Seafloor primary production in a changing Arctic Ocean.

Phytoplankton and sea ice algae are traditionally considered to be the main primary producers in the Arctic Ocean. In this Perspective, we explore the importance of benthic primary producers (BPPs) encompassing microalgae, macroalgae, and seagrasses, which represent a poorly quantified source of Arctic marine primary production. Despite scarce observations, models predict that BPPs are widespread, colonizing ~3 million km2 of the extensive Arctic coastal and shelf seas. Using a synthesis of published data and a novel model, we estimate that BPPs currently contribute ~77 Tg C y-1 of primary production to the Arctic, equivalent to ~20 to 35% of annual phytoplankton production. Macroalgae contribute ~43 Tg C y-1, seagrasses contribute ~23 Tg C y-1, and microalgae-dominated shelf habitats contribute ~11 to 16 Tg C y-1. Since 2003, the Arctic seafloor area exposed to sunlight has increased by ~47,000 km2 y-1, expanding the realm of BPPs in a warming Arctic. Increased macrophyte abundance and productivity is expected along Arctic coastlines with continued ocean warming and sea ice loss. However, microalgal benthic primary production has increased in only a few shelf regions despite substantial sea ice loss over the past 20 y, as higher solar irradiance in the ice-free ocean is counterbalanced by reduced water transparency. This suggests complex impacts of climate change on Arctic light availability and marine primary production. Despite significant knowledge gaps on Arctic BPPs, their widespread presence and obvious contribution to coastal and shelf ecosystem production call for further investigation and for their inclusion in Arctic ecosystem models and carbon budgets.

Rebuilding marine life.

Sustainable Development Goal 14 of the United Nations aims to "conserve and sustainably use the oceans, seas and marine resources for sustainable development". Achieving this goal will require rebuilding the marine life-support systems that deliver the many benefits that society receives from a healthy ocean. Here we document the recovery of marine populations, habitats and ecosystems following past conservation interventions. Recovery rates across studies suggest that substantial recovery of the abundance, structure and function of marine life could be achieved by 2050, if major pressures-including climate change-are mitigated. Rebuilding marine life represents a doable Grand Challenge for humanity, an ethical obligation and a smart economic objective to achieve a sustainable future.

Functional changes across marine habitats due to ocean acidification.

Global environmental change drives diversity loss and shifts in community structure. A key challenge is to better understand the impacts on ecosystem function and to connect species and trait diversity of assemblages with ecosystem properties that are in turn linked to ecosystem functioning. Here we quantify shifts in species composition and trait diversity associated with ocean acidification (OA) by using field measurements at marine CO2 vent systems spanning four reef habitats across different depths in a temperate coastal ecosystem. We find that both species and trait diversity decreased, and that ecosystem properties (understood as the interplay between species, traits, and ecosystem function) shifted with acidification. Furthermore, shifts in trait categories such as autotrophs, filter feeders, herbivores, and habitat-forming species were habitat-specific, indicating that OA may produce divergent responses across habitats and depths. Combined, these findings reveal the importance of connecting species and trait diversity of marine benthic habitats with key ecosystem properties to anticipate the impacts of global environmental change. Our results also generate new insights on the predicted general and habitat-specific ecological consequences of OA.

Magnitude and Predictability of pH Fluctuations Shape Plastic Responses to Ocean Acidification.

AbstractPhenotypic plasticity is expected to facilitate the persistence of natural populations as global change progresses. The attributes of fluctuating environments that favor the evolution of plasticity have received extensive theoretical investigation, yet empirical validation of these findings is still in its infancy. Here, we combine high-resolution environmental data with a laboratory-based experiment to explore the influence of habitat pH fluctuation dynamics on the plasticity of gene expression in two populations of the Mediterranean mussel, Mytilus galloprovincialis. We linked differences in the magnitude and predictability of pH fluctuations in two habitats to population-specific gene expression profiles in ambient and stressful pH treatments. Our results demonstrate population-based differentiation in gene expression plasticity, whereby mussels native to a habitat exhibiting a large magnitude of pH fluctuations with low predictability display reduced phenotypic plasticity between experimentally imposed pH treatments. This work validates recent theoretical findings on evolution in fluctuating environments, suggesting that the predictability of fluctuating selection pressures may play a predominant role in shaping the phenotypic variation observed across natural populations.

Ocean acidification causes variable trait-shifts in a coral species.

High pCO2 habitats and their populations provide an unparalleled opportunity to assess how species may survive under future ocean acidification conditions, and help to reveal the traits that confer tolerance. Here we utilize a unique CO2 vent system to study the effects of exposure to elevated pCO2 on trait-shifts observed throughout natural populations of Astroides calycularis, an azooxanthellate scleractinian coral endemic to the Mediterranean. Unexpected shifts in skeletal and growth patterns were found. Colonies shifted to a skeletal phenotype characterized by encrusting morphology, smaller size, reduced coenosarc tissue, fewer polyps, and less porous and denser skeletons at low pH. Interestingly, while individual polyps calcified more and extended faster at low pH, whole colonies found at low pH site calcified and extended their skeleton at the same rate as did those at ambient pH sites. Transcriptomic data revealed strong genetic differentiation among local populations of this warm water species whose distribution range is currently expanding northward. We found excess differentiation in the CO2 vent population for genes central to calcification, including genes for calcium management (calmodulin, calcium-binding proteins), pH regulation (V-type proton ATPase), and inorganic carbon regulation (carbonic anhydrase). Combined, our results demonstrate how coral populations can persist in high pCO2 environments, making this system a powerful candidate for investigating acclimatization and local adaptation of organisms to global environmental change.

Ocean acidification affects calcareous tube growth in adults and reared offspring of serpulid polychaetes.

The energetically costly transition from free-swimming larvae to a benthic life stage and maintenance of a calcareous structure can make calcifying marine invertebrates vulnerable to ocean acidification. The first goal of this study was to evaluate the impact of ocean acidification on calcified tube growth for two Serpulidae polychaete worms. Spirorbis sp. and Spirobranchus triqueter were collected at 11 m depth from the northwest Mediterranean Sea and maintained for 30 and 90 days at three mean pHT levels (total scale): 8.1 (ambient), 7.7 and 7.4. Moderately decreased tube elongation rates were observed in both species at pHT 7.7 while severe reductions occurred at pHT 7.4. There was visual evidence of dissolution and tubes were more fragile at lower pH but fragility was not attributed to changes in fracture toughness. Instead, it appeared to be due to the presence of larger alveoli covered in a thinner calcareous layer. The second objective of this study was to test for effects on S. triqueter offspring development. Spawning was induced, and offspring were reared in the same pH conditions that the parents experienced. Trochophore size was reduced at the lowest pH level but settlement success was similar across pH conditions. Post-settlement tube growth was most affected. At 38 days post-settlement, juvenile tubes at pHT 7.7 and 7.4 were half the size of those at pHT 8.1. The results suggest future carbonate chemistry will negatively affect the initiation and persistence of both biofouling and epiphytic polychaete tube worms.

Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change-A review.

Marine life is controlled by multiple physical and chemical drivers and by diverse ecological processes. Many of these oceanic properties are being altered by climate change and other anthropogenic pressures. Hence, identifying the influences of multifaceted ocean change, from local to global scales, is a complex task. To guide policy-making and make projections of the future of the marine biosphere, it is essential to understand biological responses at physiological, evolutionary and ecological levels. Here, we contrast and compare different approaches to multiple driver experiments that aim to elucidate biological responses to a complex matrix of ocean global change. We present the benefits and the challenges of each approach with a focus on marine research, and guidelines to navigate through these different categories to help identify strategies that might best address research questions in fundamental physiology, experimental evolutionary biology and community ecology. Our review reveals that the field of multiple driver research is being pulled in complementary directions: the need for reductionist approaches to obtain process-oriented, mechanistic understanding and a requirement to quantify responses to projected future scenarios of ocean change. We conclude the review with recommendations on how best to align different experimental approaches to contribute fundamental information needed for science-based policy formulation.

Near-future pH conditions severely impact calcification, metabolism and the nervous system in the pteropod Heliconoides inflatus.

Shelled pteropods play key roles in the global carbon cycle and food webs of various ecosystems. Their thin external shell is sensitive to small changes in pH, and shell dissolution has already been observed in areas where aragonite saturation state is ~1. A decline in pteropod abundance has the potential to disrupt trophic networks and directly impact commercial fisheries. Therefore, it is crucial to understand how pteropods will be affected by global environmental change, particularly ocean acidification. In this study, physiological and molecular approaches were used to investigate the response of the Mediterranean pteropod, Heliconoides inflatus, to pH values projected for 2100 under a moderate emissions trajectory (RCP6.0). Pteropods were subjected to pHT 7.9 for 3 days, and gene expression levels, calcification and respiration rates were measured relative to pHT 8.1 controls. Gross calcification decreased markedly under low pH conditions, while genes potentially involved in calcification were up-regulated, reflecting the inability of pteropods to maintain calcification rates. Gene expression data imply that under low pH conditions, both metabolic processes and protein synthesis may be compromised, while genes involved in acid-base regulation were up-regulated. A large number of genes related to nervous system structure and function were also up-regulated in the low pH treatment, including a GABAA receptor subunit. This observation is particularly interesting because GABAA receptor disturbances, leading to altered behavior, have been documented in several other marine animals after exposure to elevated CO2 . The up-regulation of many genes involved in nervous system function suggests that exposure to low pH could have major effects on pteropod behavior. This study illustrates the power of combining physiological and molecular approaches. It also reveals the importance of behavioral analyses in studies aimed at understanding the impacts of low pH on marine animals.

Effects of elevated pCO2 and feeding on net calcification and energy budget of the Mediterranean cold-water coral Madrepora oculata.

Ocean acidification is a major threat to calcifying marine organisms such as deep-sea cold-water corals (CWCs), but related knowledge is scarce. The aragonite saturation threshold (Ωa) for calcification, respiration and organic matter fluxes were investigated experimentally in the Mediterranean Madrepora oculata Over 10 weeks, colonies were maintained under two feeding regimes (uptake of 36.75 and 7.46 µmol C polyp-1 week-1) and exposed in 2 week intervals to a consecutively changing air-CO2 mix (pCO2) of 400, 1600, 800, 2000 and 400 ppm. There was a significant effect of feeding on calcification at initial ambient pCO2, while with consecutive pCO2 treatments, feeding had no effect on calcification. Respiration was not significantly affected by feeding or pCO2 levels. Coral skeletons started to dissolve at an average Ωa threshold of 0.92, but recovered and started to calcify again at Ωa≥1. The surplus energy required to counteract dissolution at elevated pCO2 (≥1600 µatm) was twice that at ambient pCO2 Yet, feeding had no mitigating effect at increasing pCO2 levels. This could be due to the fact that the energy required for calcification is a small fraction (1-3%) of the total metabolic energy demand and corals even under low food conditions might therefore still be able to allocate this small portion of energy to calcification. The response and resistance to ocean acidification are consequently not controlled by feeding in this species, but more likely by chemical reactions at the site of calcification and exchange processes between the calicoblastic layer and ambient seawater.

Response of two temperate scleractinian corals to projected ocean warming and marine heatwaves.

The Mediterranean Sea is a hotspot of global change, particularly exposed to ocean warming and the increasing occurrence of marine heatwaves (MHWs). However, experiments based on long-term temperature data from the field are scarce. Here, we investigate the response of the zooxanthellate coral Cladocora caespitosa and the azooxanthellate coral Astroides calycularis to future warming and MHWs based on 8 years of in situ data. Corals were maintained in the laboratory for five months under four temperature conditions: Warming (3.2°C above the in situ mean from 2012 to 2020), Heatwave (temperatures of 2018 with two heatwaves), Ambient (in situ mean) and Cool (deeper water temperatures). Under the Warming treatment, some C. caespitosa colonies severely bleached and A. calycularis colonies presented necrosis. Cladocora caespitosa symbiosis was impaired by temperature with a decrease in the density of endosymbiotic algae and an increase in per cent whiteness in all the treatments except for the coolest. Recovery for both species was observed through different mechanisms such as regrowth of polyps of A. calycularis and recovery of pigmentation for C. caespitosa. These results suggest that A. calycularis and C. caespitosa may be resilient to heat stress and can recover from physiological stresses caused by heatwaves in the laboratory.

Elevated heterotrophic capacity as a strategy for Mediterranean corals to cope with low pH at CO2 vents.

The global increase in anthropogenic CO2 is leading to ocean warming and acidification, which is threatening corals. In Ischia, Italy, two species of Mediterranean scleractinian corals-the symbiotic Cladocora caespitosa and the asymbiotic Astroides calycularis-were collected from ambient pH sites (average pHT = 8.05) and adjacent CO2 vent sites (average pHT = 7.8) to evaluate their response to ocean acidification. Coral colonies from both sites were reared in a laboratory setting for six months at present day pH (pHT ~ 8.08) or low pH (pHT ~7.72). Previous work showed that these corals were tolerant of low pH and maintained positive calcification rates throughout the experiment. We hypothesized that these corals cope with low pH by increasing their heterotrophic capacity (i.e., feeding and/or proportion of heterotrophically derived compounds incorporated in their tissues), irrespective of site of origin, which was quantified indirectly by measuring δ13C, δ15N, and sterols. To further characterize coral health, we quantified energy reserves by measuring biomass, total lipids, and lipid classes. Additional analysis for C. caespitosa included carbohydrates (an energy reserve) and chlorophyll a (an indicator of photosynthetic capacity). Isotopic evidence shows that ambient-sourced Mediterranean corals, of both species, decreased heterotrophy in response to six months of low pH. Despite maintaining energy reserves, lower net photosynthesis (C. caespitosa) and a trend of declining calcification (A. calycularis) suggest a long-term cost to low heterotrophy under ocean acidification conditions. Conversely, vent-sourced corals maintained moderate (C. caespitosa) or high (A. calycularis) heterotrophic capacity and increased photosynthesis rates (C. caespitosa) in response to six months at low pH, allowing them to sustain themselves physiologically. Provided there is sufficient zooplankton and/or organic matter to meet their heterotrophic needs, vent-sourced corals are more likely to persist this century and potentially be a source for new corals in the Mediterranean.

Sustainability limits needed for CO2 removal.

The true climate mitigation challenge is revealed by considering sustainability impacts.

Productivity of mixed kelp communities in an Arctic fjord exhibit tolerance to a future climate.

Arctic fjords are considered to be one of the ecosystems changing most rapidly in response to climate change. In the Svalbard archipelago, fjords are experiencing a shift in environmental conditions due to the Atlantification of Arctic waters and the retreat of sea-terminating glaciers. These environmental changes are predicted to facilitate expansion of large, brown macroalgae, into new ice-free regions. The potential resilience of macroalgal benthic communities in these fjord systems will depend on their response to combined pressures from freshening due to glacial melt, exposure to warmer waters, and increased turbidity from meltwater runoff which reduces light penetration. Current predictions, however, have a limited ability to elucidate the future impacts of multiple-drivers on macroalgal communities with respect to ecosystem function and biogeochemical cycling in Arctic fjords. To assess the impact of these combined future environmental changes on benthic productivity and resilience, we conducted a two-month mesocosm experiment exposing mixed kelp communities to three future conditions comprising increased temperature (+ 3.3 and + 5.3°C), seawater freshening by ∼ 3.0 and ∼ 5.0 units (i.e., salinity of 30 and 28, respectively), and decreased photosynthetically active radiation (PAR, - 25 and - 40 %). Exposure to these combined treatments resulted in non-significant differences in short-term productivity, and a tolerance of the photosynthetic capacity across the treatment conditions. We present the first robust estimates of mixed kelp community production in Kongsfjorden and place a median compensation irradiance of ∼12.5 mmol photons m-2 h-1 as the threshold for positive net community productivity. These results are discussed in the context of ecosystem productivity and biological tolerance of kelp communities in future Arctic fjord systems.

Taking action against ocean acidification: a review of management and policy options.

Ocean acidification has emerged over the last two decades as one of the largest threats to marine organisms and ecosystems. However, most research efforts on ocean acidification have so far neglected management and related policy issues to focus instead on understanding its ecological and biogeochemical implications. This shortfall is addressed here with a systematic, international and critical review of management and policy options. In particular, we investigate the assumption that fighting acidification is mainly, but not only, about reducing CO2 emissions, and explore the leeway that this emerging problem may open in old environmental issues. We review nine types of management responses, initially grouped under four categories: preventing ocean acidification; strengthening ecosystem resilience; adapting human activities; and repairing damages. Connecting and comparing options leads to classifying them, in a qualitative way, according to their potential and feasibility. While reducing CO2 emissions is confirmed as the key action that must be taken against acidification, some of the other options appear to have the potential to buy time, e.g. by relieving the pressure of other stressors, and help marine life face unavoidable acidification. Although the existing legal basis to take action shows few gaps, policy challenges are significant: tackling them will mean succeeding in various areas of environmental management where we failed to a large extent so far.

Microbial associates of an endemic Mediterranean seagrass enhance the access of the host and the surrounding seawater to inorganic nitrogen under ocean acidification.

Seagrasses are important primary producers in oceans worldwide. They live in shallow coastal waters that are experiencing carbon dioxide enrichment and ocean acidification. Posidonia oceanica, an endemic seagrass species that dominates the Mediterranean Sea, achieves high abundances in seawater with relatively low concentrations of dissolved inorganic nitrogen. Here we tested whether microbial metabolisms associated with P. oceanica and surrounding seawater enhance seagrass access to nitrogen. Using stable isotope enrichments of intact seagrass with amino acids, we showed that ammonification by free-living and seagrass-associated microbes produce ammonium that is likely used by seagrass and surrounding particulate organic matter. Metagenomic analysis of the epiphytic biofilm on the blades and rhizomes support the ubiquity of microbial ammonification genes in this system. Further, we leveraged the presence of natural carbon dioxide vents and show that the presence of P. oceanica enhanced the uptake of nitrogen by water column particulate organic matter, increasing carbon fixation by a factor of 8.6-17.4 with the greatest effect at CO2 vent sites. However, microbial ammonification was reduced at lower pH, suggesting that future ocean climate change will compromise this microbial process. Thus, the seagrass holobiont enhances water column productivity, even in the context of ocean acidification.

Impact of aragonite saturation state changes on migratory pteropods.

Thecosome pteropods play a key role in the food web of various marine ecosystems and they calcify, secreting the unstable CaCO(3) mineral aragonite to form their shell material. Here, we have estimated the effect of ocean acidification on pteropod calcification by exploiting empirical relationships between their gross calcification rates (CaCO(3) precipitation) and aragonite saturation state Ω(a), combined with model projections of future Ω(a). These were corrected for modern model-data bias and taken over the depth range where pteropods are observed to migrate vertically. Results indicate large reductions in gross calcification at temperate and high latitudes. Over much of the Arctic, the pteropod Limacina helicina will become unable to precipitate CaCO(3) by the end of the century under the IPCC SRES A2 scenario. These results emphasize concerns over the future of shelled pteropods, particularly L. helicina in high latitudes. Shell-less L. helicina are not known to have ever existed nor would we expect them to survive. Declines of pteropod populations could drive dramatic ecological changes in the various pelagic ecosystems in which they play a critical role.

Molecular basis of ocean acidification sensitivity and adaptation in Mytilus galloprovincialis.

Predicting the potential for species adaption to climate change is challenged by the need to identify the physiological mechanisms that underpin species vulnerability. Here, we investigated the sensitivity to ocean acidification in marine mussels during early development, and specifically the trochophore stage. Using RNA and DNA sequencing and in situ RNA hybridization, we identified developmental processes associated with abnormal development and rapid adaptation to low pH. Trochophores exposed to low pH seawater exhibited 43 differentially expressed genes. Gene annotation and in situ hybridization of differentially expressed genes point to pH sensitivity of (1) shell field development and (2) cellular stress response. Five genes within these two processes exhibited shifts in allele frequencies indicative of a potential for rapid adaptation. This case study contributes direct evidence that protecting species' existing genetic diversity is a critical management action to facilitate species resilience to climate change.

Global seaweed productivity.

The magnitude and distribution of net primary production (NPP) in the coastal ocean remains poorly constrained, particularly for shallow marine vegetation. Here, using a compilation of in situ annual NPP measurements across >400 sites in 72 geographic ecoregions, we provide global predictions of the productivity of seaweed habitats, which form the largest vegetated coastal biome on the planet. We find that seaweed NPP is strongly coupled to climatic variables, peaks at temperate latitudes, and is dominated by forests of large brown seaweeds. Seaweed forests exhibit exceptionally high per-area production rates (a global average of 656 and 1711 gC m-2 year-1 in the subtidal and intertidal, respectively), being up to 10 times higher than coastal phytoplankton in temperate and polar seas. Our results show that seaweed NPP is a strong driver of production in the coastal ocean and call for its integration in the oceanic carbon cycle, where it has traditionally been overlooked.

Early development and molecular plasticity in the Mediterranean sea urchin Paracentrotus lividus exposed to CO2-driven acidification.

Ocean acidification is predicted to have significant effects on benthic calcifying invertebrates, in particular on their early developmental stages. Echinoderm larvae could be particularly vulnerable to decreased pH, with major consequences for adult populations. The objective of this study was to understand how ocean acidification would affect the initial life stages of the sea urchin Paracentrotus lividus, a common species that is widely distributed in the Mediterranean Sea and the NE Atlantic. The effects of decreased pH (elevated P(CO(2))) were investigated through physiological and molecular analyses on both embryonic and larval stages. Eggs and larvae were reared in Mediterranean seawater at six pH levels, i.e. pH(T) 8.1, 7.9, 7.7, 7.5, 7.25 and 7.0. Fertilization success, survival, growth and calcification rates were monitored over a 3 day period. The expression of genes coding for key proteins involved in development and biomineralization was also monitored. Paracentrotus lividus appears to be extremely resistant to low pH, with no effect on fertilization success or larval survival. Larval growth was slowed when exposed to low pH but with no direct impact on relative larval morphology or calcification down to pH(T) 7.25. Consequently, at a given time, larvae exposed to low pH were present at a normal but delayed larval stage. More surprisingly, candidate genes involved in development and biomineralization were upregulated by factors of up to 26 at low pH. Our results revealed plasticity at the gene expression level that allows a normal, but delayed, development under low pH conditions.