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  • 1
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    Digestion in sea urchin larvae impaired under ocean acidification (2013)
    Nature Publishing Group
    In:  Nature Climate Change, 3 (12). pp. 1044-1049.
    Details
    Publication Date: 2019-09-23
    Description: Larval stages are considered as the weakest link when a species is exposed to challenging environmental changes1, 2. Reduced rates of growth and development in larval stages of calcifying invertebrates in response to ocean acidification might be caused by energetic limitations3. So far no information exists on how ocean acidification affects digestive processes in marine larval stages. Here we reveal alkaline (~pH 9.5) conditions in the stomach of sea urchin larvae. Larvae exposed to decreased seawater pH suffer from a drop in gastric pH, which directly translates into decreased digestive efficiencies and triggers compensatory feeding. These results suggest that larval digestion represents a critical process in the context of ocean acidification, which has been overlooked so far.
    Type: Article , PeerReviewed , info:eu-repo/semantics/article
    Format: text
    Format: text
    DOI: 10.1038/nclimate2028
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    OceanRep: Article in a Scientific Journal - peer-reviewed
  • 2
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    Conditions of Mytilus edulis extracellular body fluids and shell composition in a pH-treatment experiment: Acid-base status, trace elements and delta B-11 (2012)
    AGU (American Geophysical Union)
    In:  Geochemistry, Geophysics, Geosystems, 13 (1). Q01005.
    Details
    Publication Date: 2019-09-23
    Description: Mytilus edulis were cultured for 3 months under six different seawater pCO(2) levels ranging from 380 to 4000 mu atm. Specimen were taken from Kiel Fjord (Western Baltic Sea, Germany) which is a habitat with high and variable seawater pCO(2) and related shifts in carbonate system speciation (e. g., low pH and low CaCO3 saturation state). Hemolymph (HL) and extrapallial fluid (EPF) samples were analyzed for pH and total dissolved inorganic carbon (C-T) to calculate pCO(2) and [HCO3-]. A second experiment was conducted for 2 months with three different pCO(2) levels (380, 1400 and 4000 mu atm). Boron isotopes (delta B-11) were investigated by LA-MC-ICP-MS (Laser Ablation-Multicollector-Inductively Coupled Plasma-Mass Spectrometry) in shell portions precipitated during experimental treatment time. Additionally, elemental ratios (B/Ca, Mg/Ca and Sr/Ca) in the EPF of specimen from the second experiment were measured via ICP-OES (Inductively Coupled Plasma-Optical Emission Spectrometry). Extracellular pH was not significantly different in HL and EPF but systematically lower than ambient water pH. This is due to high extracellular pCO(2) values, a prerequisite for metabolic CO2 excretion. No accumulation of extracellular [HCO3-] was measured. Elemental ratios (B/Ca, Mg/Ca and Sr/Ca) in the EPF increased slightly with pH which is in accordance with increasing growth and calcification rates at higher seawater pH values. Boron isotope ratios were highly variable between different individuals but also within single shells. This corresponds to a high individual variability in fluid B/Ca ratios and may be due to high boron concentrations in the organic parts of the shell. The mean delta B-11 value shows no trend with pH but appears to represent internal pH (EPF) rather than ambient water pH.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1029/2011GC003790
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  • 3
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    Food availability outweighs ocean acidification effects in juvenileMytilus edulis: laboratory and field experiments (2013)
    Wiley
    In:  Global Change Biology, 19 (4). pp. 1017-1027.
    Details
    Publication Date: 2019-09-23
    Description: Ocean acidification is expected to decrease calcification rates of bivalves. Nevertheless in many coastal areas high pCO2 variability is encountered already today. Kiel Fjord (Western Baltic Sea) is a brackish (12-20 g kg-1) and CO2 enriched habitat, but the blue mussel Mytilus edulis dominates the benthic community. In a coupled field and laboratory study we examined the annual pCO2 variability in this habitat and the combined effects of elevated pCO2 and food availability on juvenile M. edulis growth and calcification. In the laboratory experiment, mussel growth and calcification were found to chiefly depend on food supply, with only minor impacts of pCO2 up to 3350 μatm. Kiel Fjord was characterized by strong seasonal pCO2 variability. During summer, maximal pCO2 values of 2500 μatm were observed at the surface and 〉3000 μatm at the bottom. However, the field growth experiment revealed seven times higher growth and calcification rates of M. edulis at a high pCO2 inner fjord field station (mean pCO2 ca. 1000 μatm) in comparison to a low pCO2 outer fjord station (ca. 600 μatm). In addition, mussels were able to outcompete the barnacle Amphibalanus improvisus at the high pCO2 site. High mussel productivity at the inner fjord site was enabled by higher particulate organic carbon concentrations. Kiel Fjord is highly impacted by eutrophication, which causes bottom water hypoxia and consequently high seawater pCO2. At the same time, elevated nutrient concentrations increase the energy availability for filter feeding organisms such as mussels. Thus M. edulis can dominate over a seemingly more acidification resistant species such as A. improvisus. We conclude that benthic stages of M. edulis tolerate high ambient pCO2 when food supply is abundant and that important habitat characteristics such as species interactions and energy availability need to be considered to predict species vulnerability to ocean acidification.
    Type: Article , PeerReviewed
    Format: text
    Format: text
    DOI: 10.1111/gcb.12109
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  • 4
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    CO2-driven seawater acidification differentially affects development and molecular plasticity along life history of fish (Oryzias latipes) (2013)
    Elsevier
    In:  Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology, 165 (2). pp. 119-130.
    Details
    Publication Date: 2020-08-04
    Description: Fish early life stages have been shown to react sensitive to simulated ocean acidification. In particular, acid–base disturbances elicited by altered seawater carbonate chemistry have been shown to induce pathologies in larval fish. However, the mechanisms underlying these disturbances are largely unknown. We used gene expression profiling of genes involved in acid–base regulation and metabolism to investigate the effects of seawater hypercapnia on developing Japanese ricefish (medaka; Oryzias latipes). Our results demonstrate that embryos respond with delayed development during the time window of 2–5 dpf when exposed to a seawater pCO2 of 0.12 and 0.42 kPa. This developmental delay is associated with strong down-regulation of genes from major metabolic pathways including glycolysis (G6PDH), Krebs cycle (CS) and the electron transport chain (CytC). In a second step we identified acid–base relevant genes in different ontogenetic stages (embryos, hatchlings and adults) and tissues (gill and intestine) that are up regulated in response to hypercapnia, including NHE3, NBCa, NBCb, AE1a, AE1b, ATP1a1a.1, ATP1a1b, ATP1b1a, Rhag, Rhbg and Rhcg. Interestingly, NHE3 and Rhcg expressions were increased in response to environmental hypercapnia in all ontogenetic stages and tissues tested, indicating the central role of these proteins in acid–base regulation. Furthermore, the increased expression of genes from amino acid metabolism pathways (ALT1, ALT2, AST1a, AST1b, AST2 and GLUD) suggests that energetic demands of hatchlings are fueled by the breakdown of amino acids. The present study provides a first detailed gene expression analysis throughout the ontogeny of a euryhaline teleost in response to seawater hypercapnia, indicating highest sensitivity in early embryonic stages, when functional ion regulatory epithelia are not yet developed.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1016/j.cbpa.2013.02.005
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  • 5
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    Sour times: seawater acidification effects on growth, feeding behaviour and acid–base status of Asterias rubens and Carcinus maenas (2012)
    Inter Research
    In:  Marine Ecology Progress Series, 459 . pp. 85-98.
    Details
    Publication Date: 2019-09-23
    Description: The impact of seawater acidification on calcifying organisms varies at the species level. If the impact differs between predator and prey in strength and/or sign, trophic interactions may be altered. In the present study, we investigated the impact of 3 different seawater pCO2 levels (650, 1250 and 3500 µatm) on the acid–base status or the growth of 2 predatory species, the common sea star Asterias rubens and the shore crab Carcinus maenas, and tested whether the quantity or size of prey consumed is affected. We exposed both the predators and their prey, the blue mussel Mytilus edulis, over a time span of 10 wk and subsequently performed feeding experiments. Intermediate acidification levels had no significant effect on growth or consumption in either predator species. The highest acidification level reduced feeding and growth rates in sea stars by 56%, while in crabs a 41% decrease in consumption rates of mussels could be demonstrated over the 10 wk experimental period but not in the subsequent shorter feeding assays. Because only a few crabs moulted in the experiment, acidification effects on crab growth could not be investigated. Active extracellular pH compensation by means of bicarbonate accumulation was observed in C. maenas, whereas the coelomic fluid pH in A. rubens remained uncompensated. Acidification did not provoke a measurable shift in prey size preferred by either predator. Mussels exposed to elevated pCO2 were preferred by previously untreated A. rubens but not by C. maenas. The observed effects on species interactions were weak even at the high acidification levels expected in the future in marginal marine habitats such as the Baltic Sea. Our results indicate that when stress effects are similar (and weak) on interacting species, biotic interactions may remain unaffected.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.3354/meps09697
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  • 6
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    Influence of Temperature, Hypercapnia, and Development on the Relative Expression of Different Hemocyanin Isoforms in the Common CuttlefishSepia officinalis (2012)
    Wiley
    In:  Journal of Experimental Zoology Part A: Ecological Genetics and Physiology, 317 (8). pp. 511-523.
    Details
    Publication Date: 2019-09-23
    Description: The cuttlefish Sepia officinalis expresses several hemocyanin isoforms with potentially different pH optima, indicating their reliance on efficient pH regulation in the blood. Ongoing ocean warming and acidification could influence the oxygen-binding properties of respiratory pigments in ectothermic marine invertebrates. This study examined whether S. officinalis differentially expresses individual hemocyanin isoforms to maintain optimal oxygen transport during development and acclimation to elevated seawater pCO2 and temperature. Using quantitative PCR, we measured relative mRNA expression levels of three different hemocyanin isoforms in several ontogenetic stages (embryos, hatchlings, juveniles, and adults), under different temperatures and elevated seawater pCO2. Our results indicate moderately altered hemocyanin expression in all embryonic stages acclimated to higher pCO2, while hemocyanin expression in hatchlings and juveniles remained unaffected. During the course of development, total hemocyanin expression increased independently of pCO2 or thermal acclimation status. Expression of isoform 3 is reported for the first time in a cephalopod in this study and was found to be generally low but highest in the embryonic stages (0.2% of total expression). Despite variable hemocyanin expression, hemolymph total protein concentrations remained constant in the experimental groups. Our data provide first evidence that ontogeny has a stronger influence on hemocyanin isoform expression than the environmental conditions chosen, and they suggest that hemocyanin protein abundance in response to thermal acclimation is regulated by post-transcriptional/translational rather than by transcriptional modifications
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1002/jez.1743
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  • 7
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    Ocean acidification and temperature rise: effects on calcification during early development of the cuttlefish Sepia officinalis (2013)
    Springer
    In:  Marine Biology, 160 (8). pp. 2007-2022.
    Details
    Publication Date: 2018-06-29
    Description: This study investigated the effects of seawater pH (i.e., 8.10, 7.85 and 7.60) and temperature (16 and 19 °C) on (a) the abiotic conditions in the fluid surrounding the embryo (viz. the perivitelline fluid), (b) growth, development and (c) cuttlebone calcification of embryonic and juvenile stages of the cephalopod Sepia officinalis. Egg swelling increased in response to acidification or warming, leading to an increase in egg surface while the interactive effects suggested a limited plasticity of the swelling modulation. Embryos experienced elevated pCO2 conditions in the perivitelline fluid (〉3-fold higher pCO2 than that of ambient seawater), rendering the medium under-saturated even under ambient conditions. The growth of both embryos and juveniles was unaffected by pH, whereas 45Ca incorporation in cuttlebone increased significantly with decreasing pH at both temperatures. This phenomenon of hypercalcification is limited to only a number of animals but does not guarantee functional performance and calls for better mechanistic understanding of calcification processes.
    Type: Article , PeerReviewed , info:eu-repo/semantics/article
    Format: text
    DOI: 10.1007/s00227-012-2059-6
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  • 8
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    Future ocean acidification will be amplified by hypoxia in coastal habitats (2013)
    Springer
    In:  Marine Biology, 160 . pp. 1875-1888.
    Details
    Publication Date: 2019-09-23
    Description: Ocean acidification is elicited by anthropogenic carbon dioxide emissions and resulting oceanic uptake of excess CO2 and might constitute an abiotic stressor powerful enough to alter marine ecosystem structures. For surface waters in gas-exchange equilibrium with the atmosphere, models suggest increases in CO2 partial pressure (pCO2) from current values of ca. 390 μatm to ca. 700–1,000 μatm by the end of the century. However, in typically unequilibrated coastal hypoxic regions, much higher pCO2 values can be expected, as heterotrophic degradation of organic material is necessarily related to the production of CO2 (i.e., dissolved inorganic carbon). Here, we provide data and estimates that, even under current conditions, maximum pCO2 values of 1,700–3,200 μatm can easily be reached when all oxygen is consumed at salinities between 35 and 20, respectively. Due to the nonlinear nature of the carbonate system, the approximate doubling of seawater pCO2 in surface waters due to ocean acidification will most strongly affect coastal hypoxic zones as pCO2 during hypoxia will increase proportionally: we calculate maximum pCO2 values of ca. 4,500 μatm at a salinity of 20 (T = 10 °C) and ca. 3,400 μatm at a salinity of 35 (T = 10 °C) when all oxygen is consumed. Upwelling processes can bring these CO2-enriched waters in contact with shallow water ecosystems and may then affect species performance there as well. We conclude that (1) combined stressor experiments (pCO2 and pO2) are largely missing at the moment and that (2) coastal ocean acidification experimental designs need to be closely adjusted to carbonate system variability within the specific habitat. In general, the worldwide spread of coastal hypoxic zones also simultaneously is a spread of CO2-enriched zones. The magnitude of expected changes in pCO2 in these regions indicates that coastal systems may be more endangered by future global climate change than previously thought.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1007/s00227-012-1954-1
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  • 9
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    Maintenance of coelomic fluid pH in sea urchins exposed to elevated CO2: the role of body cavity epithelia and stereom dissolution (2013)
    Springer
    In:  Marine Biology, 160 (10). pp. 2631-2645.
    Details
    Publication Date: 2019-09-23
    Description: Experimental ocean acidification leads to a shift in resource allocation and to an increased [HCO3 −] within the perivisceral coelomic fluid (PCF) in the Baltic green sea urchin Strongylocentrotus droebachiensis. We investigated putative mechanisms of this pH compensation reaction by evaluating epithelial barrier function and the magnitude of skeleton (stereom) dissolution. In addition, we measured ossicle growth and skeletal stability. Ussing chamber measurements revealed that the intestine formed a barrier for HCO3 − and was selective for cation diffusion. In contrast, the peritoneal epithelium was leaky and only formed a barrier for macromolecules. The ossicles of 6 week high CO2-acclimatised sea urchins revealed minor carbonate dissolution, reduced growth but unchanged stability. On the other hand, spines dissolved more severely and were more fragile following acclimatisation to high CO2. Our results indicate that epithelia lining the PCF space contribute to its acid–base regulation. The intestine prevents HCO3 − diffusion and thus buffer leakage. In contrast, the leaky peritoneal epithelium allows buffer generation via carbonate dissolution from the surrounding skeletal ossicles. Long-term extracellular acid–base balance must be mediated by active processes, as sea urchins can maintain relatively high extracellular [HCO3 −]. The intestinal epithelia are good candidate tissues for this active net import of HCO3 − into the PCF. Spines appear to be more vulnerable to ocean acidification which might significantly impact resistance to predation pressure and thus influence fitness of this keystone species
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1007/s00227-013-2257-x
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  • 10
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    New insights into ion regulation of cephalopod molluscs: a role of epidermal ionocytes in acid-base regulation during embryogenesis (2011)
    American Physiological Society, APS
    In:  American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 301 (6). R1700-R1709.
    Details
    Publication Date: 2019-09-23
    Description: The constraints of an active life in a pelagic habitat led to numerous convergent morphological and physiological adaptations that enable cephalopod molluscs and teleost fishes to compete for similar resources. Here we show for the first time that such convergent developments are also found in the ontogenetic progression of ion regulatory tissues: as in teleost fish epidermal ionocytes scattered on skin and yolk sac of cephalopod embryos appear to be responsible for ionic and acid-base regulation before gill epithelia become functional. Ion and acid-base regulation is crucial in cephalopod embryos, as they are surrounded by a hypercapnic egg fluid with a pCO2 of 0.2-0.4 kPa. Epidermal ionocytes were characterized via immunohistochemistry, in situ hybridization and vital dye staining techniques. We found one group of cells that is recognized by Concavalin A and MitoTracker, which also expresses Na+/H+ exchangers (NHE) and Na+/K+-ATPase. Similar to findings obtained in teleosts these NHE3-rich cells take up sodium in exchange for protons, illustrating the energetic superiority of NHE based proton excretion in marine systems. In vivo electrophysiological techniques demonstrated that acid equivalents are secreted by the yolk and skin integument. Intriguingly, epidermal ionocytes of cephalopod embryos are ciliated as demonstrated by scanning electron microscopy suggesting a dual function of epithelial cells in water convection and ion regulation. These findings add significant knowledge to our mechanistic understanding of hypercapnia tolerance in marine organisms, as it demonstrates that marine taxa which were identified as powerful acid-base regulators during hypercapnic challenges already exhibit strong acid-base regulatory abilities during embryogenesis.
    Type: Article , PeerReviewed
    Format: text
    DOI: 10.1152/ajpregu.00107.2011
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