The effect of Ocean Acidification (OA) on marine biota is quasi-predictable at best. While perturbation studies, in the form of incubations under elevated pCO2, reveal sensitivities and responses of individual species, one missing link in the OA story results from a chronic lack of pH data specific to a given species' natural habitat. Here, we present a compilation of continuous, high-resolution time series of upper ocean pH, collected using autonomous sensors, over a variety of ecosystems ranging from polar to tropical, open-ocean to coastal, kelp forest to coral reef. These observations reveal a continuum of month-long pH variability with standard deviations from 0.004 to 0.277 and ranges spanning 0.024 to 1.430 pH units. The nature of the observed variability was also highly site-dependent, with characteristic diel, semi-diurnal, and stochastic patterns of varying amplitudes. These biome-specific pH signatures disclose current levels of exposure to both high and low dissolved CO2, often demonstrating that resident organisms are already experiencing pH regimes that are not predicted until 2100. Our data provide a first step toward crystallizing the biophysical link between environmental history of pH exposure and physiological resilience of marine organisms to fluctuations in seawater CO2. Knowledge of this spatial and temporal variation in seawater chemistry allows us to improve the design of OA experiments: we can test organisms with a priori expectations of their tolerance guardrails, based on their natural range of exposure. Such hypothesis-testing will provide a deeper understanding of the effects of OA. Both intuitively simple to understand and powerfully informative, these and similar comparative time series can help guide management efforts to identify areas of marine habitat that can serve as refugia to acidification as well as areas that are particularly vulnerable to future ocean change.
Late in summer 2003, extensive mass mortality of at least 25 rocky benthic macro-invertebrate species (mainly gorgonians and sponges) was observed in the entire Northwestern (NW) Mediterranean region, affecting several thousand kilometers of coastline. We were able to characterize the mortality event by studying six areas covering the main regions of the NW Mediterranean basin. The degree of impact on each study area was quantified at 49 sites by estimating the proportion of colonies affected in populations of several gorgonian species compared with reference data obtained in years without mortality signs. According to these data, the western areas (Catalan coast and Balearic Islands) were the least affected, while the central areas (Provence coast and Corsica-Sardinia) showed a moderate impact. The northernmost and eastern areas (Gulf of Genoa and Gulf of Naples) displayed the highest impact, with almost 80% of gorgonian colonies affected. The heat wave of 2003 in Europe caused an anomalous warming of seawater, which reached the highest temperatures ever recorded in the studied regions, between 1 and 3 degrees C above the climatic values (mean and maximum). Because this exceptional warming was observed in the depth ranges most affected by the mortality, it seems likely that the 2003 anomalous temperature played a key role in the observed mortality event. A correlation analysis between temperature conditions and degree of impact seems to support this hypothesis. Under the present climate warming trend, new mass mortality events may occur in the near future, possibly driving a major biodiversity crisis in the Mediterranean Sea
Ocean acidification is predicted to impact all areas of the oceans and affect a diversity of marine organisms. However, the diversity of responses among species prevents clear predictions about the impact of acidification at the ecosystem level. Here, we used shallow water CO 2 vents in the Mediterranean Sea as a model system to examine emergent ecosystem responses to ocean acidification in rocky reef communities. We assessed in situ benthic invertebrate communities in three distinct pH zones (ambient, low, and extreme low), which differed in both the mean and variability of seawater pH along a continuous gradient. We found fewer taxa, reduced taxonomic evenness, and lower biomass in the extreme low pH zones. However, the number of individuals did not differ among pH zones, suggesting that there is density compensation through population blooms of small acidificationtolerant taxa. Furthermore, the trophic structure of the invertebrate community shifted to fewer trophic groups and dominance by generalists in extreme low pH, suggesting that there may be a simplification of food webs with ocean acidification. Despite high variation in individual species' responses, our findings indicate that ocean acidification decreases the diversity, biomass, and trophic complexity of benthic marine communities. These results suggest that a loss of biodiversity and ecosystem function is expected under extreme acidification scenarios.global change | natural gradient | emergent effects
More than 60 marine non-indigenous species (NIS) have been removed from previous lists and 84 species have been added, bringing the total to 986 alien species in the Mediterranean [775 in the eastern Mediterranean (EMED), 249 in the central Mediterranean (CMED), 190 in the Adriatic Sea (ADRIA) and 308 in the western Mediterranean (WMED)]. There were 48 new entries since 2011 which can be interpreted as approximately one new entry every two weeks. The number of alien species continues to increase, by 2-3 species per year for macrophytes, molluscs and polychaetes, 3-4 species per year for crustaceans, and 6 species per year for fish. The dominant group among alien species is molluscs (with 215 species), followed by crustaceans (159) and polychaetes (132). Macrophytes are the leading group of NIS in the ADRIA and the WMED, reaching 26-30% of all aliens, whereas in the EMED they barely constitute 10% of the introductions. In the EMED, molluscs are the most species-rich group, followed by crustaceans, fish and polychaetes. More than half (54%) of the marine alien species in the Mediterranean were probably introduced by corridors (mainly Suez). Shipping is blamed directly for the introduction of only 12 species, whereas it is assumed to be the most likely pathway of introduction (via ballasts or fouling) of another 300 species. For approximately 100 species shipping is a probable pathway along with the Suez Canal and/or aquaculture. Approximately 20 species have been introduced with certainty via aquaculture, while >50 species (mostly macroalgae), occurring in the vicinity of oyster farms, are assumed to be introduced accidentally as contaminants of imported species. A total of 18 species are assumed to have been introduced by the aquarium trade. Lessepsian species decline westwards, while the reverse pattern is evident for ship-mediated species and for those introduced with aquaculture. There is an increasing trend in new introductions via the Suez Canal and via shipping.
Flow dynamics in Zostera marina L. (eelgrass) were studied in a large seawater flume. Velocity and turbulence intensity profiles were measured at 3 free-stream flow velocities (5. 10 and 20 cm S-'), at 5 shoot densities (1200, 1000,800, 600 and 400 shoots rne2), and at 5 along-stream positions relative to the leading edge of the eelgrass bed (10 cm upstream of the bed; 25, 50, 75 and 100 cm downstream of the leading edge of the bed). All the profiles (75) above the canopy or over bare sand fitted a log-profile relationship. At all densities and ambient velocities tested, mean velocity increased above the canopy, while within the bed water speed dropped distinctly below the canopy-water interface. Depending on shoot density, water speed was from 2 to 10 times lower under the canopy than upstream of the seagrass bed. Shear velocities (U%) above the canopy were 2 to 11 times greater than outside the bed at equivalent height, and Increased significantly with distance into the meadow. No significant differences among dens~ties were observed. Turbulence intensity showed a dramatic increase in all the profiles at the canopy-water interface, a significant increase with distance into the bed, but showed no significant differences between densities. Fluid flux within the bed decreased significantly with distance into the meadow, but exhibited no significant dependence on density. Downstream, vertically integrated fluid flux at 100 cm into the bed ranged between 14.7 and 40.6 O/O of upstream values. The least flux reduction occurred at the highest velocity (20 cm S-'). Trends in shear velocity and turbulence intensity show clearly that within the bed one can distinguish 2 dynamically different environments. The 'canopy-water interface' habitat 1s characterized by high shear stress and high turbulence intensity; the 'below-canopy' habitat is characterized by low shear stress and a reduction of turbulence intensity.
Ocean acidification represents a pervasive environmental change that is predicted to affect a wide range of species 1,2 , yet our understanding of the emergent ecosystem impacts is very limited. Many studies report detrimental effects of acidification on single species in lab studies, especially those with calcareous shells or skeletons 3-5 . Observational studies using naturally acidified ecosystems have shown profound shifts away from such calcareous species 6-8 , and there has been an assumption that direct impacts of acidification on sensitive species drive most ecosystem responses. We tested an alternative hypothesis that species interactions attenuate or amplify the direct effects of acidification on individual species 9-12 . Here, we show that altered competitive dynamics between calcareous species and fleshy seaweeds drive significant ecosystem shifts in acidified conditions. Although calcareous species recruited and grew at similar rates in ambient and low pH conditions during early successional stages, they were rapidly overgrown by fleshy seaweeds later in succession in low pH conditions. The altered competitive dynamics between calcareous species and fleshy seaweeds is probably the combined result of decreased growth rates of calcareous species, increased growth rates of fleshy seaweeds, and/or altered grazing rates 13 . Phase shifts towards ecosystems dominated by fleshy seaweed are common in many marine ecosystems 14-16 , and our results suggest that changes in the competitive balance between these groups represent a key leverage point through which the physiological responses of individual species to acidification could indirectly lead to profound ecosystem changes in an acidified ocean.We deployed recruitment substrates in zones of extreme low, low and ambient seawater pH caused by shallow CO 2 vents at two replicate sites (Supplementary Fig. S1). The pH zones are caused by spatial variability in CO 2 venting 6 , resulting in decreased pH and carbonate ion concentrations and increased dissolved inorganic carbon at ambient temperature and alkalinity (Supplementary Fig. S1 and Table S1). The carbonate chemistry in the ambient pH zone is comparable to current conditions in the temperate surface ocean in the Mediterranean, whereas the low pH zones are comparable to predictions for the acidification of the near-future surface ocean (in the year 2100; ref. 17). The carbonate chemistry in the extreme low pH zones is not predicted in the near future but provides an endmember scenario for understanding acidification impacts. Previous studies have highlighted a reduction in diversity and the abundance of calcareous species in the low and extreme low pH zones 6,7,18 , but the processes underlying these patterns have not been investigated. Recruitment tiles were deployed at the beginning of the growing season for algae, and an independent
We present the Wrst study of the eVects of ocean acidiWcation on settlement of benthic invertebrates and microfauna. ArtiWcial collectors were placed for 1 month along pH gradients at CO 2 vents oV Ischia (Tyrrhenian Sea, Italy). Seventy-nine taxa were identiWed from six main taxonomic groups (foraminiferans, nematodes, polychaetes, molluscs, crustaceans and chaetognaths). Calcareous foraminiferans, serpulid polychaetes, gastropods and bivalves showed highly signiWcant reductions in recruitment to the collectors as pCO 2 rose from normal (336-341 ppm, pH 8.09-8.15) to high levels (886-5,148 ppm) causing acidi-Wed conditions near the vents (pH 7.08-7.79). Only the syllid polychaete Syllis prolifera had higher abundances at the most acidiWed station, although a wide range of polychaetes and small crustaceans was able to settle and survive under these conditions. A few taxa (Amphiglena mediterranea, Leptochelia dubia, Caprella acanthifera) were particularly abundant at stations acidiWed by intermediate amounts of CO 2 (pH 7.41-7.99). These results show that increased levels of CO 2 can profoundly aVect the settlement of a wide range of benthic organisms. Communicated by F. Bulleri. M. Cigliano and M. C. Gambi contributed equally.
Metabolic rate determines the physiological and life-history performances of ectotherms. Thus, the extent to which such rates are sensitive and plastic to environmental perturbation is central to an organism's ability to function in a changing environment. Little is known of long-term metabolic plasticity and potential for metabolic adaptation in marine ectotherms exposed to elevated p CO 2 . Consequently, we carried out a series of in situ transplant experiments using a number of tolerant and sensitive polychaete species living around a natural CO 2 vent system. Here, we show that a marine metazoan (i.e. Platynereis dumerilii ) was able to adapt to chronic and elevated levels of p CO 2 . The vent population of P. dumerilii was physiologically and genetically different from nearby populations that experience low p CO 2 , as well as smaller in body size. By contrast, different populations of Amphiglena mediterranea showed marked physiological plasticity indicating that adaptation or acclimatization are both viable strategies for the successful colonization of elevated p CO 2 environments. In addition, sensitive species showed either a reduced or increased metabolism when exposed acutely to elevated p CO 2 . Our findings may help explain, from a metabolic perspective, the occurrence of past mass extinction, as well as shed light on alternative pathways of resilience in species facing ongoing ocean acidification.
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