Shift in algal blooms from micro- to macroalgae around China with increasing eutrophication and climate change.

Blooms of microalgal red tides and macroalgae (e.g., green and golden tides caused by Ulva and Sargassum) have caused widespread problems around China in recent years, but there is uncertainty around what triggers these blooms and how they interact. Here, we use 30 years of monitoring data to help answer these questions, focusing on the four main species of microalgae Prorocentrum donghaiense, Karenia mikimotoi, Noctiluca scintillans, and Skeletonema costatum) associated with red tides in the region. The frequency of red tides increased from 1991 to 2003 and then decreased until 2020, with S. costatum red tides exhibiting the highest rate of decrease. Green tides started to occur around China in 1999 and the frequency of green tides has since been on the increase. Golden tides were first reported to occur around China in 2012. The frequency of macroalgal blooms has a negative linear relationship with the frequency and coverage of red tides around China, and a positive correlation with total nitrogen and phosphorus loads as well as with atmospheric CO2 and sea surface temperature (SST). Increased outbreaks of macroalgal blooms are very likely due to worsening levels of eutrophication, combined with rising CO2 and SST, which contribute to the reduced frequency of red tides. The increasing grazing rate of microzooplankton also results in the decline in areas affected by red tides. This study shows a clear shift of algal blooms from microalgae to macroalgae around China over the past 30 years driven by the combination of eutrophication, climate change, and grazing stress, indicating a fundamental change in coastal systems in the region.

Levelling-up rhodolith-bed science to address global-scale conservation challenges.

Global marine conservation remains fractured by an imbalance in research efforts and policy actions, limiting progression towards sustainability. Rhodolith beds represent a prime example, as they have ecological importance on a global scale, provide a wealth of ecosystem functions and services, including biodiversity provision and potential climate change mitigation, but remain disproportionately understudied, compared to other coastal ecosystems (tropical coral reefs, kelp forests, mangroves, seagrasses). Although rhodolith beds have gained some recognition, as important and sensitive habitats at national/regional levels during the last decade, there is still a notable lack of information and, consequently, specific conservation efforts. We argue that the lack of information about these habitats, and the significant ecosystem services they provide, is hindering the development of effective conservation measures and limiting wider marine conservation success. This is becoming a pressing issue, considering the multiple severe pressures and threats these habitats are exposed to (e.g., pollution, fishing activities, climate change), which may lead to an erosion of their ecological function and ecosystem services. By synthesizing the current knowledge, we provide arguments to highlight the importance and urgency of levelling-up research efforts focused on rhodolith beds, combating rhodolith bed degradation and avoiding the loss of associated biodiversity, thus ensuring the sustainability of future conservation programs.

Ocean acidification stunts molluscan growth at CO2 seeps.

Ocean acidification can severely affect bivalve molluscs, especially their shell calcification. Assessing the fate of this vulnerable group in a rapidly acidifying ocean is therefore a pressing challenge. Volcanic CO2 seeps are natural analogues of future ocean conditions that offer unique insights into the scope of marine bivalves to cope with acidification. Here, we used a 2-month reciprocal transplantation of the coastal mussel Septifer bilocularis collected from reference and elevated pCO2 habitats to explore how they calcify and grow at CO2 seeps on the Pacific coast of Japan. We found significant decreases in condition index (an indication of tissue energy reserves) and shell growth of mussels living under elevated pCO2 conditions. These negative responses in their physiological performance under acidified conditions were closely associated with changes in their food sources (shown by changes to the soft tissue δ13C and δ15N ratios) and changes in their calcifying fluid carbonate chemistry (based on shell carbonate isotopic and elemental signatures). The reduced shell growth rate during the transplantation experiment was further supported by shell δ13C records along their incremental growth layers, as well as their smaller shell size despite being of comparable ontogenetic ages (5-7 years old, based on shell δ18O records). Taken together, these findings demonstrate how ocean acidification at CO2 seeps affects mussel growth and reveal that lowered shell growth helps them survive stressful conditions.

Ocean acidification increases the impact of typhoons on algal communities.

Long-term environmental change, sudden pulses of extreme perturbation, or a combination of both can trigger regime shifts by changing the processes and feedbacks which determine community assembly, structure, and function, altering the state of ecosystems. Our understanding of the mechanisms that stabilise against regime shifts or lock communities into altered states is limited, yet also critical to anticipating future states, preventing regime shifts, and reversing unwanted state change. Ocean acidification contributes to the restructuring and simplification of algal systems, however the mechanisms through which this occurs and whether additional drivers are involved requires further study. Using monthly surveys over three years at a shallow-water volcanic seep we examined how the composition of algal communities change seasonally and following periods of significant physical disturbance by typhoons at three levels of ocean acidification (equivalent to means of contemporary ∼350 and future ∼500 and 900 µatm pCO2). Sites exposed to acidification were increasingly monopolised by structurally simple, fast-growing turf algae, and were clearly different to structurally complex macrophyte-dominated reference sites. The distinct contemporary and acidified community states were stabilised and maintained at their respective sites by different mechanisms following seasonal typhoon disturbance. Macroalgal-dominated sites were resistant to typhoon damage. In contrast, significant losses of algal biomass represented a near total ecosystem reset by typhoons for the turf-dominated communities at the elevated pCO2 sites (i.e. negligible resistance). A combination of disturbance and subsequent turf recovery maintained the same simplified state between years (elevated CO2 levels promote turf growth following algal removal, inhibiting macroalgal recruitment). Thus, ocean acidification may promote shifts in algal systems towards degraded ecosystem states, and short-term disturbances which reset successional trajectories may 'lock-in' these alternative states of low structural and functional diversity.

Whole community and functional gene changes of biofilms on marine plastic debris in response to ocean acidification.

Plastics are accumulating in the world's oceans, while ocean waters are becoming acidified by increased CO2. We compared metagenome of biofilms on tethered plastic bottles in subtidal waters off Japan naturally enriched in CO2, compared to normal ambient CO2 levels. Extending from an earlier amplicon study of bacteria, we used metagenomics to provide direct insights into changes in the full range of functional genes and the entire taxonomic tree of life in the context of the changing plastisphere. We found changes in the taxonomic community composition of all branches of life. This included a large increase in diatom relative abundance across the treatments but a decrease in diatom diversity. Network complexity among families decreased with acidification, showing overall simplification of biofilm integration. With acidification, there was decreased prevalence of genes associated with cell-cell interactions and antibiotic resistance, decreased detoxification genes, and increased stress tolerance genes. There were few nutrient cycling gene changes, suggesting that the role of plastisphere biofilms in nutrient processes within an acidified ocean may not change greatly. Our results suggest that as ocean CO2 increases, the plastisphere will undergo broad-ranging changes in both functional and taxonomic composition, especially the ecologically important diatom group, with possible wider implications for ocean ecology.

Decreased Diversity and Abundance of Marine Invertebrates at CO2 Seeps in Warm-Temperate Japan.

Japan has many coastal carbon dioxide seeps as it is one of the most volcanically active parts of the world. These shallow seeps do not have the spectacular aggregations of specialist fauna seen in deep-sea vent systems but they do have gradients in seawater carbonate chemistry that are useful as natural analogues of the effects of ocean acidification on marine biodiversity, ecosystem function and fisheries. Here, we compare macroinvertebrate diversity and abundance on rocky habitats at ambient (mean ≤ 410 µatm) and high (mean 971-1484 µatm) levels of seawater pCO2 in the warm-temperate region of Japan, avoiding areas with toxic sulphur or warm-water conditions. We show that although 70% of intertidal taxa and 40% of shallow subtidal taxa were able to tolerate the high CO2 conditions, there was a marked reduction in the abundance of corals, bivalves and gastropods in acidified conditions. A narrower range of filter feeders, grazers, detritivores, scavengers and carnivores were present at high CO2 resulting in a simplified coastal system that was unable to retain the high standing stocks of marine carbon biomass found in ambient conditions. It is clear that cuts in CO2 emissions would reduce the risks of climate change and ocean acidification impacts on marine biodiversity, shellfish production and biomass in the rocky coastal shores of this region.

Understanding coralline algal responses to ocean acidification: Meta-analysis and synthesis.

Ocean acidification (OA) is a major threat to the persistence of biogenic reefs throughout the world's ocean. Coralline algae are comprised of high magnesium calcite and have long been considered one of the most susceptible taxa to the negative impacts of OA. We summarize these impacts and explore the causes of variability in coralline algal responses using a review/qualitative assessment of all relevant literature, meta-analysis, quantitative assessment of critical responses, and a discussion of physiological mechanisms and directions for future research. We find that most coralline algae experienced reduced abundance, calcification rates, recruitment rates, and declines in pH within the site of calcification in laboratory experiments simulating OA or at naturally elevated CO2 sites. There were no other consistent physiological responses of coralline algae to simulated OA (e.g., photo-physiology, mineralogy, and survival). Calcification/growth was the most frequently measured parameters in coralline algal OA research, and our meta-analyses revealed greater declines in seawater pH were associated with significant decreases in calcification in adults and similar but nonsignificant trends for juveniles. Adults from the family Mesophyllumaceae also tended to be more robust to OA, though there was insufficient data to test similar trends for juveniles. OA was the dominant driver in the majority of laboratory experiments where other local or global drivers were assessed. The interaction between OA and any other single driver was often additive, though factors that changed pH at the surface of coralline algae (light, water motion, epiphytes) acted antagonistically or synergistically with OA more than any other drivers. With advances in experimental design and methodological techniques, we now understand that the physiology of coralline algal calcification largely dictates their responses to OA. However, significant challenges still remain, including improving the geographic and life-history spread of research effort and a need for holistic assessments of physiology.

Simplification, not "tropicalization", of temperate marine ecosystems under ocean warming and acidification.

Ocean warming is altering the biogeographical distribution of marine organisms. In the tropics, rising sea surface temperatures are restructuring coral reef communities with sensitive species being lost. At the biogeographical divide between temperate and tropical communities, warming is causing macroalgal forest loss and the spread of tropical corals, fishes and other species, termed "tropicalization". A lack of field research into the combined effects of warming and ocean acidification means there is a gap in our ability to understand and plan for changes in coastal ecosystems. Here, we focus on the tropicalization trajectory of temperate marine ecosystems becoming coral-dominated systems. We conducted field surveys and in situ transplants at natural analogues for present and future conditions under (i) ocean warming and (ii) both ocean warming and acidification at a transition zone between kelp and coral-dominated ecosystems. We show that increased herbivory by warm-water fishes exacerbates kelp forest loss and that ocean acidification negates any benefits of warming for range extending tropical corals growth and physiology at temperate latitudes. Our data show that, as the combined effects of ocean acidification and warming ratchet up, marine coastal ecosystems lose kelp forests but do not gain scleractinian corals. Ocean acidification plus warming leads to overall habitat loss and a shift to simple turf-dominated ecosystems, rather than the complex coral-dominated tropicalized systems often seen with warming alone. Simplification of marine habitats by increased CO2 levels cascades through the ecosystem and could have severe consequences for the provision of goods and services.

Major loss of coralline algal diversity in response to ocean acidification.

Calcified coralline algae are ecologically important in rocky habitats in the marine photic zone worldwide and there is growing concern that ocean acidification will severely impact them. Laboratory studies of these algae in simulated ocean acidification conditions have revealed wide variability in growth, photosynthesis and calcification responses, making it difficult to assess their future biodiversity, abundance and contribution to ecosystem function. Here, we apply molecular systematic tools to assess the impact of natural gradients in seawater carbonate chemistry on the biodiversity of coralline algae in the Mediterranean and the NW Pacific, link this to their evolutionary history and evaluate their potential future biodiversity and abundance. We found a decrease in the taxonomic diversity of coralline algae with increasing acidification with more than half of the species lost in high pCO2 conditions. Sporolithales is the oldest order (Lower Cretaceous) and diversified when ocean chemistry favoured low Mg calcite deposition; it is less diverse today and was the most sensitive to ocean acidification. Corallinales were also reduced in cover and diversity but several species survived at high pCO2 ; it is the most recent order of coralline algae and originated when ocean chemistry favoured aragonite and high Mg calcite deposition. The sharp decline in cover and thickness of coralline algal carbonate deposits at high pCO2 highlighted their lower fitness in response to ocean acidification. Reductions in CO2 emissions are needed to limit the risk of losing coralline algal diversity.

Feedback mechanisms stabilise degraded turf algal systems at a CO2 seep site.

Human activities are rapidly changing the structure and function of coastal marine ecosystems. Large-scale replacement of kelp forests and coral reefs with turf algal mats is resulting in homogenous habitats that have less ecological and human value. Ocean acidification has strong potential to substantially favour turf algae growth, which led us to examine the mechanisms that stabilise turf algal states. Here we show that ocean acidification promotes turf algae over corals and macroalgae, mediating new habitat conditions that create stabilising feedback loops (altered physicochemical environment and microbial community, and an inhibition of recruitment) capable of locking turf systems in place. Such feedbacks help explain why degraded coastal habitats persist after being initially pushed past the tipping point by global and local anthropogenic stressors. An understanding of the mechanisms that stabilise degraded coastal habitats can be incorporated into adaptive management to better protect the contribution of coastal systems to human wellbeing.

Ocean acidification locks algal communities in a species-poor early successional stage.

Long-term exposure to CO2 -enriched waters can considerably alter marine biological community development, often resulting in simplified systems dominated by turf algae that possess reduced biodiversity and low ecological complexity. Current understanding of the underlying processes by which ocean acidification alters biological community development and stability remains limited, making the management of such shifts problematic. Here, we deployed recruitment tiles in reference (pHT 8.137 ± 0.056 SD) and CO2 -enriched conditions (pHT 7.788 ± 0.105 SD) at a volcanic CO2 seep in Japan to assess the underlying processes and patterns of algal community development. We assessed (i) algal community succession in two different seasons (Cooler months: January-July, and warmer months: July-January), (ii) the effects of initial community composition on subsequent community succession (by reciprocally transplanting preestablished communities for a further 6 months), and (iii) the community production of resulting communities, to assess how their functioning was altered (following 12 months recruitment). Settlement tiles became dominated by turf algae under CO2 -enrichment and had lower biomass, diversity and complexity, a pattern consistent across seasons. This locked the community in a species-poor early successional stage. In terms of community functioning, the elevated pCO2 community had greater net community production, but this did not result in increased algal community cover, biomass, biodiversity or structural complexity. Taken together, this shows that both new and established communities become simplified by rising CO2 levels. Our transplant of preestablished communities from enriched CO2 to reference conditions demonstrated their high resilience, since they became indistinguishable from communities maintained entirely in reference conditions. This shows that meaningful reductions in pCO2 can enable the recovery of algal communities. By understanding the ecological processes responsible for driving shifts in community composition, we can better assess how communities are likely to be altered by ocean acidification.

Ervilia castanea (Mollusca, Bivalvia) populations adversely affected at CO2 seeps in the North Atlantic.

Sites with naturally high CO2 conditions provide unique opportunities to forecast the vulnerability of coastal ecosystems to ocean acidification, by studying the biological responses and potential adaptations to this increased environmental variability. In this study, we investigated the bivalve Ervilia castanea in coastal sandy sediments at reference sites and at volcanic CO2 seeps off the Azores, where the pH of bottom waters ranged from average oceanic levels of 8.2, along gradients, down to 6.81, in carbonated seawater at the seeps. The bivalve population structure changed markedly at the seeps. Large individuals became less abundant as seawater CO2 levels rose and were completely absent from the most acidified sites. In contrast, small bivalves were most abundant at the CO2 seeps. We propose that larvae can settle and initially live in high abundances under elevated CO2 levels, but that high rates of post-settlement dispersal and/or mortality occur. Ervilia castanea were susceptible to elevated CO2 levels and these effects were consistently associated with lower food supplies. This raises concerns about the effects of ocean acidification on the brood stock of this species and other bivalve molluscs with similar life history traits.

Fishery reforms for the management of non-indigenous species.

Marine ecosystems are undergoing major transformations due to the establishment and spread of Non-Indigenous Species (NIS). Some of these organisms have adverse effects, for example by reducing biodiversity and causing ecosystem shifts. Others have upsides, such as benefits to fisheries or replacing lost ecological functions and strengthening biogenic complexity. Stopping the spread of NIS is virtually impossible and so the societal challenge is how to limit the socioeconomic, health, and ecological risks, and sustainably exploit the benefits provided by these organisms. We propose a move away from the notion that NIS have only negative effects, and suggest a turn towards an Ecosystem-Based Fishery Management approach for NIS (EBFM-NIS) in the Mediterranean Sea, the world's most invaded marine region. A structured, iterative, and adaptive framework that considers the range of costs and benefits to ecosystems, ecosystem services, and fisheries is set out to determine whether NIS stocks should be managed using sustainable or unsustainable exploitation. We propose fishery reforms such as multiannual plans, annual catch limits, technical measures for sustainable exploitation, and legitimization of unlimited fishing of selected NIS and introduction of a radical new license for NIS fishing for unsustainable exploitation. Depending on local conditions, investment strategies can be included within the EBFM-NIS framework to protect/enhance natural assets to improve ecosystem resilience against NIS, as well as fishery assets to improve the performance of NIS fisheries. Examples of the former include the enhancement of Marine Protected Areas, harvesting of invasive NIS within MPAs, and protection of overfished predators and key species. Examples of the latter include market promotion and valorisation of NIS products, development of novel NIS products, and innovative/alternative NIS fishing such as fishery-related tourism ('pescatourism'). The application of the suggested EBFM-NIS would create jobs, protect and enhance ecosystem services, and help to meet the United Nations Sustainable Development Goal 14: Conserve and sustainably use the oceans, seas, and marine resources for sustainable development.

Ocean acidification alters bacterial communities on marine plastic debris.

The increasing quantity of plastic waste in the ocean is providing a growing and more widespread novel habitat for microbes. Plastics have taxonomically distinct microbial communities (termed the 'Plastisphere') and can raft these unique communities over great distances. In order to understand the Plastisphere properly it will be important to work out how major ocean changes (such as warming, acidification and deoxygenation) are shaping microbial communities on waste plastics in marine environments. Here, we show that common plastic drinking bottles rapidly become colonised by novel biofilm-forming bacterial communities, and that ocean acidification greatly influences the composition of plastic biofilm assemblages. We highlight the potential implications of this community shift in a coastal community exposed to enriched CO2 conditions.

Changes in fish communities due to benthic habitat shifts under ocean acidification conditions.

Ocean acidification will likely change the structure and function of coastal marine ecosystems over coming decades. Volcanic carbon dioxide seeps generate dissolved CO2 and pH gradients that provide realistic insights into the direction and magnitude of these changes. Here, we used fish and benthic community surveys to assess the spatio-temporal dynamics of fish community properties off CO2 seeps in Japan. Adding to previous evidence from ocean acidification ecosystem studies conducted elsewhere, our findings documented shifts from calcified to non-calcified habitats with reduced benthic complexity. In addition, we found that such habitat transition led to decreased diversity of associated fish and to selection of those fish species better adapted to simplified ecosystems dominated by algae. Our data suggest that near-future projected ocean acidification levels will oppose the ongoing range expansion of coral reef-associated fish due to global warming.

They are here to stay: the biology and ecology of lionfish (Pterois miles) in the Mediterranean Sea.

The lionfish, Pterois miles, is one of the most recent Lessepsian immigrants into the Mediterranean Sea, and it poses a serious threat to marine ecosystems in the region. This study assesses the basic biology and ecology of lionfish in the Mediterranean, examining morphometrics, reproduction and diet as well as population structure and distribution. The population density of lionfish has increased dramatically in Cyprus since the first sighting in late 2012; by 2018 aggregations of up to 70 lionfish were found on rocky grounds with complex reefs and artificial reefs in depths of 0-50 m. Lionfish in Cyprus become mature within a year, and adults are capable of spawning year-round, with peak spawning in summer when the sea-surface temperature reaches 28.4°C. The Cypriot lionfish grow faster and bigger than in their native range, and females are more common than males. Lionfish are generalist predators in these waters, as also found in their native range, consuming a range of teleost and crustacean prey, some of which are of high economic value (e.g., Spicara smaris and Sparisoma cretense) or have an important role in local trophic webs (e.g., Chromis chromis). Overall, the reproductive patterns, the presence of juveniles and adults throughout the year, the rapid growth rates and the generalist diet indicate that lionfish are thriving and are now already well established in the region and could potentially become the serious nuisance that they are in their temperate and tropical western Atlantic-invasive range.

Responses of Intertidal Bacterial Biofilm Communities to Increasing pCO2.

The effects of ocean acidification on ecosystems remain poorly understood, because it is difficult to simulate the effects of elevated CO2 on entire marine communities. Natural systems enriched in CO2 are being used to help understand the long-term effects of ocean acidification in situ. Here, we compared biofilm bacterial communities on intertidal cobbles/boulders and bedrock along a seawater CO2 gradient off Japan. Samples sequenced for 16S rRNA showed differences in bacterial communities with different pCO2 and between habitat types. In both habitats, bacterial diversity increased in the acidified conditions. Differences in pCO2 were associated with differences in the relative abundance of the dominant phyla. However, despite the differences in community composition, there was no indication that these changes would be significant for nutrient cycling and ecosystem function. As well as direct effects of seawater chemistry on the biofilm, increased microalgal growth and decreased grazing may contribute to the shift in bacterial composition at high CO2, as documented by other studies. Thus, the effects of changes in bacterial community composition due to globally increasing pCO2 levels require further investigation to assess the implications for marine ecosystem function. However, the apparent lack of functional shifts in biofilms along the pCO2 gradient is a reassuring indicator of stability of their ecosystem functions in shallow ocean margins.

How experimental physiology and ecological niche modelling can inform the management of marine bioinvasions?

Marine bioinvasions are increasing worldwide by a number of factors related to the anthroposphere, such as higher ship traffic, climate change and biotic communities' alterations. Generating information about species with high invasive potential is necessary to inform management decisions aiming to prevent their arrival and spread. Grateloupia turuturu, one of the most harmful invasive macroalgae, is capable of damaging ecosystem functions and services, and causing biodiversity loss. Here we developed an ecological niche model using occurrence and environmental data to infer the potential global distribution of G. turuturu. In addition, ecophysiological experiments were performed with G. turuturu populations from different climatic regions to test predictions regarding invasion risk. Our model results show high suitability in temperate and warm temperate regions around the world, with special highlight to some areas where this species still doesn't occur. Thalli representing a potential temperate region origin, were held at 10, 13, 16, 20 and 24 °C, and measurements of optimal quantum field (Fv/Fm) demonstrated a decrease of photosynthetic yield in the higher temperature. Thalli from the population already established in warm temperate South Atlantic were held at 18, 24 and 30 °C with high and low nutrient conditions. This material exposed to the higher temperature demonstrated a drop in photosynthetic yield and significant reduction of growth rate. The congregation of modelling and physiological approach corroborate the invasive potential of G. turuturu and indicate higher invasion risk in temperate zones. Further discussions regarding management initiatives must be fostered to mitigate anthropogenic transport and eventually promote eradication initiatives in source areas, with special focus in the South America. We propose that this combined approach can be used to assess the potential distribution and establishment of other marine invasive species.

Author Correction: The future of Blue Carbon science.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Biomonitoring acidification using marine gastropods.

Ocean acidification is mainly being monitored using data loggers which currently offer limited coverage of marine ecosystems. Here, we trial the use of gastropod shells to monitor acidification on rocky shores. Animals living in areas with highly variable pH (8.6-5.9) were compared with those from sites with more stable pH (8.6-7.9). Differences in site pH were reflected in size, shape and erosion patterns in Nerita chamaeleon and Planaxis sulcatus. Shells from acidified sites were shorter, more globular and more eroded, with both of these species proving to be good biomonitors. After an assessment of baseline weathering, shell erosion can be used to indicate the level of exposure of organisms to corrosive water, providing a tool for biomonitoring acidification in heterogeneous intertidal systems. A shell erosion ranking system was found to clearly discriminate between acidified and reference sites. Being spatially-extensive, this approach can identify coastal areas of greater or lesser acidification. Cost-effective and simple shell erosion ranking is amenable to citizen science projects and could serve as an early-warning-signal for natural or anthropogenic acidification of coastal waters.