 3247 µatm during the last 2 months of incubation. In contrast, tests of the subdominant species, Elphidium incertum, stayed intact. Our results emphasize that the sensitivity to ocean acidification of the endobenthic foraminifera Ammonia aomoriensis in their natural sediment habitat is much lower compared to the experimental response of specimens isolated from the sediment.
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