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.

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.

Sustainability limits needed for CO2 removal.

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

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.

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.

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.

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.

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.

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.

Near-future ocean warming and acidification alter foraging behaviour, locomotion, and metabolic rate in a keystone marine mollusc.

Environmentally-induced changes in fitness are mediated by direct effects on physiology and behaviour, which are tightly linked. We investigated how predicted ocean warming (OW) and acidification (OA) affect key ecological behaviours (locomotion speed and foraging success) and metabolic rate of a keystone marine mollusc, the sea hare Stylocheilus striatus, a specialist grazer of the toxic cyanobacterium Lyngbya majuscula. We acclimated sea hares to OW and/or OA across three developmental stages (metamorphic, juvenile, and adult) or as adults only, and compare these to sea hares maintained under current-day conditions. Generally, locomotion speed and time to locate food were reduced ~1.5- to 2-fold when the stressors (OW or OA) were experienced in isolation, but reduced ~3-fold when combined. Decision-making was also severely altered, with correct foraging choice nearly 40% lower under combined stressors. Metabolic rate appeared to acclimate to the stressors in isolation, but was significantly elevated under combined stressors. Overall, sea hares that developed under OW and/or OA exhibited a less severe impact, indicating beneficial phenotypic plasticity. Reduced foraging success coupled with increased metabolic demands may impact fitness in this species and highlight potentially large ecological consequences under unabated OW and OA, namely in regulating toxic cyanobacteria blooms on coral reefs.

Drivers of Microbial Carbon Fluxes Variability in Two Oligotrophic Mediterranean Coastal Systems.

The carbon fluxes between phytoplankton and heterotrophic bacterioplankton were studied in two coastal oligotrophic sites in the NW Mediterranean. Phytoplankton and bacterial production rates were measured under natural conditions using different methods. In the Bay of Villefranche, the temporal variability revealed net heterotrophy in July-October and net autotrophy in December-March. The spatial variability was studied in the Bay of Palma, showing net autotrophic areas in the west and heterotrophic areas in the east. On average bacterial respiration, represented 62% of the total community respiration. Bacterial growth efficiency (BGE) values were significantly higher in autotrophic conditions than in heterotrophic ones. During autotrophic periods, dissolved primary production (DPP) was enough to sustained bacterial metabolism, although it showed a positive correlation with organic carbon stock (DOC). Under heterotrophic conditions, DPP did not sustain bacterial metabolism but bacterial respiration correlated with DPP and bacterial production with DOC. Temperature affected positively, DOC, BGE, bacterial respiration and production when the trophic status was autotrophic. To summarize, the response of bacterial metabolism to temperature and carbon sources depends on the trophic status within these oligotrophic coastal systems.

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.

Bottom-up effects on biomechanical properties of the skeletal plates of the sea urchin Paracentrotus lividus (Lamarck, 1816) in an acidified ocean scenario.

Sea urchins, ecologically important herbivores of shallow subtidal temperate reefs, are considered particularly threatened in a future ocean acidification scenario, since their carbonate structures (skeleton and grazing apparatus) are made up of the very soluble high-magnesium calcite, particularly sensitive to a decrease in pH. The biomechanical properties of their skeletal structures are of great importance for their individual fitness, because the skeleton provides the means for locomotion, grazing and protection from predators. Sea urchin skeleton is composed of discrete calcite plates attached to each other at sutures by organic ligaments. The present study addressed the fate of the sea urchin Paracentrotus lividus (Lamarck, 1816) skeleton in acidified oceans, taking into account the combined effect of reduced pH and macroalgal diet, with potential cascading consequences at the ecosystem level. A breaking test on individual plates of juvenile specimens fed different macroalgal diets has been performed, teasing apart plate strength and stiffness from general robustness. Results showed no direct short-term effect of a decrease in seawater pH nor of the macroalgal diet on single plate mechanical properties. Nevertheless, results from apical plates, the ones presumably formed during the experimental period, provided an indication of a possible diet-mediated response, with sea urchins fed the more calcified macroalga sustaining higher forces before breakage than the one fed the non-calcified algae. This, on the long term, may produce bottom-up effects on sea urchins, leading to potential shifts in the ecosystem equilibrium under an ocean acidified scenario.

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.

Taking the metabolic pulse of the world's coral reefs.

Worldwide, coral reef ecosystems are experiencing increasing pressure from a variety of anthropogenic perturbations including ocean warming and acidification, increased sedimentation, eutrophication, and overfishing, which could shift reefs to a condition of net calcium carbonate (CaCO3) dissolution and erosion. Herein, we determine the net calcification potential and the relative balance of net organic carbon metabolism (net community production; NCP) and net inorganic carbon metabolism (net community calcification; NCC) within 23 coral reef locations across the globe. In light of these results, we consider the suitability of using these two metrics developed from total alkalinity (TA) and dissolved inorganic carbon (DIC) measurements collected on different spatiotemporal scales to monitor coral reef biogeochemistry under anthropogenic change. All reefs in this study were net calcifying for the majority of observations as inferred from alkalinity depletion relative to offshore, although occasional observations of net dissolution occurred at most locations. However, reefs with lower net calcification potential (i.e., lower TA depletion) could shift towards net dissolution sooner than reefs with a higher potential. The percent influence of organic carbon fluxes on total changes in dissolved inorganic carbon (DIC) (i.e., NCP compared to the sum of NCP and NCC) ranged from 32% to 88% and reflected inherent biogeochemical differences between reefs. Reefs with the largest relative percentage of NCP experienced the largest variability in seawater pH for a given change in DIC, which is directly related to the reefs ability to elevate or suppress local pH relative to the open ocean. This work highlights the value of measuring coral reef carbonate chemistry when evaluating their susceptibility to ongoing global environmental change and offers a baseline from which to guide future conservation efforts aimed at preserving these valuable ecosystems.

Comparison of Mediterranean Pteropod Shell Biometrics and Ultrastructure from Historical (1910 and 1921) and Present Day (2012) Samples Provides Baseline for Monitoring Effects of Global Change.

Anthropogenic carbon perturbation has caused decreases in seawater pH and increases in global temperatures since the start of the 20th century. The subsequent lowering of the saturation state of CaCO3 may make the secretion of skeletons more problematic for marine calcifiers. As organisms that precipitate thin aragonite shells, thecosome pteropods have been identified as being particularly vulnerable to climate change effects. Coupled with their global distribution, this makes them ideal for use as sentinel organisms. Recent studies have highlighted shell dissolution as a potential indicator of ocean acidification; however, this metric is not applicable for monitoring pH changes in supersaturated basins. In this study, the novel approach of high resolution computed tomography (CT) scanning was used to produce quantitative 3-dimensional renderings pteropod shells to assess the potential of using this method to monitor small changes in shell biometrics that may be driven by climate change drivers. An ontogenetic analysis of the shells of Cavolinia inflexa and Styliola subula collected from the Mediterranean was used to identify suitable monitoring metrics. Modern samples were then compared to historical samples of the same species, collected during the Mediterranean leg of the Thor (1910) and Dana (1921) cruises to assess whether any empirical differences could be detected. Shell densities were calculated and scanning electron microscopy was used to compare the aragonite crystal morphology. pH for the collection years was hind-cast using temperature and salinity time series with atmospheric CO2 concentrations from ice core data. Historical samples of S. subula were thicker than S. subula shells of the same size from 2012 and C. inflexa shells collected in 1910 were significantly denser than those from 2012. These results provide a baseline for future work to develop monitoring techniques for climate change in the oceans using the novel approach of high-resolution CT scanning.

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.