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 By January 2015, a total of 581 data sets (over 4 000 000 data points) from 539 papers had been archived.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.

Early Oligocene continental climate ofthe Paleogene Basin in Hungary and Slovenia

This paper concentrates on the Early Oligocene palaeoclimate of the southern part of Eastern and Central Europe and gives a detailed climatological analysis, combined with leaf-morphological studies and modelling of the palaeoatmospheric CO2 level using stomatal and d13 C data. Climate data are calculated using the Coexistence Approach for Kiscellian floras of the Palaeogene Basin (Hungary and Slovenia) and coeval assemblages from Central and Southeastern Europe. Potential microclimatic or habitat variations are considered using morphometric analysis of fossil leaves from Hungarian, Slovenian and Italian floras. Reconstruction of CO2 is performed by applying a recently introduced mechanistic model. Results of climate analysis indicate distinct latitudinal and longitudinal climate patterns for various variables which agree well with reconstructed palaeogeography and vegetation. Calculated climate variables in general suggest a warm and frost-free climate with low seasonal variation of temperature. A difference in temperature parameters is recorded between localities from Central and Southeastern Europe, manifested mainly in the mean temperature of the coldest month. Results of morphometric analysis suggest microclimatic or habitat difference among studied floras. Extending the scarce information available on atmospheric CO2 levels during the Oligocene, we provide data for a well-defined time-interval. Reconstructed atmospheric CO2 levels agree well with threshold values for Antarctic ice sheet growth suggested by recent modelling studies. The successful application of the mechanistic model for the reconstruction of atmospheric CO2 levels raises new possibitities for future climate inference from macro-flora studies.

(Table 1) Variation in chemical composition of Black Sea ctenophores depending on size

Data of chemical analysis of Black Sea ctenophore Mnemiopsis leidyi indicates that their body contains on average 5.28% carbon, 3.48% nitrogen, 0.11% phosphorus, and 0.03% silicon on dry weight. Mean ratios of the main biogenic elements in ctenophores is C:N=1.4, N:P=10.9, and C:P=32.2. Comparing concentration of the main biogenic elements in the surface layer with their concentrations in ctenophores it is concluded that mass development of M. leidyi has negative effect on the hydrochemical structure of the Black Sea.

Berry production, shoot growth and biomass of E. hermaphroditum, V. vitis-idaea and V. myrtillis at Abisco ANS

Extreme weather events can have strong negative impacts on species survival and community structure when surpassing lethal thresholds. Extreme, short-lived, winter warming events in the Arctic rapidly melt snow and expose ecosystems to unseasonably warm air (for instance, 2-10 °C for 2-14 days) but upon return to normal winter climate exposes the ecosystem to much colder temperatures due to the loss of insulating snow. Single events have been shown to reduce plant reproduction and increase shoot mortality, but impacts of multiple events are little understood as are the broader impacts on community structure, growth, carbon balance, and nutrient cycling. To address these issues, we simulated week-long extreme winter warming events - using infrared heating lamps and soil warming cables - for 3 consecutive years in a sub-Arctic heathland dominated by the dwarf shrubs Empetrum hermaphroditum, Vaccinium vitis-idaea (both evergreen) and Vaccinium myrtillus (deciduous). During the growing seasons after the second and third winter event, spring bud burst was delayed by up to a week for E. hermaphroditum and V. myrtillus, and berry production reduced by 11-75% and 52-95% for E. hermaphroditum and V. myrtillus, respectively. Greater shoot mortality occurred in E. hermaphroditum (up to 52%), V. vitis-idaea (51%), and V. myrtillus (80%). Root growth was reduced by more than 25% but soil nutrient availability remained unaffected. Gross primary productivity was reduced by more than 50% in the summer following the third simulation. Overall, the extent of damage was considerable, and critically plant responses were opposite in direction to the increased growth seen in long-term summer warming simulations and the 'greening' seen for some arctic regions. Given the Arctic is warming more in winter than summer, and extreme events are predicted to become more frequent, this generates large uncertainty in our current understanding of arctic ecosystem responses to climate change.

Seawater carbonate chemistry, nutrients and growth rate during experiments with coral Astrangia poculata and field observations, 2010

Zooxanthellate colonies of the scleractinian coral Astrangia poculata were grown under combinations of ambient and elevated nutrients (5 µM NO, 0.3 µM PO4, and 2nM Fe) and CO2 (780 ppmv) treatments for a period of 6 months. Coral calcification rates, estimated from buoyant weights, were not significantly affected by moderately elevated nutrients at ambient CO2 and were negatively affected by elevated CO2 at ambient nutrient levels. However, calcification by corals reared under elevated nutrients combined with elevated CO2 was not significantly different from that of corals reared under ambient conditions, suggesting that CO2 enrichment can lead to nutrient limitation in zooxanthellate corals. A conceptual model is proposed to explain how nutrients and CO2 interact to control zooxanthellate coral calcification. Nutrient limited corals are unable to utilize an increase in dissolved inorganic carbon (DIC) as nutrients are already limiting growth, thus the effect of elevated CO2 on saturation state drives the calcification response. Under nutrient replete conditions, corals may have the ability to utilize more DIC, thus the calcification response to CO2 becomes the product of a negative effect on saturation state and a positive effect on gross carbon fixation, depending upon which dominates, the calcification response can be either positive or negative. This may help explain how the range of coral responses found in different studies of ocean acidification can be obtained.

Combined effects of CO2 and light on large and small isolates of the unicellular N2-fixing cyanobacterium Crocosphaera watsonii from the western tropical Atlantic Ocean

We examined the combined effects of light and pCO2 on growth, CO2-fixation and N2-fixation rates by strains of the unicellular marine N2-fixing cyanobacterium Crocosphaera watsonii with small (WH0401) and large (WH0402) cells that were isolated from the western tropical Atlantic Ocean. In low-pCO2-acclimated cultures (190 ppm) of WH0401, growth, CO2-fixation and N2-fixation rates were significantly lower than those in cultures acclimated to higher (present-day 385 ppm, or future 750 ppm) pCO2 treatments. Growth rates were not significantly different, however, in low-pCO2-acclimated cultures of WH0402 in comparison with higher pCO2 treatments. Unlike previous reports for C. watsonii (strain WH8501), N2-fixation rates did not increase further in cultures of WH0401 or WH0402 when acclimated to 750 ppm relative to those maintained at present-day pCO2. Both light and pCO2 had a significant negative effect on gross : net N2-fixation rates in WH0402 and trends were similar in WH0401, implying that retention of fixed N was enhanced under elevated light and pCO2. These data, along with previously reported results, suggest that C. watsonii may have wide-ranging, strain-specific responses to changing light and pCO2, emphasizing the need for examining the effects of global change on a range of isolates within this biogeochemically important genus. In general, however, our data suggest that cellular N retention and CO2-fixation rates of C. watsonii may be positively affected by elevated light and pCO2 within the next 100 years, potentially increasing trophic transfer efficiency of C and N and thereby facilitating uptake of atmospheric carbon by the marine biota.

Effects of Ocean Acidification and Warming on Sperm Activity and Early Life Stages of the Mediterranean Mussel (Mytilus galloprovincialis)

Larval stages are among those most vulnerable to ocean acidification (OA). Projected atmospheric CO2 levels for the end of this century may lead to negative impacts on communities dominated by calcifying taxa with planktonic life stages. We exposed Mediterranean mussel (Mytilus galloprovincialis) sperm and early life stages to pHT levels of 8.0 (current pH) and 7.6 (2100 level) by manipulating pCO2 level (380 and 1000 ppm). Sperm activity was examined at ambient temperatures (16-17 °C) using individual males as replicates. We also assessed the effects of temperature (ambient and = 20 °C) and pH on larval size, survival, respiration and calcification of late trochophore/early D-veliger stages using a cross-factorial design. Increased pCO2 had a negative effect on the percentage of motile sperm (mean response ratio R= 71%) and sperm swimming speed (R= 74%), possibly indicating reduced fertilization capacity of sperm in low concentrations. Increased temperature had a more prominent effect on larval stages than pCO2, reducing performance (RSize = 90% and RSurvival = 70%) and increasing energy demand (RRespiration = 429%). We observed no significant interactions between pCO2 and temperature. Our results suggest that increasing temperature might have a larger impact on very early larval stages of M. galloprovincialis than OA at levels predicted for the end of the century.

Seawater carbonate chemistry and larval development and settlement of the sea urchin Arbacia lixula in a laboratory experiment

We studied the effects of temperature and pH on larval development, settlement and juvenile survival of a Mediterranean population of the sea urchin Arbacia lixula. Three temperatures (16, 17.5 and 19 °C) were tested at present pH conditions (pHT 8.1). At 19 °C, two pH levels were compared to reflect present average (pHT 8.1) and near-future average conditions (pHT 7.7, expected by 2100). Larvae were reared for 52-days to achieve the full larval development and complete the metamorphosis to the settler stage. We analyzed larval survival, growth, morphology and settlement success. We also tested the carry-over effect of acidification on juvenile survival after 3 days. Our results showed that larval survival and size significantly increased with temperature. Acidification resulted in higher survival rates and developmental delay. Larval morphology was significantly altered by low temperatures, which led to narrower larvae with relatively shorter skeletal rods, but larval morphology was only marginally affected by acidification. No carry-over effects between larvae and juveniles were detected in early settler survival, though settlers from larvae reared at pH 7.7 were significantly smaller than their counterparts developed at pH 8.1. These results suggest an overall positive effect of environmental parameters related to global change on the reproduction of A. lixula, and reinforce the concerns about the increasing negative impact on shallow Mediterranean ecosystems of this post-glacial colonizer.

Seawater carbonate chemistry, fertilization and early development of the coral eating crown-of-thorns starfish, Acanthaster planci in a laboratory experiment

Outbreaks of crown-of-thorns starfish (COTS), Acanthaster planci, contribute to major declines of coral reef ecosystems throughout the Indo-Pacific. As the oceans warm and decrease in pH due to increased anthropogenic CO2 production, coral reefs are also susceptible to bleaching, disease and reduced calcification. The impacts of ocean acidification and warming may be exacerbated by COTS predation, but it is not known how this major predator will fare in a changing ocean. Because larval success is a key driver of population outbreaks, we investigated the sensitivities of larval A. planci to increased temperature (2-4 °C above ambient) and acidification (0.3-0.5 pH units below ambient) in flow-through cross-factorial experiments (3 temperature × 3 pH/pCO2 levels). There was no effect of increased temperature or acidification on fertilization or very early development. Larvae reared in the optimal temperature (28 °C) were the largest across all pH treatments. Development to advanced larva was negatively affected by the high temperature treatment (30 °C) and by both experimental pH levels (pH 7.6, 7.8). Thus, planktonic life stages of A. planci may be negatively impacted by near-future global change. Increased temperature and reduced pH had an additive negative effect on reducing larval size. The 30 °C treatment exceeded larval tolerance regardless of pH. As 30 °C sea surface temperatures may become the norm in low latitude tropical regions, poleward migration of A. planci may be expected as they follow optimal isotherms. In the absence of acclimation or adaptation, declines in low latitude populations may occur. Poleward migration will be facilitated by strong western boundary currents, with possible negative flow-on effects on high latitude coral reefs. The contrasting responses of the larvae of A. planci and those of its coral prey to ocean acidification and warming are considered in context with potential future change in tropical reef ecosystems.

Effects of seawater pCO2 and temperature on shell growth, shell stability, condition and cellular stress of Western Baltic Sea Mytilus edulis (L.) and Arctica islandica (L.)

Acidification of the World's oceans may directly impact reproduction, performance and shell formation of marine calcifying organisms. In addition, since shell production is costly and stress in general draws on an organism's energy budget, shell growth and stability of bivalves should indirectly be affected by environmental stress. The aim of this study was to investigate whether a combination of warming and acidification leads to increased physiological stress (lipofuscin accumulation and mortality) and affects the performance [shell growth, shell breaking force, condition index (Ci)] of young Mytilus edulis and Arctica islandica from the Baltic Sea. We cultured the bivalves in a fully-crossed 2-factorial experimental setup (seawater (sw) pCO2 levels "low", "medium" and "high" for both species, temperature levels 7.5, 10, 16, 20 and 25 °C for M. edulis and 7.5, 10 and 16 °C for A. islandica) for 13 weeks in summer. Mytilus edulis and A. islandica appeared to tolerate wide ranges of sw temperature and pCO2. Lipofuscin accumulation of M. edulis increased with temperature while the Ci decreased, but shell growth of the mussels only sharply decreased while its mortality increased between 20 and 25 °C. In A. islandica, lipofuscin accumulation increased with temperature, whereas the Ci, shell growth and shell breaking force decreased. The pCO2 treatment had only marginal effects on the measured parameters of both bivalve species. Shell growth of both bivalve species was not impaired by under-saturation of the sea water with respect to aragonite and calcite. Furthermore, independently of water temperatures shell breaking force of both species and shell growth of A. islandica remained unaffected by the applied elevated sw pCO2 for several months. Only at the highest temperature (25 °C), growth arrest of M. edulis was recorded at the high sw pCO2 treatment and the Ci of M. edulis was slightly higher at the medium sw pCO2 treatment than at the low and high sw pCO2 treatments. The only effect of elevated sw pCO2 on A. islandica was an increase in lipofuscin accumulation at the high sw pCO2 treatment compared to the medium sw pCO2 treatment. Our results show that, despite this robustness, growth of both M. edulis and A. islandica can be reduced if sw temperatures remain high for several weeks in summer. As large body size constitutes an escape from crab and sea star predation, this can make bivalves presumably more vulnerable to predation with possible negative consequences on population growth. In M. edulis, but not in A. islandica, this effect is amplified by elevated sw pCO2. We follow that combined effects of elevated sw pCO2 and ocean warming might cause shifts in future Western Baltic Sea community structures and ecosystem services; however, only if predators or other interacting species do not suffer as strong from these stressors.

Habitat traits and food availability determine the response of marine invertebrates to ocean acidification

Energy availability and local adaptation are major components in mediating the effects of ocean acidification (OA) on marine species. In a long-term study, we investigated the effects of food availability and elevated pCO2 (ca 400, 1000 and 3000 µatm) on growth of newly settled Amphibalanus (Balanus) improvisus to reproduction, and on their offspring. We also compared two different populations, which were presumed to differ in their sensitivity to pCO2 due to differing habitat conditions: Kiel Fjord, Germany (Western Baltic Sea) with naturally strong pCO2 fluctuations, and the Tjärnö Archipelago, Sweden (Skagerrak) with far lower fluctuations. Over 20 weeks, survival, growth, reproduction and shell strength of Kiel barnacles were all unaffected by elevated pCO2, regardless of food availability. Moulting frequency and shell corrosion increased with increasing pCO2 in adults. Larval development and juvenile growth of the F1 generation were tolerant to increased pCO2, irrespective of parental treatment. In contrast, elevated pCO2 had a strong negative impact on survival of Tjärnö barnacles. Specimens from this population were able to withstand moderate levels of elevated pCO2 over 5 weeks when food was plentiful but showed reduced growth under food limitation. Severe levels of elevated pCO2 negatively impacted growth of Tjärnö barnacles in both food treatments. We demonstrate a conspicuously higher tolerance to elevated pCO2 in Kiel barnacles than in Tjärnö barnacles. This tolerance was carried-over from adults to their offspring. Our findings indicate that populations from fluctuating pCO2 environments are more tolerant to elevated pCO2 than populations from more stable pCO2 habitats. We furthermore provide evidence that energy availability can mediate the ability of barnacles to withstand moderate CO2 stress. Considering the high tolerance of Kiel specimens and the possibility to adapt over many generations, near future OA alone does not seem to present a major threat for A. improvisus

Temperature is the evil twin: Effects of increased temperature and ocean acidification on reproduction in a reef fish

Reproduction in many organisms can be disrupted by changes to the physical environment, such as those predicted to occur during climate change. Marine organisms face the dual climate change threats of increasing temperature and ocean acidification, yet no studies have examined the potential interactive effects of these stressors on reproduction in marine fishes. We used a long-term experiment to test the interactive effects of increased temperature and CO2 on the reproductive performance of the anemonefish, Amphiprion melanopus. Adult breeding pairs were kept for 10 months at three temperatures, 28.5°C (+0.0°C), 30.0°C (+1.5°C) and 31.5°C (+3.0°C), cross-factored with 3 CO2 levels, a current day control (417 µatm) and moderate (644 µatm) and high (1134 µatm) treatments consistent with the range of CO2 projections for the year 2100 under RCP8.5. We recorded each egg clutch produced during the breeding season, the number of eggs laid per clutch, average egg size, fertilization success, survival to hatching, hatchling length and yolk provisioning. Adult body condition, hepatosomatic index, gonadosomatic index, and plasma 17beta-estradiol concentrations were measured at the end of the breeding season to determine the effect of prolonged exposure to increased temperature and elevated CO2 on adults, and to examine potential physiological mechanisms for changes in reproduction. Temperature had by far the stronger influence on reproduction, with clear declines in reproduction occurring in the +1.5°C treatment and ceasing altogether in the +3.0°C treatment. In contrast, CO2 had a minimal effect on the majority of reproductive traits measured, but caused a decline in offspring quality in combination with elevated temperature. We detected no significant effect of temperature or CO2 on adult body condition or hepatosomatic index. Elevated temperature had a significant negative effect on plasma 17beta-estradiol concentrations, suggesting that declines in reproduction with increasing temperature were due to the thermal sensitivity of reproductive hormones rather than a reduction in energy available for reproduction. Our results show that elevated temperature exerts a stronger influence than high CO2 on reproduction in A. melanopus. Understanding how these two environmental variables interact to affect the reproductive performance of marine organisms will be important for predicting the future impacts of climate change.

Response of A. aurita ephyrae to three stressors: high-temperature, high-CO2 and low-oxygen

Global change is affecting marine ecosystems through a combination of different stressors such as warming, ocean acidification and oxygen depletion. Very little is known about the interactions among these factors, especially with respect to gelatinous zooplankton. Therefore, in this study we investigated the direct effects of pH, temperature and oxygen availability on the moon jellyfish Aurelia aurita, concentrating on the ephyral life stage. Starved one-day-old ephyrae were exposed to a range of pCO2 (400-4000 ppm) and three different dissolved oxygen levels (from saturated to hypoxic conditions), in two different temperatures (5 and 15 °C) for 7 days. Carbon content and swimming activity were analysed at the end of the incubation period, and mortality noted. General linearized models were fitted through the data, with the best fitting models including two- and three-way interactions between pCO2, temperature and oxygen concentration. The combined effect of the stressors was small but significant, with the clearest negative effect on growth caused by the combination of all three stressors present (high temperature, high CO2, low oxygen). We conclude that A. aurita ephyrae are robust and that they are not likely to suffer from these environmental stressors in a near future.

A stereo-image analysis JAVA software with links to executable and source code

Scientists planning to use underwater stereoscopic image technologies are often faced with numerous problems during the methodological implementations: commercial equipment is too expensive; the setup or calibration is too complex; or the imaging processing (i.e. measuring objects in the stereo-images) is too complicated to be performed without a time-consuming phase of training and evaluation. The present paper addresses some of these problems and describes a workflow for stereoscopic measurements for marine biologists. It also provides instructions on how to assemble an underwater stereo-photographic system with two digital consumer cameras and gives step-by-step guidelines for setting up the hardware. The second part details a software procedure to correct stereo-image pairs for lens distortions, which is especially important when using cameras with non-calibrated optical units. The final part presents a guide to the process of measuring the lengths (or distances) of objects in stereoscopic image pairs. To reveal the applicability and the restrictions of the described systems and to test the effects of different types of camera (a compact camera and an SLR type), experiments were performed to determine the precision and accuracy of two generic stereo-imaging units: a diver-operated system based on two Olympus Mju 1030SW compact cameras and a cable-connected observatory system based on two Canon 1100D SLR cameras. In the simplest setup without any correction for lens distortion, the low-budget Olympus Mju 1030SW system achieved mean accuracy errors (percentage deviation of a measurement from the object's real size) between 10.2 and -7.6% (overall mean value: -0.6%), depending on the size, orientation and distance of the measured object from the camera. With the single lens reflex (SLR) system, very similar values between 10.1% and -3.4% (overall mean value: -1.2%) were observed. Correction of the lens distortion significantly improved the mean accuracy errors of either system. Even more, system precision (spread of the accuracy) improved significantly in both systems. Neither the use of a wide-angle converter nor multiple reassembly of the system had a significant negative effect on the results. The study shows that underwater stereophotography, independent of the system, has a high potential for robust and non-destructive in situ sampling and can be used without prior specialist training.

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.