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.

Green Tides Significantly Alter the Molecular Composition and Properties of Coastal DOC and Perform Dissolved Carbon Sequestration.

Despite green tides (or macroalgal blooms) having multiple negative effects, it is thought that they have a positive effect on carbon sequestration, although this aspect is rarely studied. Here, during the world's largest green tide (caused by Ulva prolifera) in the Yellow Sea, the concentration of dissolved organic carbon (DOC) increased by 20-37% in intensive macroalgal areas, and thousands of new molecular formulas rich in CHNO and CHOS were introduced. The DOC molecular species derived from U. prolifera constituted ∼18% of the total DOC molecular species in the seawater of bloom area, indicating the profound effect that green tides have on shaping coastal DOC. In addition, 46% of the macroalgae-derived DOC was labile DOC (LDOC), which had only a short residence time due to rapid microbial utilization. The remaining 54% was recalcitrant DOC (RDOC) rich in humic-like substances, polycyclic aromatics, and highly aromatic compounds that resisted microbial degradation and therefore have the potential to play a role in long-term carbon sequestration. Notably, source analysis showed that in addition to the microbial carbon pump, macroalgae are also an important source of RDOC. The number of RDOC molecular species contributed by macroalgae even exceed (77 vs 23%) that contributed by microorganisms.

Two bloom-forming species of Ulva (Chlorophyta) show different responses to seawater temperature and no antagonistic interaction.

The generalized use of molecular identification tools indicated that multispecific green tides are more common than previously thought. Temporal successions between bloom-forming species on a seasonal basis were also revealed in different cold temperate estuaries, suggesting a key role of photoperiod and temperature controlling bloom development and composition. According to the Intergovernmental Panel on Climate Change, water temperatures are predicted to increase around 4°C by 2100 in Ireland, especially during late spring coinciding with early green tide development. Considering current and predicted temperatures, and photoperiods during bloom development, different eco-physiological experiments were developed. These experiments indicated that the growth of Ulva lacinulata was controlled by temperature, while U. compressa was unresponsive to the photoperiod and temperatures assayed. Considering a scenario of global warming for Irish waters, an earlier development of bloom is expected in the case of U. lacinulata. This could have significant consequences for biomass balance in Irish estuaries and the maximum accumulated biomass during peak bloom. The observed seasonal patterns and experiments also indicated that U. compressa may facilitate U. lacinulata development. When both species were co-cultivated, the culture performance showed intermediate responses to experimental treatments in comparison with monospecific cultures of both species.

Photosynthetic and biochemical traits change in the green-tide-forming macroalga Ulva pertusa during sporulation1.

The physiological and biochemical changes in the green macroalga Ulva pertusa during the progression of sporulation have been characterized. The transition from the vegetative to the sporulation stage was accompanied by an increase in chlorophyll a (Chl a), chlorophyll b (Chl b), and carotenoid content, as well as an increase in DPPH scavenging and responsiveness to diphenylamine. However, oxygen evolution and maximum electron transport rate decreased. The discrepancy between photosynthetic performance and pigment content might relate to the self-shading of spores within a sporangium. Spore-forming U. pertusa thalli were low-light-adapted, due to an increase in the number of photosynthetic units. Decreased electron transport during sporulation might trigger sporulation, as for some cyanobacteria and other Ulva spp., via oxidization of the plastoquinone pool and cyclic phosphorylation, thus producing ATP to generate carbon and nitrogen skeletons required for spores. It is thus concluded that carotenoids function both in spore initiation and/or maturation and in their photoprotection.

Ulva lactuca, A Source of Troubles and Potential Riches.

Ulva lactuca is a green macro alga involved in devastating green tides observed worldwide. These green tides or blooms are a consequence of human activities. Ulva blooms occur mainly in shallow waters and the decomposition of this alga can produce dangerous vapors. Ulva lactuca is a species usually resembling lettuce, but genetic analyses demonstrated that other green algae with tubular phenotypes were U. lactuca clades although previously described as different species or even genera. The capacity for U. lactuca to adopt different phenotypes can be due to environment parameters, such as the degree of water salinity or symbiosis with bacteria. No efficient ways have been discovered to control these green tides, but the Mediterranean seas appear to be protected from blooms, which disappear rapidly in springtime. Ulva contains commercially valuable components, such as bioactive compounds, food or biofuel. The biomass due to this alga collected on beaches every year is beginning to be valorized to produce valuable compounds. This review describes different processes and strategies developed to extract these different valuable components.

'I am an Intensive Guy': The Possibility and Conditions of Reconciliation Through the Ecological Intensification Framework.

The need for better conciliation between food production and environmental protection calls for new conceptual approaches in agronomy. Ecological intensification (EI) is one of the most encouraging and successful conceptual frameworks for designing more sustainable agricultural systems, though relying upon semantic ambivalences and epistemic tensions. This article discusses abilities and limits of the EI framework in the context of strong social and environmental pressure for agricultural transition. The purpose is thus to put EI at stake in the light of the results of an interdisciplinary and participatory research project that explicitly adopted EI goals in livestock semi-industrialized farming systems. Is it possible to maintain livestock production systems that are simultaneously productive, sustainable, and viable and have low nitrate emissions in vulnerable coastal areas? If so, how do local stakeholders use these approaches? The main steps of the innovation process are described. The effects of political and social dynamics on the continuity of the transition process are analyzed, with a reflexive approach. This experiment invites one to consider that making EI operational in a context of socio-technical transition toward agroecology represents system innovation, requiring on-going dialogue, reflexivity, and long-term involvement by researchers.

The ever-lasting green tides: What can we do？.

Macroalgal blooms (Green tides) are occurring more frequently in many regions of the world because of the combined effects of increasingly intense human activity and climate change. In the last decade, the world's largest Ulva prolifera green tide has become a recurrent phenomenon, appearing every summer in the southern Yellow Sea, China. Green tides can hurt coastal tourism and eradicate aquaculture and artisanal fishing. Eutrophication in nearshore waters is the ultimate explanation for the explosive growth of the macroalgal biomass, but the specific course of each nearshore green tide is often complex and requires in-depth and extensive research to develop effective mitigation strategies. Researchers have undertaken extensive studies on the prevention, control and mitigation of large-scale green algal blooms, and felicitated the utilization of green tide harmful biomass through bio-refining, bioconversion and other measures. However, due to the large-scale and trans-regional nature of the green tide, the government's administrative coordination measures are also essential for effective control. Nevertheless, it is becoming increasingly urgent to prevent and control the bloom at the early stage, and efficiently salvage and use these valuable raw materials.

Seasonal dynamics of amino acids in the Southern Yellow Sea: Feedback on the mechanism of green tides caused by Ulva prolifera.

The biogeochemical processes of amino acids in the Southern Yellow Sea (SYS) have become more dynamic under the influence of the world's largest-scale green tide. The potential relationship between amino acids and green tides has not been effectively assessed, despite its critical importance for exploring dissolved organic matter (DOM) cycling processes in marginal seas. In this study, three cruises were conducted to analyze the concentrations and compositions of total hydrolyzed amino acids (THAAs) in the SYS during the spring, summer, and autumn of 2019. The bioavailability potential of DOM was evaluated using the degradation index (DI) and THAA nitrogen normalized yield (THAA (%DON)) (DON as dissolved organic nitrogen). The variation dynamics of amino acid indicators during different stages of green tide were further explored. The results showed that the THAA concentrations and DOM bioavailability in the SYS were considerably influenced by biological processes. The THAA concentrations (0.96 ± 0.34 µmol L-1) exhibited the lowest mean values in the summer, while the DI values (0.106 ± 0.461) and mean THAA (%DON) values (18.20 ± 6.58 %) were the highest during this season. The distribution of amino acid indicators in the summer (the late-tide stage) was regulated by the green tide mechanism, and kept pace with the green tide floating region. In comparison with the waters in south of 35° N, the THAA concentrations and DI values experienced significant seasonal variations (p < 0.05) in north of 35° N, with the highest DI values (1.217) observed in the green tide aggregation area. This indicates the transformation of nutrient sources for Ulva prolifera in the late-tide stage and its impact on DOM bioavailability. Thus, as a potential feedback indicator of green tides, the study of amino acids is meaningful for understanding the occurrence of green tides and the source-sink pattern of organic nitrogen.

A new set of N isotopic reference values for monitoring Ulva green tides in coral reef ecosystems.

Green tides occurrence has increased in coral reefs, yet few reference values have been documented to support bloom management in these ecosystems. Here, we took advantage of recent Ulva green tides that occurred in New Caledonia to (i) identify the elements limiting the growth of Ulva spp. during these blooms; and (ii) validate the use of isotopic markers for identifying sources of nutrients that generated blooms. N/P ratios highlighted a stronger limitation of algae by phosphorus than by nitrogen on sites under oceanic influence, while the proportions of N and P were optimal for algal growth at sites where green tides occurred. Macroalgae highly exposed to sewage water was characterized by higher δ15N than macroalgae collected in areas exposed to synthetic inorganic fertilizers. From these results, we established a new set of threshold values for using δ15N in Ulva species as an indicator of nitrogen source type in coral reefs.

Effective capping of dissolved sulfide generated in Ulva prolifera-rich marine sediments by iron-rich red soil.

Bloom-induced macroalgal enrichment on the seafloor can substantially facilitate dissolved sulfide (DS) production through sulfate reduction. The reaction of DS with sedimentary reactive iron (Fe) is the main mechanism of DS consumption, which however usually could not effectively prevent DS accumulation caused by pulsed macroalgal enrichment. Here we used incubations to investigate the performance of Fe-rich red soil for buffering of DS produced from macroalgae (Ulva prolifera)-enriched sediment. Based on our results, a combination of red soil additions (6.8 kg/m2) before and immediately after pulsed macroalgal deposition (455 g/m2) can effectively cap DS within the red soil layer. The effective DS buffering is mainly due to ample Fe-oxide surface sites available for reaction with DS. Only a small loss (4 %) of buffering capacity after 18-d incubation suggests that the red soil is capable of prolonged DS buffering in macroalgae-enriched sediments.

Evolutionary trends and analysis of the driving factors of Ulva prolifera green tides: A study based on the random forest algorithm and multisource remote sensing images.

Understanding the prolonged spatiotemporal evolution and identifying the underlying causes of Ulva prolifera green tides play pivotal roles in managing such occurrences, restoring water ecology, and fostering sustainable development in marine ecosystems. Satellite remote sensing represents the primary choice for monitoring Ulva prolifera green tides due to its capability for extensive, long-term ocean monitoring. Based on multi-source remote sensing images, ecological and environmental datasets, and machine learning algorithms, therefore, this study focused on "remote sensing modelling - evolution history - change trends - mechanism analysis" to elucidate both the remote sensing monitoring models and the underlying driving factors governing the spatiotemporal evolution of Ulva prolifera green tides in the highly impacted South Yellow Sea of China. With the use of GOCI Ⅰ/Ⅱ images, an hybrid remote sensing extraction model merging the robustness of the random forest (RF) model and the optical algae cloud index (ACI) was established to map Ulva prolifera distribution patterns. The ACI-RF method exhibited exceptional performance, with an F1 score surpassing 0.95, outperforming alternative methods such as the support vector machine (SVM) and K-nearest neighbour (KNN) methods. On the basis, we analysed the evolutionary trends and the driving factors determining these distribution patterns using meteorological data, runoff data, and data on various water quality parameters (SST, ocean current speed, wind speed, precipitation, DO, PAR, Si, NO3-, PO43-and N/P). Over the period from 2011 to 2022, excluding 2021, there was a notable decline in the area of Ulva prolifera green tides, varying between 397 and 2689.9 km2, with an average annual reduction rate of 3%. The maximum annual biomass varied between 0.12 and 15.9 kt. Notably, more than 75% of the area of Ulva prolifera green tides exhibited northward drift, which was significantly influenced by northern currents and wind fields. The analysis of driving factors indicates that factors such as average sea surface temperature, eastward wind speed, northward wind speed, precipitation, PO43- and N/P/Si significantly influence the biological growth rate of Ulva prolifera. Furthermore, coastal land use change and surface runoff, particularly surface runoff in June, significantly impacted the growth rate of Ulva prolifera, with Pearson correlation coefficients of 0.74 and 0.67, respectively. Against the background of global warming and severe deterioration in the marine environment, Ulva prolifera blooms persist. Consequently, two distinct management strategies were proposed based on the distribution patterns and cause analysis results for addressing Ulva prolifera green tides: establishing a continuous protection framework for rivers, lakes, and nearshore areas to mitigate pollutant inputs and implementing precise environmental monitoring measures in urban expansion areas and farmlands to combat overgrowth-induced green tides. This methodology could be applied in other regions affected by marine ecological disasters, and the criteria for selecting influencing factors offer a valuable reference for designing tailored and proactive measures aimed at controlling Ulva prolifera green tides.

Morphological and Molecular Identification of Ulva spp. (Ulvophyceae; Chlorophyta) from Algarrobo Bay, Chile: Understanding the Composition of Green Tides.

Green algae blooms of the genus Ulva are occurring globally and are primarily attributed to anthropogenic factors. At Los Tubos beach in Algarrobo Bay along the central Chilean coast, there have been blooms of these algae that persist almost year-round over the past 20 years, leading to environmental, economic, and social issues that affect the local government and communities. The objective of this study was to characterize the species that form these green tides based on a combination of ecological, morpho-anatomical, and molecular information. For this purpose, seasonal surveys of beached algal fronds were conducted between 2021 and 2022. Subsequently, the sampled algae were analyzed morphologically and phylogenetically using the molecular markers ITS1 and tufA, allowing for the identification of at least five taxa. Of these five taxa, three (U. stenophylloides, U. uncialis, U. australis) have laminar, foliose, and distromatic morphology, while the other two (U. compressa, U. aragoensis) have tubular, filamentous, and monostromatic fronds. Intertidal surveys showed that U. stenophylloides showed the highest relative coverage throughout the seasons and all intertidal levels, followed by U. uncialis. Therefore, we can establish that the green tides on the coast of Algarrobo in Chile are multispecific, with differences in relative abundance during different seasons and across the intertidal zone, opening opportunities for diverse future studies, ranging from ecology to algal biotechnology.

Identification and assessment of the drift velocity of green tides using the maximum cross-correlation method in the Yellow Sea.

The green tides outbreak events seriously threaten the ecological balance of the coastal areas. Quickly and accurately obtaining the spatial distribution and drift state of green tides is key to early warning. Based on Landsat 8 (L8) and Sentinel-2 (S2) image pair, the green tides drift velocity was extracted using the maximum cross-correlation (MCC) method, and windage was calculated by combining ocean current and wind data. The results of the MCC method were validated. Ulva's drift in the Yellow Sea is shaped by both ocean currents and wind, closely aligning with the direction of the currents. Notably, the northward drift velocity of Ulva exhibits a clear boundary around 34°40'N. Windage shows similar characteristics with the Ulva drift velocity, as its values vary with time and space. This study will enhance our comprehension of the dynamic mechanism of green tides drift.

Influences of environmental factors on the dissipation of green tides in the Yellow Sea, China.

Green tides attack the Yellow Sea every year since 2007 and have caused substantial financial loss. Based on Haiyang-1C/Coastal zone imager (HY-1C/CZI) and Terra/MODIS satellite images, the temporal and spatial distribution of green tides floating in the Yellow Sea during 2019 was extracted. The relationships between the growth rate of the green tides and the environmental factors including sea surface temperature (SST), photosynthetically active radiation (PAR), sea surface salinity (SSS), nitrate and phosphate during the green tides' dissipation phase has been detected. Based on the maximum likelihood estimation, a regression model that includes SST, PAR and phosphate was recommended to predict the growth rate of the green tides in the dissipation phase (R2 = 0.63), and this model was also examined using Bayesian information criterion and Akaike information criterion. When the average SST in the study area was above 23.6 °C, the coverage of green tides began to decrease with the increase in temperature under the influence of PAR. The growth rate of the green tides was related to SST (R = -0.38), PAR (R = -0.67) and phosphate (R = 0.40) in the dissipation phase. Compared with HY-1C/CZI, the green tide area extracted using Terra/MODIS tended to be underestimated when the green tide patches were smaller than 11.2 km2. Otherwise, the lower spatial resolution of MODIS resulted in larger mixed pixels of water and algae, which would overestimate the total area of the green tides.

Estimating Ulva prolifera green tides of the Yellow Sea through ConvLSTM data fusion.

Green tides, a worldwide problem, are harmful to aquaculture, tourism, marine ecosystems, and maritime traffic. Currently, green tide detection relies on remote sensing (RS) images, which are often missing or unusable. Thus, the observation and detection of green tides cannot be performed daily, which makes it difficult to improve environmental quality and ecological health. To address this problem, this study proposed a novel green tide estimation framework (GTEF) through convolutional long short-term memory, which learned the historical spatial-temporal seasonal and trend patterns of green tides from 2008 to 2021 and fused the previously observed or estimated data and biological (optional) and physical (optional) data over the preceding seven days when RS images were absent or unusable for daily observation and detection tasks. The results showed that the overall accuracy (OA), false-alarm rating (FAR), and missing-alarm rating (MAR) of the GTEF were 0.9592 ± 0.0375, 0.0885 ± 0.1877 and 0.4315 ± 0.2848, respectively. The estimated results described the green tides in terms of attributes, geometry and position features. Especially in the latitudinal features, the Pearson correlation coefficient of the predicted data and observed data were over 0.8 (P < 0.05), which showed a strong correlation. In addition, this study also discussed the role of biological and physical factors in the GTEF. Sea surface salinity may be the dominant factor in the early stages of green tides; in the late stage, solar irradiance may be the dominant factor. Sea surface winds and sea surface currents also played a significant role in green tide estimation. Results showed the OA, FAR and MAR of the GTEF which, with physical factors but without biological factors, were 0.9556 ± 0.0389, 0.1311 ± 0.3338 and 0.4297 ± 0.3180, respectively. In short, the proposed approach could generate a daily map of green tides, even if RS images were missing or unusable.

Differential responses of bloom-forming Ulva intestinalis and economically important Gracilariopsis lemaneiformis to marine heatwaves under changing nitrate conditions.

Marine heatwaves (MHWs) are affecting the survival of macroalgae. However, little is known regarding how the impacts of MHWs are regulated by nitrogen availability. In this study, we investigated the physiological and genetic responses of a green-tide macroalga Ulva intestinalis Linnaeus and a commercially cultivated macroalga Gracilariopsis lemaneiformis (Bory) E.Y. Dawson, Acleto & Foldvik under different nitrate conditions to simulated MHWs. Under nitrogen limited conditions (LN), heatwaves did not significantly affect biomass or Fv/Fm of U. intestinalis although it led to an earlier biomass decline due to more reproduction events, and meanwhile an upregulation in genes related to TCA cycle and oxidative phosphorylation was detected, supporting sporulation. Under nitrogen replete conditions (HN), heatwaves did not change biomass, Fv/Fm or photosynthetic pigments but reduced reproduction rate along with insignificant change of oxidative phosphorylation and TCA cycle related genes. Meanwhile, genes related to photosynthesis and glutathione metabolism were upregulated. Regarding G. lemaneiformis, heatwaves reduced its Fv/Fm and photosynthetic pigments content, leading to bleaching and death, and photosynthesis-related genes were also downregulated at LN. Fv/Fm was improved and photosynthesis-related genes were up-regulated by the combination of nitrogen enrichment and heatwaves, whereas G. lemaneiformis remained bleached and died by day 12. Therefore, U. intestinalis could survive heatwaves through shifting to micropropagules at LN and protecting its photosynthesis at HN. In contrast, G. lemaneiformis died of bleaching when suffering heatwaves regardless of nitrogen availability. These findings suggest that in future oceans with eutrophication and MHWs, the harmful alga U. intestinalis may have more advantages over the economic alga G. lemaneiformis.

Integrated biotechnology to mitigate green tides.

Around the world, green tides are happening with increasing frequency because of the dual effects of increasingly intense human activity and climate change; this leads to significant impacts on marine ecology and economies. In the last decade, the world's largest green tide, which is formed by Ulva/Enteromorpha porifera, has become a recurrent phenomenon every year in the southern Yellow Sea (China), and it has been getting worse. To alleviate the impacts of such green tide outbreaks, multiple measures need to be developed. Among these approaches, biotechnology plays important roles in revealing the outbreak mechanism (e.g., molecular identification technology for algal genotypes), controlling and preventing outbreaks at the origin sites (e.g., technology to inhibit propagation), and utilizing valuable algal biomass. This review focuses on the various previously used biotechnological approaches that may be applicable to worldwide seaweed blooms that result from global climate change and environmental degradation.

Corrigendum: Assessing Herbivorous Impacts of Apohyale sp. on the Ulva prolifera Green Tide in China.

[This corrects the article DOI: 10.3389/fpls.2021.795560.].

Controlling the main source of green tides in the Yellow Sea through the method of biological competition.

Macroalgal blooms have become a serious threat to public health, fisheries, ecosystems, and global economies. Since 2007, in the Yellow Sea, China, Ulva green tides have occurred for 15 consecutive years. However, effective control methods are limited. Ulva prolifera attached to Neopyropia aquaculture rafts are believed to be the main source of blooms, therefore eliminating Ulva from rafts could effectively prevent and control blooms. We investigated this phenomenon and showed that macroalgae germination was significantly inhibited by dried Neopyropia yezoensis at concentrations of 1.2, 2.4, and 4.8 g DW-1. Also, the inhibitory effects of dried N. yezoensis toward U. prolifera gametes at 2.4 and 4.8 g DW-1 were >90% at day 21. N. yezoensis culture filtrates and thalli were also used to determine dose-dependent inhibition effects on U. prolifera gamete germination. Both were potent and significantly inhibited germination at 1.75-7 g FW-1; the inhibitory effect 7 g FW-1 was >90% at day 21. As N. yezoensis thalli exhibited high inhibitory effects in laboratory experiments, we also performed field studies. N. yezoensis on ropes displayed high inhibitory effects on Ulva attachment and growth. Thus N. yezoensis powder, culture filtrates, and thalli displayed strong inhibitory effects on U. prolifera gametes, suggesting N. yezoensis attachment to ropes could be used to control green tides at the source.

Assessing Herbivorous Impacts of Apohale sp. on the Ulva prolifera Green Tide in China.

An epiphytic gammarid species, Apohyale sp. , was abundant in the floating Ulva prolifera (U. prolifera), which forms large-scale green tides in the Yellow Sea (YSGT). Field observation and laboratory experiments were subsequently conducted to study the species identity, abundance, and grazing effects on the floating algal biomass. The abundance of Apohyale sp. showed great spatial variation and varied from 0.03 to 1.47 inds g-1 in the YSGT. In average, each gram of Apohyale sp. body mass can consume 0.43 and 0.60 g algal mass of U. prolifera per day, and the grazing rates varied among the algae cultured with different nutritional seawaters. It was estimated that grazing of Apohale sp. could efficiently reduce ~0.4 and 16.6% of the algal growth rates in Rudong and Qingdao, respectively. The U. prolifera fragments resulting from gnawing of Apohyale sp. had a higher growth rate and similar photosynthetic activities compared to the floating algae, indicating probably positive feedback on the floating algal biomass. This research corroborated the significant impact of Apohyale sp. on the floating algal mass of YSGT through the top-down control. However, further research is needed to understand the population dynamics of these primary predators and hence their correlation with the expansion or decline of YSGT, especially under the complex food webs in the southern Yellow Sea.