Data compilation on the biological response to ocean acidification: environmental and experimental context of data sets and related literature

The exponential growth of studies on the biological response to ocean acidification over the last few decades has generated a large amount of data. To facilitate data comparison, a data compilation hosted at the data publisher PANGAEA was initiated in 2008 and is updated on a regular basis (doi:10.1594/PANGAEA.149999). By January 2015, a total of 581 data sets (over 4 000 000 data points) from 539 papers had been archived. Here we present the developments of this data compilation five years since its first description by Nisumaa et al. (2010). Most of study sites from which data archived are still in the Northern Hemisphere and the number of archived data from studies from the Southern Hemisphere and polar oceans are still relatively low. Data from 60 studies that investigated the response of a mix of organisms or natural communities were all added after 2010, indicating a welcomed shift from the study of individual organisms to communities and ecosystems. The initial imbalance of considerably more data archived on calcification and primary production than on other processes has improved. There is also a clear tendency towards more data archived from multifactorial studies after 2010. For easier and more effective access to ocean acidification data, the ocean acidification community is strongly encouraged to contribute to the data archiving effort, and help develop standard vocabularies describing the variables and define best practices for archiving ocean acidification data.

ATPase activity, proton gradients and proton secretion inhibition during experiments with Sepia officinalis and Sepioteuthis lessoniana

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 between 0.2 and 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 (NHE3) 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.

Adult acclimation to combined temperature and pH stressors significantly enhances reproductive outcomes compared to short-term exposures

This study examined the effects of long-term culture under altered conditions on the Antarctic sea urchin, Sterechinus neumayeri. Sterechinus neumayeri was cultured under the combined environmental stressors of lowered pH (-0.3 and -0.5 pH units) and increased temperature (+2 °C) for 2 years. This time-scale covered two full reproductive cycles in this species and analyses included studies on both adult metabolism and larval development. Adults took at least 6-8 months to acclimate to the altered conditions, but beyond this, there was no detectable effect of temperature or pH. Animals were spawned after 6 and 17 months exposure to altered conditions, with markedly different outcomes. At 6 months, the percentage hatching and larval survival rates were greatest in the animals kept at 0 °C under current pH conditions, whilst those under lowered pH and +2 °C performed significantly less well. After 17 months, performance was not significantly different across treatments, including controls. However, under the altered conditions urchins produced larger eggs compared with control animals. These data show that under long-term culture adult S. neumayeri appear to acclimate their metabolic and reproductive physiology to the combined stressors of altered pH and increased temperature, with relatively little measureable effect. They also emphasize the importance of long-term studies in evaluating effects of altered pH, particularly in slow developing marine species with long gonad maturation times, as the effects of altered conditions cannot be accurately evaluated unless gonads have fully matured under the new conditions.

Seawater carbonate chemistry and processes during experiments with amphipod Gammarus locusta, 2009

We report an investigation of the effects of increases in pCO2 on the survival, growth and molecular physiology of the neritic amphipod Gammarus locusta which has a cosmopolitan distribution in estuaries. Amphipods were reared from juvenile to mature adult in laboratory microcosms at three different levels of pH in nominal range 8.1-7.6. Growth rate was estimated from weekly measures of body length. At sexual maturity the amphipods were sacrificed and assayed for changes in the expression of genes coding for a heat shock protein (hsp70 gene) and the metabolic enzyme glyceraldehyde-3-phosphate dehydrogenase (gapdh gene). The data show that the growth and survival of this species is not significantly impacted by a decrease in sea water pH of up to 0.5 units. Quantitative real-time PCR analysis indicated that there was no significant effect of growth in acidified sea water on the sustained expression of the hsp70 gene. There was a consistent and significant increase in the expression of the gapdh gene at a pH of ~7.5 which, when combined with observations from other workers, suggests that metabolic changes may occur in response to acidification. It is concluded that sensitive assays of tissue physiology and molecular biology should be routinely employed in future studies of the impacts of sea water acidification as subtle effects on the physiology and metabolism of coastal marine species may be overlooked in conventional gross "end-point" studies of organism growth or mortality.

PM2.5, PM10, and PM10-associated elements in the air in Bamako, Mali (2012-2013)

Saharan dust incursions and particulates emitted from human activities degrade air quality throughout West Africa, especially in the rapidly expanding urban centers in the region. Particulate matter (PM) that can be inhaled is strongly associated with increased incidence of and mortality from cardiovascular and respiratory diseases and cancer. Air samples collected in the capital of a Saharan-Sahelian country (Bamako, Mali) between September 2012 - July 2013 were found to contain inhalable PM concentrations that exceeded World Health Organization (WHO) and US Environmental Protection Agency (USEPA) PM2.5 and PM10 24-h limits 58 - 98% of days and European Union (EU) PM10 24-h limit 98% of days. Mean concentrations were 1.2-to-4.5 fold greater than existing limits. Inhalable PM was enriched in transition metals, known to produce reactive oxygen species and initiate the inflammatory reaction, and other potentially bioactive and biotoxic metals/metalloids. Eroded mineral dust composed the bulk of inhalable PM, whereas most enriched metals/metalloids were likely emitted from oil combustion, biomass burning, refuse incineration, vehicle traffic, and mining activities. Human exposure to inhalable PM and associated metals/metalloids over 24-h was estimated. The findings indicate that inhalable PM in the Sahara-Sahel region may present a threat to human health, especially in urban areas with greater inhalable PM and transition metal exposure.

Copepod vital rates under CO2-induced acidification: a calanoid species and a cyclopoid species under short-term exposures

Although copepods have been considered tolerant against the direct influence of the ocean acidification (OA) projected for the end of the century, some recent studies have challenged this view. Here, we have examined the direct impact of short-term exposure to a pCO2/pH level relevant for the year 2100 (pHNBS, control: 8.18, low pH: 7.78), on the physiological performance of two representative marine copepods: the calanoid Acartia grani and the cyclopoid Oithona davisae. Adults of both species, from laboratory cultures, were preconditioned for four consecutive days in algal suspensions (Akashiwo sanguinea) prepared with filtered sea water pre-adjusted to the targeted pH values via CO2 bubbling. We measured the feeding and respiratory activity and reproductive output of those pre-conditioned females. The largely unaffected fatty acid composition of the prey offered between OA treatments and controls supports the absence in the study of indirect OA effects (i.e. changes of food nutritional quality). Our results show no direct effect of acidification on the vital rates examined in either copepod species. Our findings are compared with results from previous short- and long-term manipulative experiments on other copepod species.

Influence of temperature and CO2 on the strontium and magnesium composition of coccolithophore calcite

Marine calcareous sediments provide a fundamental basis for palaeoceanographic studies aiming to reconstruct past oceanic conditions and understand key biogeochemical element cycles. Calcifying unicellular phytoplankton (coccolithophores) are a major contributor to both carbon and calcium cycling by photosynthesis and the production of calcite (coccoliths) in the euphotic zone, and the subsequent long-term deposition and burial into marine sediments. Here we present data from controlled laboratory experiments on four coccolithophore species and elucidate the relation between the divalent cation (Sr, Mg and Ca) partitioning in coccoliths and cellular physiology (growth, calcification and photosynthesis). Coccolithophores were cultured under different seawater temperature and carbonate chemistry conditions. The partition coefficient of strontium (DSr) was positively correlated with both carbon dioxide (pCO2) and temperature but displayed no coherent relation to particulate organic and inorganic carbon production rates. Furthermore, DSr correlated positively with cellular growth rates when driven by temperature but no correlation was present when changes in growth rates were pCO2-induced. Our results demonstrate the complex interaction between environmental forcing and physiological control on the strontium partitioning in coccolithophore calcite and challenge interpretations of the coccolith Sr / Ca ratio from high-pCO2 environments (e.g. Palaeocene-Eocene thermal maximum). The partition coefficient of magnesium (DMg) displayed species-specific differences and elevated values under nutrient limitation. No conclusive correlation between coccolith DMg and temperature was observed but pCO2 induced a rising trend in coccolith DMg. Interestingly, the best correlation was found between coccolith DMg and chlorophyll a production, suggesting that chlorophyll a and calcite associated Mg originate from the same intracellular pool. These and previous findings indicate that Mg is transported into the cell and to the site of calcification via different pathways than Ca and Sr. Consequently, the coccolith Mg / Ca ratio should be decoupled from the seawater Mg / Ca ratio. This study gives an extended insight into the driving factors influencing the coccolith Mg / Ca ratio and should be considered for future palaeoproxy calibrations.

Ocean Acidification Affects Redox-Balance and Ion-Homeostasis in the Life-Cycle Stages of Emiliania huxleyi

Ocean Acidification (OA) has been shown to affect photosynthesis and calcification in the coccolithophore Emiliania huxleyi, a cosmopolitan calcifier that significantly contributes to the regulation of the biological carbon pumps. Its non-calcifying, haploid life-cycle stage was found to be relatively unaffected by OA with respect to biomass production. Deeper insights into physiological key processes and their dependence on environmental factors are lacking, but are required to understand and possibly estimate the dynamics of carbon cycling in present and future oceans. Therefore, calcifying diploid and non-calcifying haploid cells were acclimated to present and future CO2 partial pressures (pCO2; 38.5 Pa vs. 101.3 Pa CO2) under low and high light (50 vs. 300 µmol photons/m**2 /s). Comparative microarray-based transcriptome profiling was used to screen for the underlying cellular processes and allowed to follow up interpretations derived from physiological data. In the diplont, the observed increases in biomass production under OA are likely caused by stimulated production of glycoconjugates and lipids. The observed lowered calcification under OA can be attributed to impaired signal-transduction and ion-transport. The haplont utilizes distinct genes and metabolic pathways, reflecting the stage-specific usage of certain portions of the genome. With respect to functionality and energy-dependence, however, the transcriptomic OA-responses resemble those of the diplont. In both life-cycle stages, OA affects the cellular redox-state as a master regulator and thereby causes a metabolic shift from oxidative towards reductive pathways, which involves a reconstellation of carbon flux networks within and across compartments. Whereas signal transduction and ion-homeostasis appear equally OA-sensitive under both light intensities, the effects on carbon metabolism and light physiology are clearly modulated by light availability. These interactive effects can be attributed to the influence of OA and light on the redox equilibria of NAD and NADP, which function as major sensors for energization and stress. This generic mode of action of OA may therefore provoke similar cell-physiological responses in other protists.

Seawater carbonate chemistry and energy status in the periwinkle Littorina littorea during experiments, 2011

In the future, marine organisms will face the challenge of coping with multiple environmental changes associated with increased levels of atmospheric Pco2, such as ocean warming and acidification. To predict how organisms may or may not meet these challenges, an in-depth understanding of the physiological and biochemical mechanisms underpinning organismal responses to climate change is needed. Here, we investigate the effects of elevated Pco2 and temperature on the whole-organism and cellular physiology of the periwinkle Littorina littorea. Metabolic rates (measured as respiration rates), adenylate energy nucleotide concentrations and indexes, and end-product metabolite concentrations were measured. Compared with values for control conditions, snails decreased their respiration rate by 31% in response to elevated Pco2 and by 15% in response to a combination of increased Pco2 and temperature. Decreased respiration rates were associated with metabolic reduction and an increase in end-product metabolites in acidified treatments, indicating an increased reliance on anaerobic metabolism. There was also an interactive effect of elevated Pco2 and temperature on total adenylate nucleotides, which was apparently compensated for by the maintenance of adenylate energy charge via AMP deaminase activity. Our findings suggest that marine intertidal organisms are likely to exhibit complex physiological responses to future environmental drivers, with likely negative effects on growth, population dynamics, and, ultimately, ecosystem processes.