Combined effects of low pH and low oxygen on the early-life stages of the barnacle Balanus amphitrite

Ocean acidification (OA) is anticipated to interact with the more frequently occurring hypoxic conditions in shallow coastal environments. These could exert extreme stress on the barnacle-dominated fouling communities. However, the interactive effect of these two emerging stressors on early-life stages of fouling organisms remains poorly studied. We investigated both the independent and interactive effect of low pH (7.6 vs. ambient 8.2) and low oxygen (LO; 3 mg/l vs. ambient 5 mg/l) from larval development through settlement (attachment and metamorphosis) and juvenile growth of the widespread fouling barnacle, Balanus amphitrite. In particular, we focused on the critical transition between planktonic and benthic phases to examine potential limiting factors (i.e. larval energy storage and the ability to perceive cues) that may restrain barnacle recruitment under the interactive stressors. LO significantly slowed naupliar development, while the interaction with low pH (LO-LP) seemed to alleviate the negative effect. However, 20-50% of the larvae became cyprid within 4 d post-hatching, regardless of treatment. Under the two stressors interaction (LO-LP), the barnacle larvae increased their feeding rate, which may explain why their energy reserves at competency were not different from any other treatment. In the absence of a settlement-inducing cue, a significantly lower percentage of cyprids (15% lower) settled in LO and LO-LP. The presence of an inducing cue, however, elevated attachment up to 50-70% equally across all treatments. Post-metamorphic growth was not altered, although the condition index was different between LO and LO-LP treatments, potentially indicating that less and/or weaker calcified structures were developed when the two stressors were experienced simultaneously. LO was the major driver for the responses observed and its interaction with low pH should be considered in future studies to avoid underestimating the sensitivity of biofouling species to OA and associated climate change stressors.

Combined effects of short-term ocean acidification and heat shock in a benthic copepod Tigriopus japonicus Mori

Warming of the world's oceans is predicted to have many negative effects on organisms as they have optimal thermal windows. In coastal waters, however, both temperatures and pCO2 (pH) exhibit diel variations, and biological performances are likely to be modulated by physical and chemical environmental changes. To understand how coastal zooplankton respond to the combined impacts of heat shock and increased pCO2, the benthic copepod Tigriopus japonicus were treated at temperatures of 24, 28, 32 and 36 °C to simulate natural coastal temperatures experienced in warming events, when acclimated in the short term to either ambient (LC, 390 µatm) or future CO2 (HC, 1000 µatm). HC and heat shock did not induce any mortality of T. japonicus, though respiration increased up to 32 °C before being depressed at 36 °C. Feeding rate peaked at 28 °C but did not differ between CO2 treatments. Expression of heat shock proteins (hsps mRNA) was positively related to temperature, with no significant differences between the CO2 concentrations. Nauplii production was not affected across all treatments. Our results demonstrate that T. japonicus responds more sensitively to heat shocks rather than to seawater acidification; however, ocean acidification may synergistically act with ocean warming to mediate the energy allocation of copepods.

Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions

Coral reefs are globally threatened by climate change-related ocean warming and ocean acidification (OA). To date, slow-response mechanisms such as genetic adaptation have been considered the major determinant of coral reef persistence, with little consideration of rapid-response acclimatization mechanisms. These rapid mechanisms such as parental effects that can contribute to trans-generational acclimatization (e.g. epigenetics) have, however, been identified as important contributors to offspring response in other systems. We present the first evidence of parental effects in a cross-generational exposure to temperature and OA in reef-building corals. Here, we exposed adults to high (28.9°C, 805 µatm PCO2) or ambient (26.5°C, 417 µatm PCO2) temperature and OA treatments during the larval brooding period. Exposure to high treatment negatively affected adult performance, but their larvae exhibited size differences and metabolic acclimation when subsequently re-exposed, unlike larvae from parents exposed to ambient conditions. Understanding the innate capacity corals possess to respond to current and future climatic conditions is essential to reef protection and maintenance. Our results identify that parental effects may have an important role through (1) ameliorating the effects of stress through preconditioning and adaptive plasticity, and/or (2) amplifying the negative parental response through latent effects on future life stages. Whether the consequences of parental effects and the potential for trans-generational acclimatization are beneficial or maladaptive, our work identifies a critical need to expand currently proposed climate change outcomes for corals to further assess rapid response mechanisms that include non-genetic inheritance through parental contributions and classical epigenetic mechanisms.

Combined impacts of elevated CO2 and anthropogenic noise on European sea bass (Dicentrarchus labrax)

Ocean acidification (OA) and anthropogenic noise are both known to cause stress and induce physiological and behavioural changes in fish, with consequences for fitness. OA is also predicted to reduce the ocean's capacity to absorb low-frequency sounds produced by human activity. Consequently, anthropogenic noise could propagate further under an increasingly acidic ocean. For the first time, this study investigated the independent and combined impacts of elevated carbon dioxide (CO2) and anthropogenic noise on the behaviour of a marine fish, the European sea bass (Dicentrarchus labrax). In a fully factorial experiment crossing two CO2 levels (current day and elevated) with two noise conditions (ambient and pile driving), D. labrax were exposed to four CO2/noise treatment combinations: 400 µatm/ambient, 1000 µatm/ambient, 400 µatm/pile-driving, and 1000 µatm/pile driving. Pile-driving noise increased ventilation rate (indicating stress) compared with ambient noise conditions. Elevated CO2 did not alter the ventilation rate response to noise. Furthermore, there was no interaction effect between elevated CO2 and pile-driving noise, suggesting that OA is unlikely to influence startle or ventilatory responses of fish to anthropogenic noise. However, effective management of anthropogenic noise could reduce fish stress, which may improve resilience to future stressors.

Alleviation of solar ultraviolet radiation (UVR)-induced photoinhibition in diatom Chaetoceros curvisetus by ocean acidification

The study aimed to unravel the interaction between ocean acidification and solar ultraviolet radiation (UVR) in Chaetoceros curvisetus. Chaetoceros curvisetus cells were acclimated to high CO2 (HC, 1000 ppmv) and low CO2 concentration (control, LC, 380 ppmv) for 14 days. Cell density, specific growth rate and chlorophyll were measured. The acclimated cells were then exposed to PAB (photosynthetically active radiation (PAR) + UV-A + UV-B), PA (PAR + UV-A) or P (PAR) for 60 min. Photochemical efficiency (phi PSII), relative electron transport rate (rETR) and the recovery of ?PSII were determined. HC induced higher cell density and specific growth rate compared with LC. However, no difference was found in chlorophyll between HC and LC. Moreover, phi PSII and rETRs were higher under HC than LC in response to solar UVR. P exposure led to faster recovery of phi PSII, both under HC and LC, than PA and PAB exposure. It appeared that harmful effects of UVR on C. curvisetus could be counteracted by ocean acidification simulated by high CO2 when the effect of climate change is not beyond the tolerance of cells.

Ocean acidification impacts mussel control on biomineralisation

Ocean acidification is altering the oceanic carbonate saturation state and threatening the survival of marine calcifying organisms. Production of their calcium carbonate exoskeletons is dependent not only on the environmental seawater carbonate chemistry but also the ability to produce biominerals through proteins. We present shell growth and structural responses by the economically important marine calcifier Mytilus edulis to ocean acidification scenarios (380, 550, 750, 1000 µatm pCO2). After six months of incubation at 750 µatm pCO2, reduced carbonic anhydrase protein activity and shell growth occurs in M. edulis. Beyond that, at 1000 µatm pCO2, biomineralisation continued but with compensated metabolism of proteins and increased calcite growth. Mussel growth occurs at a cost to the structural integrity of the shell due to structural disorientation of calcite crystals. This loss of structural integrity could impact mussel shell strength and reduce protection from predators and changing environments.

Impact of long-term moderate hypercapnia and elevated temperature on the energy budget of isolated gills and branchial in vivo and in vitro enzyme capacities of Atlantic cod (Gadus morhua)

Effects of severe hypercapnia have been extensively studied in marine fishes, while knowledge on the impacts of moderately elevated CO2 levels and their combination with warming is scarce. Here we investigate ion regulation mechanisms and energy budget in gills from Atlantic cod acclimated long-term to elevated PCO2 levels (2500 µatm) and temperature (18 °C). Isolated perfused gill preparations established to determine gill thermal plasticity during acute exposures (10-22 °C) and in vivo costs of Na+/K+-ATPase activity, protein and RNA synthesis. Maximum enzyme capacities of F1Fo-ATPase, H+-ATPase and Na+/K+-ATPase were measured in vitro in crude gill homogenates. After whole animal acclimation to elevated PCO2 and/or warming, branchial oxygen consumption responded more strongly to acute temperature change. The fractions of gill respiration allocated to protein and RNA synthesis remained unchanged. In gills of fish CO2-exposed at both temperatures, energy turnover associated with Na+/K+-ATPase activity was reduced by 30% below rates of control fish. This contrasted in vitro capacities of Na+/K+-ATPase, which remained unchanged under elevated CO2 at 10 °C, and earlier studies which had found a strong upregulation under severe hypercapnia. F1Fo-ATPase capacities increased in hypercapnic gills at both temperatures, whereas Na+/K+ATPase and H+-ATPase capacities only increased in response to elevated CO2 and warming indicating the absence of thermal compensation under CO2. We conclude that in vivo ion regulatory energy demand is lowered under moderately elevated CO2 levels despite the stronger thermal response of total gill respiration and the upregulation of F1Fo-ATPase. This effect is maintained at elevated temperature.

Interactive effects of ocean acidification and rising sea temperatures alter predation rate and predator selectivity in reef fish communities

Ocean warming and acidification are serious threats to marine life. While each stressor alone has been studied in detail, their combined effects on the outcome of ecological interactions are poorly understood. We measured predation rates and predator selectivity of two closely related species of damselfish exposed to a predatory dottyback. We found temperature and CO2 interacted synergistically on overall predation rate, but antagonistically on predator selectivity. Notably, elevated CO2 or temperature alone reversed predator selectivity, but the interaction between the two stressors cancelled selectivity. Routine metabolic rates of the two prey showed strong species differences in tolerance to CO2 and not temperature, but these differences did not correlate with recorded mortality. This highlights the difficulty of linking species-level physiological tolerance to resulting ecological outcomes. This study is the first to document both synergistic and antagonistic effects of elevated CO2 and temperature on a crucial ecological process like predator-prey dynamics.

Effects of elevated CO2 on early life history development of the yellowtail kingfish, Seriola lalandi, a large pelagic fish

An increasing number of studies have examined the effects of elevated carbon dioxide (CO2) and ocean acidification on marine fish, yet little is known about the effects on large pelagic fish. We tested the effects of elevated CO2 on the early life history development and behaviour of yellowtail kingfish, Seriola lalandi. Eggs and larvae were reared in current day control (450 µatm) and two elevated CO2 treatments for a total of 6 d, from 12 h post-fertilization until 3 d post-hatching (dph). Elevated CO2 treatments matched projections for the open ocean by the year 2100 under RCP 8.5 (880 µatm CO2) and a higher level (1700 µatm CO2) relevant to upwelling zones where pelagic fish often spawn. There was no effect of elevated CO2 on survival to hatching or 3 dph. Oil globule diameter decreased with an increasing CO2 level, indicating potential effects of elevated CO2 on energy utilization of newly hatched larvae, but other morphometric traits did not differ among treatments. Contrary to expectations, there were no effects of elevated CO2 on larval behaviour. Activity level, startle response, and phototaxis did not differ among treatments. Our results contrast with findings for reef fish, where a wide range of sensory and behavioural effects have been reported. We hypothesize that the absence of behavioural effects in 3 dph yellowtail kingfish is due to the early developmental state of newly hatched pelagic fish. Behavioural effects of high CO2 may not occur until larvae commence branchial acid-base regulation when the gills develop; however, further studies are required to test this hypothesis. Our results suggest that the early stages of kingfish development are tolerant to rising CO2 levels in the ocean.

Hidden impacts of ocean acidification to live and dead coral framework

Cold-water corals, such as Lophelia pertusa, are key habitat-forming organisms found throughout the world's oceans to 3000 m deep. The complex three-dimensional framework made by these vulnerable marine ecosystems support high biodiversity and commercially important species. Given their importance, a key question is how both the living and the dead framework will fare under projected climate change. Here, we demonstrate that over 12 months L. pertusa can physiologically acclimate to increased CO2, showing sustained net calcification. However, their new skeletal structure changes and exhibits decreased crystallographic and molecular-scale bonding organization. Although physiological acclimatization was evident, we also demonstrate that there is a negative correlation between increasing CO2 levels and breaking strength of exposed framework (approx. 20-30% weaker after 12 months), meaning the exposed bases of reefs will be less effective 'load-bearers', and will become more susceptible to bioerosion and mechanical damage by 2100.

Impacts of ocean acidification on sediment processes in shallow waters of the arctic ocean

Despite the important roles of shallow-water sediments in global biogeochemical cycling, the effects of ocean acidification on sedimentary processes have received relatively little attention. As high-latitude cold waters can absorb more CO2 and usually have a lower buffering capacity than warmer waters, acidification rates in these areas are faster than those in sub-tropical regions. The present study investigates the effects of ocean acidification on sediment composition, processes and sediment-water fluxes in an Arctic coastal system. Undisturbed sediment cores, exempt of large dwelling organisms, were collected, incubated for a period of 14 days, and subject to a gradient of pCO2 covering the range of values projected for the end of the century. On five occasions during the experimental period, the sediment cores were isolated for flux measurements (oxygen, alkalinity, dissolved inorganic carbon, ammonium, nitrate, nitrite, phosphate and silicate). At the end of the experimental period, denitrification rates were measured and sediment samples were taken at several depth intervals for solid-phase analyses. Most of the parameters and processes (i.e. mineralization, denitrification) investigated showed no relationship with the overlying seawater pH, suggesting that ocean acidification will have limited impacts on the microbial activity and associated sediment-water fluxes on Arctic shelves, in the absence of active bio-irrigating organisms. Only following a pH decrease of 1 pH unit, not foreseen in the coming 300 years, significant enhancements of calcium carbonate dissolution and anammox rates were observed. Longer-term experiments on different sediment types are still required to confirm the limited impact of ocean acidification on shallow Arctic sediment processes as observed in this study.

Sea urchins in a high CO2 world: partitioned effects of body-size, ocean warming and acidification on metabolic rate

Body-size and temperature are the major factors explaining metabolic rate, and the additional factor of pH is a major driver at the biochemical level. These three factors have frequently been found to interact, complicating the formulation of broad models predicting metabolic rates and hence ecological functioning. In this first study of the effects of warming and ocean acidification, and their potential interaction, on metabolic rate across a broad body-size range (two-to-three orders of magnitude difference in body mass) we addressed the impact of climate change on the sea urchin Heliocidaris erythrogramma in context with climate projections for east Australia, an ocean warming hotspot. Urchins were gradually introduced to two temperatures (18 and 23 °C) and two pH (7.5 and 8.0), and maintained for two months. That a new physiological steady-state had been reached, otherwise know as acclimation, was validated through identical experimental trials separated by several weeks. The relationship between body-size, temperature and acidification on the metabolic rate of H. erythrogramma was strikingly stable. Both stressors caused increases in metabolic rate; 20% for temperature and 19% for pH. Combined effects were additive; a 44% increase in metabolism. Body-size had a highly stable relationship with metabolic rate regardless of temperature or pH. None of these diverse drivers of metabolism interacted or modulated the effects of the others, highlighting the partitioned nature of how each influences metabolic rate, and the importance of achieving a full acclimation state. Despite these increases in energetic demand there was very limited capacity for compensatory modulating of feeding rate; food consumption increased only in the very smallest specimens, and only in response to temperature, and not pH. Our data show that warming, acidification and body-size all substantially affect metabolism and are highly consistent and partitioned in their effects, and for H. erythrogramma near-future climate change will incur a substantial energetic cost.

Shallow water marine sediment bacterial community shifts along a natural CO2 gradient in the Mediterranean Sea Off vulcano, Italy

The effects of increasing atmospheric CO(2) on ocean ecosystems are a major environmental concern, as rapid shoaling of the carbonate saturation horizon is exposing vast areas of marine sediments to corrosive waters worldwide. Natural CO(2) gradients off Vulcano, Italy, have revealed profound ecosystem changes along rocky shore habitats as carbonate saturation levels decrease, but no investigations have yet been made of the sedimentary habitat. Here, we sampled the upper 2 cm of volcanic sand in three zones, ambient (median pCO(2) 419 µatm, minimum Omega (arag) 3.77), moderately CO(2)-enriched (median pCO(2) 592 µatm, minimum Omega (arag) 2.96), and highly CO(2)-enriched (median pCO(2) 1611 µatm, minimum Omega (arag) 0.35). We tested the hypothesis that increasing levels of seawater pCO(2) would cause significant shifts in sediment bacterial community composition, as shown recently in epilithic biofilms at the study site. In this study, 454 pyrosequencing of the V1 to V3 region of the 16S rRNA gene revealed a shift in community composition with increasing pCO(2). The relative abundances of most of the dominant genera were unaffected by the pCO(2) gradient, although there were significant differences for some 5 % of the genera present (viz. Georgenia, Lutibacter, Photobacterium, Acinetobacter, and Paenibacillus), and Shannon Diversity was greatest in sediments subject to long-term acidification (>100 years). Overall, this supports the view that globally increased ocean pCO(2) will be associated with changes in sediment bacterial community composition but that most of these organisms are resilient. However, further work is required to assess whether these results apply to other types of coastal sediments and whether the changes in relative abundance of bacterial taxa that we observed can significantly alter the biogeochemical functions of marine sediments.

Tough as a rock-boring urchin: adult Echinometra sp. EE from the Red Sea show high resistance to ocean acidification over long-term exposures

Ocean acidification, a process caused by the continuous rise of atmospheric CO2 levels, is expected to have a profound impact on marine invertebrates. Findings of the numerous studies conducted in this field indicate high variability in species responses to future ocean conditions. This study aimed at understanding the effects of long-term exposure to elevated pCO2 conditions on the performance of adult Echinometra sp. EE from the Gulf of Aqaba (Red Sea). During an 11-month incubation under high pCO2 (1,433 µatm, pHNBS 7.7) and control (435 µatm, pHNBS 8.1) conditions, we examined the urchins' somatic and gonadal growth, gametogenesis and skeletal microstructure. Somatic and gonadal growths were exhibited with no significant differences between the treatments. In addition, all urchins in the experiment completed a full reproductive cycle, typical of natural populations, with no detectable impact of increased pCO2 on the timing, duration or progression of the cycle. Furthermore, scanning electron microscopy imaging of urchin tests and spines revealed no signs of the usual observed effects of acidosis, such as skeletal dissolution, widened stereom pores or non-smoothed structures. Our results, which yielded no significant impact of the high pCO2 treatment on any of the examined processes in the urchins studied, suggest high resistance of adult Echinometra sp. EE to near future ocean acidification conditions. With respect to other findings in this area, the outcome of this study provides an example of the complicated and diverse responses of echinoids to the predicted environmental changes.